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Contents lists available at ScienceDirect

Neuroscience Research journal homepage: www.elsevier.com/locate/neures

Review article

The cortical motor system of the marmoset monkey (Callithrix jacchus) Sophia Bakola a,b,∗ , Kathleen J. Burman a , Marcello G.P. Rosa a,b a b

Department of Physiology, Monash University, Clayton, VIC 3800, Australia Australian Research Council Centre of Excellence for Integrative Brain Function, Monash University Node, Clayton, VIC 3800, Australia

a r t i c l e

i n f o

Article history: Received 19 September 2014 Received in revised form 14 October 2014 Accepted 14 October 2014 Available online xxx Keywords: Premotor Parietal Connectivity Evolution Motor control

a b s t r a c t Precise descriptions of the anatomical pathways that link different areas of the cerebral cortex are essential to the understanding of the sensorimotor and association processes that underlie human actions, and their impairment in pathological situations. Many years of research in macaque monkeys have critically shaped how we currently think about cortical motor function in humans. However, it is important to obtain additional understanding about the homologies between cortical areas in human and various non-human primates, and in particular how evolutionary changes in connectivity within specific neural circuits impact on the capacity for different behaviors. Current research has converged on the New World marmoset monkey as an important animal model for cortical function and dysfunction, emphasizing advantages unique to this species. However, the motor repertoire of the marmoset differs from that of the macaque in many ways, including the capacity for skilled use of the hands. Here, we review current knowledge about the cortical frontal areas in marmosets, which are key to the generation and control of motor behaviors, with focus on comparative analyses. We note significant parallels with the macaque monkey, as well as a few potentially important differences, which suggest future directions for work involving architectonic and functional analyses. © 2014 Elsevier Ireland Ltd and the Japan Neuroscience Society. All rights reserved.

Contents 1. 2. 3.

4.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Organization of marmoset motor areas . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Cortical connections . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Motor inputs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. 3.2. Somatosensory inputs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3. Posterior parietal inputs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4. Posterior medial inputs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.5. Prefrontal inputs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.6. Inputs to area 8C . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Comparative considerations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction Marmosets are small New World monkeys, which diverged from other members of the primate radiation over 30 million years ago (Purvis et al., 1995). Members of the Callitrichid family (marmosets

∗ Corresponding author at: Department of Physiology, Monash University, Clayton, VIC 3800, Australia. Tel.: +61 3 990 59213. E-mail address: sofi[email protected] (S. Bakola).

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and tamarins) have interesting morphological adaptations, such as small body size and claw-like nails that allow them to cling to vertical tree surfaces (Sussman and Kinzey, 1984). Unlike Old World and some New World monkeys, marmosets do not have the ability to move all their digits independently, and thus have limited capacity to exert fine control of their hand movements. As for other species of simian primate, the marmoset cortex contains a large number of areas, which can be defined on the basis of cytoarchitectural, myeloarchitectural, and chemoarchitectural criteria. According to a recent review (Paxinos et al., 2012), the

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Please cite this article in press as: Bakola, S., et al., The cortical motor system of the marmoset monkey (Callithrix jacchus). Neurosci. Res. (2014), http://dx.doi.org/10.1016/j.neures.2014.11.003

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of digit movements (Lemon et al., 2004; Lemon and Griffiths, 2005). Interestingly, the dexterous New World Cebus monkey has also developed a direct descending pathway to the spinal motoneurons; however, this is not seen in other New World monkeys, which have limited independent finger control (Shriver and Matzke, 1965; Bortoff and Strick, 1993). Therefore, knowledge of similarities and differences between specific areas and pathways is instrumental in interpreting the motor abilities of a species. Here, we asked how the modifications in the marmoset motor apparatus are reflected in cortical motor connectivity, particularly when compared to other primate species. Considering the increasing use of marmosets in studies of motor function and dysfunction (Marshall and Ridley, 2003; Fouad et al., 2004; Virley et al., 2004; Freret et al., 2008; Yamane et al., 2010; Konomi et al., 2012; Maggi et al., 2014; Pohlmeyer et al., 2014), a detailed examination of the circuits subserving motor control is timely.

2. Organization of marmoset motor areas

Fig. 1. Architectonic subdivisions of marmoset (top; based on Paxinos et al., 2012) and macaque (bottom; based on Barbas and Pandya, 1987) caudal frontal lobe. Areas included in the present analyses are shown in color. Sulci: as, arcuate; cs, central; ips, intraparietal; ls, lateral; ps, principal; sp, arcuate spur; sts, superior temporal. Brains are approximately to scale. Scale bar = 1 cm. Abbreviations of areas: 4C, area 4 caudal; 6DC, area 6 dorsocaudal; 6DR, area 6 dorsorostral; 6M, area 6 medial; 6Va, area 6 subdivision a; 6Vb, area 6 subdivision b; 8, prefrontal area 8; 8C, prefrontal area 8 caudal; M1, primary motor cortex.

histological evidence suggests that most, if not all of these areas have counterparts in larger species of monkey, such as macaques. At the same time, it is also important to recognize that validation of the proposed homologies, based on anatomical connectivity and functional properties, is still lacking in many cases. Studies of selected areas of the sensory (Krubitzer and Kaas, 1990; Rosa and Tweedale, 2000; e.g., Huffman and Krubitzer, 2001; Qi et al., 2002; Rosa et al., 2005; de la Mothe et al., 2006; Palmer and Rosa, 2006a,b; Iyengar et al., 2007; Reser et al., 2009; Rosa et al., 2009; for a recent review, see Solomon and Rosa, 2014) and prefrontal (Burman et al., 2006, 2011; Roberts et al., 2007; Burman and Rosa, 2009; Reser et al., 2013) cortex have revealed essential similarities between marmosets and other species of monkey used in neuroscience research, and clarified homologies. However, much still needs to be accomplished before we can be in a position to confidently extrapolate results across different species of non-human primate, and humans. One field of investigation that has seen rapid progress in recent years is the organization of the cortical motor system (Fig. 1), which is the focus of the present review. Similar to other primates, marmosets have a primary motor cortex (M1), defined as a single functional field that contains a complete topographic representation of the body musculature (Burish et al., 2008; Burman et al., 2008). Within the marmoset M1 forelimb region, the representation of distal finger movements is rather restricted, a condition that characterizes many species of New World monkey (Gould et al., 1986; Donoghue et al., 1992; Stepniewska et al., 1993; Dancause et al., 2006). In contrast, larger species of monkey, including macaques (Kwan et al., 1978; Godschalk et al., 1995) and Cebus monkeys (Dum and Strick, 2005), appear to have a larger motor territory devoted to individual finger musculature, which is one of the factors that enables more sophisticated hand use in these species (Padberg et al., 2007). Macaques and, to greater extent, humans have also developed monosynaptic corticospinal connections to the ventral horn motoneuron pools representing the hand and forearm, thereby allowing fine control

Although M1 is often equated to Brodmann’s area 4, this functional field (defined as a complete representation of the body skeletal musculature) is architecturally heterogeneous. In particular, based on mediolateral variations in the size of layer 5 pyramidal neurons, marmoset M1 is composed of 3 architectural divisions (Burman et al., 2008, 2014a; fields 4a/b and 4c of Paxinos et al., 2012), similar to that of other primates (Watanabe-Sawaguchi et al., 1991). As shown in Fig. 1, the cortex rostral to M1 in the marmoset contains a number of histological subdivisions, which have been hypothesized to correspond to the medial, dorsal, and ventral premotor areas (6M, 6D, 6V, respectively) of macaques (Barbas and Pandya, 1987; Wise et al., 1997; Geyer et al., 2000). The dorsal premotor region differentiates in caudal (6DC) and rostral (6DR) areas, which show many similarities with areas F2 and F7 of the macaque, respectively (Matelli et al., 1985). The rostral sector of macaque F7 is likely to contain a supplementary eye field (Schlag and SchlagRey, 1987), and a similar organization has been proposed in the marmoset (Burman et al., 2014b). The ventral premotor cortex of the marmoset has also been further divided into caudomedial and rostrolateral architectural subdivisions (6Va and 6Vb, Burman et al., 2006), in agreement with designations first proposed in the macaque (Barbas and Pandya, 1987; Preuss and Goldman-Rakic, 1991). Alternative schemes have been proposed for the macaque ventral premotor cortex (area F4 and subfields of area F5, Matelli et al., 1985; Belmalih et al., 2009), but the exact relationship of the resultant areas with marmoset areas 6Va and 6Vb is yet to be determined. In other New World monkeys, evidence for ventral premotor subdivisions is largely lacking (Dum and Strick, 2005; Stepniewska et al., 2006), with the exception of a rostral field, possibly a homolog of anterior area F5 (Dancause et al., 2008; Gerbella et al., 2011). In macaques, the medial premotor cortex has been divided into caudal and rostral parts (SMA proper/F3 and pre-SMA/F6, respectively, Luppino et al., 1991; Matelli et al., 1991; Tanji and Shima, 1994). The pre-SMA has distinct anatomical features and privileged connections with prefrontal and non-motor areas (Bates and Goldman-Rakic, 1993; Luppino et al., 1993; Lu et al., 1994). Similar to SMA, pre-SMA engages in motor acts but becomes activated at more abstract levels, for example, during the temporal coding of sequential behavior (Tanji, 1996; Picard and Strick, 2001; Ashe et al., 2006). Functional subdivision of marmoset area 6M is suggested by anatomical data (Burman et al., 2014a,b; see below). In marmosets, a wedge-like field with pronounced myelination inserts between the dorsal and ventral premotor cortices; this has recently been designated as area 8C (Paxinos et al., 2012), but

Please cite this article in press as: Bakola, S., et al., The cortical motor system of the marmoset monkey (Callithrix jacchus). Neurosci. Res. (2014), http://dx.doi.org/10.1016/j.neures.2014.11.003

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comparable descriptions in other species are lacking. Area 8C was originally designated as part of the dorsal premotor cortex, on the basis of its cytoarchitectonic appearance (6d*, Burman et al., 2006). Based on location, area 8C could be contained within the region designated as area 4C in the macaque, which appears to be related to the head and face representations (Barbas and Pandya, 1987; Lewis and Van Essen, 2000). A heavily myelinated field has been illustrated in a corresponding location in the human brain, in front of the motor cortex, but no other relevant information has been provided (Sereno and Huang, 2014). This region may also be the equivalent of the polysensory (visual/somatosensory/auditory) zone of the macaque ventral premotor cortex (Rizzolatti et al., 1981b; Graziano and Gandhi, 2000), and be engaged in the analysis of peripersonal space. In macaques, the medial aspect of the cerebral hemisphere contains additional motor fields, largely within cingulate area 24 (Muakkassa and Strick, 1979; Hutchins et al., 1988; Luppino et al., 1991; Nakano et al., 1992; Galea and Darian-Smith, 1994; He et al., 1995). Anatomical observations suggest that the marmoset anterior medial wall also contains subdivisions of area 24 (Burman and Rosa, 2009). The medial fields of the anterior cingulate cortex are likely to provide cognitive, emotional, and motivational influences on motor function (Vogt et al., 1992; Devinsky et al., 1995; Shima and Tanji, 1998; Kuwabara et al., 2014), through divergent projections to sensorimotor, prefrontal, and limbic areas. Tentative homologies between parts of area 24 and the motor fields have been proposed in the marmoset (Burman et al., 2014a), largely based on the somatotopy of connections; however, physiological evidence is still lacking. 3. Cortical connections We studied the cortical pattern of projections to M1 and various premotor areas by placing small retrograde tracer injections at several locations in these areas, guided by previous functional observations (Burish et al., 2008; Burman et al., 2008). The following description of projections to the motor fields is based on recognized architectonic parcellations of the marmoset cortex, as presented in the recent atlas of the marmoset brain (Paxinos et al., 2012). However, it is important to keep in mind that the proposed parcellation scheme is far from complete, given that much of the marmoset cortex, particularly beyond the primary sensory areas, remains unexplored, and that several subdivisions reported in the macaque, particularly in association cortex, have not yet been formally identified in the marmoset. At the same time, even in macaques, which constitute the most-studied primate species to date, parcellation schemes are often revised or expanded to incorporate scientific updates (e.g., Kobayashi and Amaral, 2000; Luppino et al., 2005; Petrides, 2005; Belmalih et al., 2009; Gerbella et al., 2011). 3.1. Motor inputs Interconnections among frontal motor areas vary, in terms of both areas of origin, and relative numerical strength (Burman et al., 2014a,b,c; Table 1, Figs. 2 and 3). These basic facts, which have been highlighted by previous studies in other species of primate (Jones et al., 1978; Barbas and Mesulam, 1981; Leichnetz, 1986; Barbas and Pandya, 1987; Ghosh et al., 1987; Kurata, 1991; Ghosh and Gattera, 1995; Hatanaka et al., 2001; Rizzolatti and Luppino, 2001; Dancause et al., 2006; Stepniewska et al., 2006; Gharbawie et al., 2011a,b) also apply to the marmoset. Projections to marmoset M1 (Table 1; Fig. 2, left) originate in medial (6M) and caudal premotor areas (6DC and 6V), whereas areas 6DR and 8C contribute sparser inputs (Burman et al., 2014a); connections of M1 with premotor areas are reciprocal (Burman

3

Table 1 Average percentages of extrinsic labeled cells after injections in M1 and premotor areas. Illustrated are cortical areas that contained ≥1% of labeled neurons. Cortical areas have been grouped according to their anatomical location.

46 12 45 8b 8aD 8aV Total prefrontal PrCO 6M 6DR 6DC 8C 6Va 6Vb M1 24 a-d Total motor

6DR

6DC

1.1 1.3 0.1 11.8 7.2 1.2 23.5

0.1 0.0 0.0 0.1 0.1 0.0 0.3

8C 3.9 5.8 4.3 0.5 0.2 11.6 26.2

6Va 1.9 2.5 1.0 0.3 0.1 0.5 7.2

M1 0.0 0.0 0.0 0.0 0.0 0.1 0.3

0.2 9.2

0.1 22.0 9.1

0.2 2.9 4.2 8.0

2.4 2.1 0.7 2.3 2.6

0.0 9.8 0.3 7.6 2.2 2.6 0.3

6.7 4.3 1.1 0.2 0.1 1.1 22.7

1.4 0.8 0.2 18.9 3.9 56.5

7.2 5.5 0.2 0.5 28.6

6.9 10.5 0.7 28.3

7.9 30.8

3a 3b 1/2 S2 complex Total somatosensory

0.0 0.0 0.0 0.7 1.0

0.7 0.4 9.8 2.0 13.1

0.3 0.0 0.0 6.9 7.5

7.3 1.7 11.7 21.1 42.6

15.5 7.1 9.4 5.1 38.0

PE PEC MIP Total PP dorsal

2.5 0.5 1.9 5.1

21.7 1.2 0.1 23.0

5.3 2.3 0.2 7.9

2.9 0.0 0.0 2.9

20.5 0.3 0.0 21.0

PF/PFG PG/OPt AIP LIP VIP Total PP ventral

1.2 2.4 1.4 6.6 1.2 12.8

1.8 0.0 0.0 0.0 0.1 1.9

14.9 0.6 1.0 0.0 0.2 16.7

16.2 0.0 0.0 0.0 0.0 16.2

3.8 0.1 0.1 0.0 0.0 4.0

23a-c 29/30 PGM 31 Total posterior medial

13.5 5.7 4.9 4.6 29.6

1.9 0.1 0.0 3.0 5.0

0.8 0.6 0.5 3.2 5.1

0.3 0.0 0.0 0.0 0.3

4.3 0.1 0.0 1.0 5.5

MST TE/TEO Total temporal

0.4 1.2 3.9

0.1 0.0 0.4

3.9 0.5 6.6

0.4 0.9 2.6

0.1 0.0 1.0

Total visual

1.3

0.0

1.0

0.1

0.0

Abbreviations: PEC, posterior parietal area PE caudal; PG/OPt, ventral parietal areas PG/OPt; PP, posterior parietal; TE/TEO, inferior temporal areas TE/TEO. Other abbreviations as in Figs. 1–3 (see also text).

et al., 2014b,c; Table 1). To some extent, variations in the exact composition of inputs to different parts of M1 also reflect its topographic organization, with specific emphases on connections to the regions of head, forelimb and trunk/hindlimb musculature representations (Burman et al., 2014a). For instance, dense connections between lateral M1 and ventral premotor area 6Va in the marmoset might reflect components of a cortical circuit related to orofacial and head movements (Burman et al., 2008, 2014c), as suggested previously in macaques (Matelli et al., 1986; Tokuno et al., 1997). Caudal areas 6DC and 6Va (Fig. 2, right) each receive major inputs from one of the rostral premotor areas (6DR and 6Vb, respectively), and interconnections between areas 6DC and 6Va are relatively limited (in agreement with reports on the organization of the macaque cortex; Kurata, 1991; Ghosh and Gattera, 1995). These findings suggest a dorsoventral functional segregation that mainly reflects the use of different body parts (Stepniewska et al., 2006; Graziano and Aflalo, 2007). As noted above, cytoarchitectural area 6M in the marmoset is likely to contain at least two functional areas, equivalent to SMA

Please cite this article in press as: Bakola, S., et al., The cortical motor system of the marmoset monkey (Callithrix jacchus). Neurosci. Res. (2014), http://dx.doi.org/10.1016/j.neures.2014.11.003

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4

Fig. 2. Schematic diagram of the major (≥3%) connections of M1 (left) and of the dorsal and ventral premotor areas, 6DC (orange) and 6Va (magenta) (right). The strength of connections is illustrated by different arrow widths (≥3–>10%, ≥10–>20%, ≥20%). Borders of cortical areas, shown on the lateral (bottom) and medial (top) views of a marmoset brain, according to Paxinos et al. (2012). Abbreviations of areas: 1/2, 3a, 3b, anterior parietal areas 1 and 2, 3a, 3b; 23, 24, 31, medial areas 23, 24, 31; PE, PF/PFG, posterior parietal areas PE, PF/PFG; S2, second somatosensory cortex (including areas S2 proper and PV). Other details as in Fig. 1 and Table 1. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

and pre-SMA. In general, area 6M forms substantial projections to M1 and all of the subdivisions of the premotor cortex so far explored (6DC, 6DR, and 6Va; Table 1). Projections to area 6DR (Fig. 3) originate primarily in the rostral part of area 6M, and might be contained within the territory likely to include the pre-SMA or area F6 (Burman et al., 2014b), reflecting observations in the macaque (Luppino et al., 1993). In contrast, projections from area 6M to other premotor areas also originate caudally, in the region likely to represent the homolog of SMA (Burman et al., 2014a,b,c). A final set of frontal projections, originating in subfields of medial area 24, targets mainly M1 and 6DC (Burman et al., 2014a,b; Table 1); similar findings have been reported for macaques (Luppino et al., 2003; Morecraft et al., 2012). These medial fields are likely to correspond to the cingulate motor fields CMAd and CMAr (Dum and Strick, 2002), and to contribute to the control of meaningful, goal-directed movements, such as reaching, grasping, and defensive movements (Gharbawie et al., 2011a). 3.2. Somatosensory inputs As in macaques (Nelson et al., 1980; Krubitzer et al., 2004), the cortex immediately posterior to M1 relates to the somatosensory domain, and contains 2 cytoarchitectural fields (areas 3a and 3b) with systematic arrangements of contralateral body parts (Krubitzer and Kaas, 1990; Huffman and Krubitzer, 2001). Two additional representations caudal to 3b have been described in some New World monkey species (Merzenich et al., 1978; Sur et al., 1982; Felleman et al., 1983), corresponding to macaque areas 1 and 2 (Pons et al., 1985; Taoka et al., 1998, 2000). In the Callitrichid family, limited evidence shows that cortex posterior to area 3b does not differentiate architectonically in areas 1 and 2, and that

responses to low-threshold somatic stimulation are rare (Carlson et al., 1986; Coq et al., 2004; Padberg et al., 2005); the designation “area 1/2” for this region (Krubitzer and Calford, 1992; Paxinos et al., 2012) emphasizes the ambiguity. In these species, the simpler cortical organization is reflected in the simpler morphology and limited dexterity of the hand (Padberg et al., 2007). Additional representations of the cutaneous receptors of the skin have been described along the dorsal bank of the lateral sulcus in marmosets (S2 and the parietal ventral area, PV; Krubitzer and Kaas, 1990), similar to the macaque scheme (Robinson and Burton, 1980; Krubitzer et al., 1995); the S2 complex of areas forms part of a cortical network related to tactile discriminations and memories (Murray and Mishkin, 1984; Friedman et al., 1986; Disbrow et al., 2003). The origin of somatosensory projections to marmoset M1 is particularly widespread, originating in all subdivisions of anterior and lateral somatosensory areas (Fig. 2 and Table 1). Comparisons with published maps in various species (Merzenich et al., 1978; Nelson et al., 1980; Sur et al., 1982; Carlson et al., 1986; Ghosh et al., 1987; Jain et al., 2001) suggest that somatic input from the anterior parietal fields is topographically organized, at least within large sectors of the body. In macaques, cutaneous information from area 3b preferentially targets the caudal part of M1, which is richer in distal representations (Huerta and Pons, 1990; Burton et al., 1995). A similar trend is not readily evident in the marmoset, although more detailed studies are required. The same somatosensory areas target ventral premotor area 6Va, although emphasis is markedly shifted toward S2 (Burman et al., 2014c; Table 1 and Fig. 2, right). In general, area 6Va connects with the forelimb and face representations of the somatosensory areas, as in macaques (Friedman et al., 1980; Cipolloni and Pandya, 1999; Disbrow et al., 2003), and could relay information for the

Please cite this article in press as: Bakola, S., et al., The cortical motor system of the marmoset monkey (Callithrix jacchus). Neurosci. Res. (2014), http://dx.doi.org/10.1016/j.neures.2014.11.003

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Fig. 3. Schematic diagram of the major (≥3%) connections of areas 6DR (red) and 8C (green). Abbreviations of areas: 8b, 8aD, 8aV, prefrontal areas 8b, 8a dorsal, 8a ventral; 12, 45, 46, prefrontal areas 12, 45, 46; 29/30, retrosplenial areas 29/30; LIP, lateral intraparietal area; MST, medial superior temporal area; PGM, parietal area PG medial. Other details as in Figs. 1 and 2. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

guidance of arm and mouth actions in peripersonal space, in agreement with the role of the macaque ventral premotor cortex (Fogassi et al., 1996; Graziano et al., 1997; Maranesi et al., 2012). Compared to area 6Va, dorsal premotor area 6DC receives more modest somatosensory projections (Table 1). The main exception is area 1/2, which also provides a robust connection to area 6DC, originating primarily from its putative forelimb representation. 3.3. Posterior parietal inputs Quite substantial input to M1 originates in the parietal lobe, largely within the territory of the single architectonic field PE as defined by Paxinos et al. (2012). Parietal projections are particularly dense to medial and intermediate parts of M1, related to limb control (Burman et al., 2014a). In contrast, projections to orofacial M1 sites are generally weak, and originate from ventral parts of PE as well as from area PF; a similar trend is evident in Old World primates (Künzle, 1978; Gharbawie et al., 2011b). Posterior parietal inputs to marmoset premotor cortex originate across a large region, which encompasses both cytoarchitectural area 5 and area 7 of the Brodmann scheme (Burman et al., 2014b,c). Following the anatomical trend described for the macaque, each premotor area in marmosets receives its primary posterior parietal projections from a specific region. Thus, area 6DC receives the majority of its projections from dorsal parietal areas (including, in particular, area PE of the nomenclature proposed by Paxinos et al., 2012), whereas the major projections to area 6Va originate in rostroventral parietal areas (PF/PFG). Parietal projections to rostral premotor area 6DR originate in all of the putative homologs of the intraparietal areas (i.e., anterior, lateral, medial, ventral areas, AIP, LIP, MIP, VIP, respectively; note that in the marmoset these areas

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are located on the surface of the parietal lobe), as well as in ventral posterior parietal areas. However, the largest concentration of projecting neurons originates in LIP (Table 1; Fig. 3). The definition of intraparietal area LIP in marmosets is currently limited to architectonic observations (Paxinos et al., 2012) and connections with dorsal visual stream areas (Rosa et al., 2009); in addition, large visual receptive fields have been recorded in this region (Rosa and Schmid, 1995). In Old World monkeys, projections from lateral posterior parietal cortex to the 6DR homolog (F7) do not appear to be as prominent, except for an LIP input to the part of F7 that contains an oculomotor field (Matelli et al., 1998). Based on functional studies in the macaque, the information relayed from “intraparietal” cortex to marmoset 6DR is likely related to spatial aspects of behavior, including visual attention and directing gaze shifts, and to visually guided arm movements to peripersonal space (Andersen and Buneo, 2002; Grefkes and Fink, 2005; Gottlieb, 2007). In macaques, parallel parietofrontal streams have been described (Petrides and Pandya, 1984; Marconi et al., 2001; TanneGariepy et al., 2002; Rozzi et al., 2006; Gamberini et al., 2009; Bakola et al., 2010, 2013), which have been proposed to be linked to particular aspects of movement (Kalaska et al., 1997; Matelli et al., 1998; Culham and Kanwisher, 2001; Gregoriou and Savaki, 2003; Caminiti et al., 2010). Although the evidence in New World monkeys also points to a similar segregation (for a recent discussion, see Stepniewska et al., 2014), the boundaries and connectivity patterns of most parietal areas in these species remain largely unexplored, and may be refined as knowledge of the parietal cortex evolves. Indeed, preliminary investigations in the marmoset show that the prominence of projections to premotor cortex changes along the caudorostral axis of the parietal cortex (Burman et al., 2008), reminiscent of the macaque condition. Future anatomical and physiological research, including injections in the various proposed subdivisions and recording studies in awake-behaving preparations, will be necessary to clarify the boundaries of the homologs of intraparietal areas in marmosets. It remains to be determined if the described species differences simply reflect the inexact knowledge about the boundaries of homologs of these areas in the marmoset, or actual differences in cortical connectivity which may have emerged in relation to the different degrees of dexterity and nature of the uses of the forelimb across species. 3.4. Posterior medial inputs On the basis of comparisons with macaque architectonic data and their relative location (Burman and Rosa, 2009; Paxinos et al., 2012), several areas are currently recognized in the posterior part of marmoset medial cortex. Moderate projections from this region, particularly from parts of area 23 and area 31, target M1 and 6DC (Burman et al., 2014a,b; Table 1), in general agreement with reports in other species (Morecraft and Van Hoesen, 1992; Stepniewska et al., 1993; Hatanaka et al., 2001; Morecraft et al., 2004, 2012). Some of these studies have shown additional connections of M1 and 6DC with the supplementary somatosensory area (SSA, Murray and Coulter, 1981), which might correspond to medial area PEci of Pandya and Seltzer (1982). An anatomical description of medial area PEci in marmosets is still lacking, and the equivalent subdivision could be included either within the limits of currently recognized area PEC and/or area 31. Compared to the other frontal areas, area 6DR receives dense projections from the posteromedial cortex (including ventral sectors of area 23, area PGM, and retrosplenial areas 29/30, Burman et al., 2014b; Table 1 and Fig. 3). Functions attributed to these caudal areas are biased toward visuospatial analyses for orientation and navigation, memory, and attention (Vogt and Laureys, 2005; Vann et al., 2009; Kravitz et al., 2013). At least some of these functions might be accomplished via the oculomotor

Please cite this article in press as: Bakola, S., et al., The cortical motor system of the marmoset monkey (Callithrix jacchus). Neurosci. Res. (2014), http://dx.doi.org/10.1016/j.neures.2014.11.003

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system, and posteromedial areas exhibit eye-movement- or eyeand-hand-related activity (Olson et al., 1996; Ferraina et al., 1997; Thier and Andersen, 1998; Dean et al., 2004), and connections with visual and oculomotor fields (Cavada and Goldman-Rakic, 1989a,b; Leichnetz, 2001; Morecraft et al., 2004; Passarelli et al., 2013), including representations of the peripheral visual field (Rosa and Schmid, 1995; Yu et al., 2012). Although many of the functions for this system have been described in rather broad anatomical terms in macaques (Cavanna and Trimble, 2006; Vann et al., 2009), the main point here is that robust posteromedial connections characterize macaque and marmoset 6DR cortex, suggesting a highly conserved pathway among primates. It is possible that the evolutionary significance of posteromedial cortex is best considered in relation to the default network of brain areas (Raichle, 2001; Buckner et al., 2008); in particular, the macaque posterior midline areas form part of a distributed system of association areas that exhibit diminished hemodynamic responses and neuronal activity with execution of goal-directed tasks (Hayden et al., 2009; Kojima et al., 2009; Mantini et al., 2011). A recent restingstate fMRI analysis identified the posteromedial network as key component of the default system in marmosets (Belcher et al., 2013). 3.5. Prefrontal inputs Parcellation of marmoset prefrontal cortex has been verified on the basis of architectonic and connectional data (Burman et al., 2006; Roberts et al., 2007; Paxinos et al., 2012; Reser et al., 2013), consistent with macaque studies (Barbas and Mesulam, 1981; Schall et al., 1995; Petrides and Pandya, 1999). Prefrontal projections (mainly from areas 46, 12, 45, 8, and the precentral opercular cortex, PrCo) target premotor areas 6Va and 6DR, although with different weights (Burman et al., 2014b,c; Table 1, Figs. 2 and 3). Among prefrontal projections, those from the area 8 complex to 6DR are particularly prominent, in parallel with macaque findings (Schall et al., 1993; Luppino et al., 2003). Area 8 has been traditionally associated with the frontal eye fields, particularly the region of large saccades (Robinson and Fuchs, 1969; Bruce and Goldberg, 1985; Moschovakis et al., 2004), but might be more generally involved in orientation and cognitive processes that could allow more accurate interactions with the world (van der Steen et al., 1986; Knight and Fuchs, 2007; Lucchetti et al., 2008; Wardak et al., 2010; Katsuki and Constantinidis, 2012). As in macaques (Barbas, 1988; Luppino et al., 2003), many connections are shared between marmoset area 8 and 6DR (Reser et al., 2013; Burman et al., 2014b), for example, connections with dorsal and ventral prefrontal areas, which are engaged in spatial and object-specific aspects of working memory, respectively (Wilson et al., 1993; Ungerleider et al., 1998; Petrides and Pandya, 2002). In addition, 6DR and area 8 in marmosets share inputs from extrastriate visual areas, although these are somewhat diminished for 6DR. These connections, which are much sparser or nonexistent in other premotor subdivisions (Burman et al., 2014b,c; Table 1), include the motionrelated areas MST (medial superior temporal area), FST (fundus of the superior temporal area), and MTC (middle temporal crescent) (Rosa and Elston, 1998), area DA/V3A (dorsoanterior/visual area 3A) (Rosa et al., 2005, 2013), and the peripheral representation of areas V2 (second visual area) and VLA/V4 (ventrolateral anterior/visual area 4) (Rosa and Tweedale, 2000). Overall, these visual inputs seem to originate in the dorsomedial subdivision of the dorsal stream (Gattass et al., 1990), which emphasizes vision in the far periphery and visuomotor function. Additional sensory inputs originate in polysensory areas of the temporal lobe, including areas STP (superior temporal polysensory area) and Tpt (temporoparietal transition area), and some subdivisions of the rostral inferior

temporal cortex. In contrast, visual projections to macaque 6DR have not been described, with the exception of input from MST and/or caudal STP (Seltzer and Pandya, 1989; Huerta and Kaas, 1990; Luppino et al., 2001, 2003). On the other hand, evidence for prefrontal-ventral premotor connections in other primates is extremely sparse; the few available studies confirm general similarities among species (Preuss and Goldman-Rakic, 1989; Lu et al., 1994; Wang et al., 2002; Dum and Strick, 2005; Gerbella et al., 2011). Prefrontal areas that target area 6Va have been related to memorized and non-spatial processing (Barbas, 1988; Levy and Goldman-Rakic, 2000). Thus, it appears that, in addition to skeletomotor circuits, frontal circuits related to more complex processing are a common feature of cortical organization in both New World and Old World monkeys.

3.6. Inputs to area 8C Area 8C presents an interesting case in primate cortical anatomy, as it has only been described in marmosets (Burman et al., 2006, 2014c; Paxinos et al., 2012); therefore, homologies with other primates are tentative. Area 8C has substantial connections with the neighboring motor fields of the dorsal and ventral premotor areas, whereas projections from M1 are negligible (Table 1 and Fig. 3). Significant sensory components are observed with the S2 complex in the lateral sulcus and areas PF/PFG in the rostral ventral parietal cortex; in this respect, input to area 8C resembles that to 6Va. However, unlike the latter, area 8C does not receive significant projections from more anterior somatosensory fields. On the other hand, area 8C receives stronger projections from prefrontal areas, particularly 8aV. Compared to 6DC, 8C lacks strong motor and dorsal posterior parietal connections. The overall pattern of cortical connections and input from the motor complex of the ventral thalamus (Burman et al., 2014c) demonstrates that area 8C should be considered part of the premotor network of areas. On the basis of dense connections with area 8aV and the visual motion area MST, area 8C could have a role in sensorimotor processes related to eye movements, attributed to the region near the arcuate spur in macaques (Gottlieb et al., 1994; Tanaka and Fukushima, 1998; Fukushima et al., 2000; Moschovakis et al., 2004; Baker et al., 2006), although a purely oculomotor function for this cortical region seems unlikely (Savaki et al., 2014). Rather, the general pattern of connections of area 8C shows parallels with the vestibular-related network of areas described in New World squirrel monkeys (Guldin et al., 1992), which has been implicated in head and body movements in space.

4. Comparative considerations The main findings of our studies emphasize the notion that the marmoset frontal agranular cortex contains anatomically discrete motor-related areas, with unique sets of connections, including thalamocortical connections (Burman et al., 2014a,b,c), in parallel with the anatomical organization in other species. Furthermore, our anatomical data indicate a pivotal role for marmoset medial area 6M (which provided input to all frontal areas under study) in the control of limb and orofacial actions, as suggested for macaque medial motor areas (Tanji and Kurata, 1982; Mitz and Wise, 1987). Functional studies are necessary to evaluate participation of marmoset area 6M in specific aspects of movement such as temporal coding if actions, monitoring of the behavioral outcomes of movements and performance reward (Shima and Tanji, 2000; Akkal et al., 2002; Scangos et al., 2013). These observations follow analogous findings in sensory systems, and suggest that cortical circuits are conserved among primates, despite differences in brain size and

Please cite this article in press as: Bakola, S., et al., The cortical motor system of the marmoset monkey (Callithrix jacchus). Neurosci. Res. (2014), http://dx.doi.org/10.1016/j.neures.2014.11.003

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life styles, particularly in terms of their requirement for manual dexterity. The dorsocaudal premotor subdivision (6DC) is dominated by motor and inputs from higher-order somatosensory areas, indicating that this area plays a key role in motor control in many species, and arose early in primate evolution. The connectivity pattern of marmoset 6DC is essentially similar to that of large monkeys. Likewise, cortical connections of area 6Va are generally similar to those described in macaques, indicating that ventral premotor circuits are a shared feature of primate motor cortex organization. Area 6Va forms major connections with lateral parts of M1 and somatosensory areas, suggesting a specialized circuitry related to purposeful mouth/hand actions, such as feeding behaviors, as proposed for macaques (Rizzolatti et al., 1981a; Yokochi et al., 2003; Fogassi et al., 2005). Differences in input to premotor areas from posterior parietal fields would require confirmation from more extensive studies, although these could be, at least partly, attributed to specific adaptations for hand skills, which are generally less developed in many New World monkeys (Padberg et al., 2005, 2007). Many of the key questions to be addressed by future studies relate to the number, architectural extent, and functional properties of posterior parietal subdivisions (e.g., V6A, PEip, AIP), which in macaques are involved in the planning and execution of forelimb movements. Perhaps more surprising are the substantial interspecies similarities in the connectivity of area 6DR. Thus, weak inputs from skeletomotor areas and dense input from prefrontal areas indicate that marmoset 6DR operates at relatively more abstract levels of motor control, such as input integration, and preparation of movement according to different behavioral contexts (Boussaoud, 2001; Cisek and Kalaska, 2005; Abe and Hanakawa, 2009), and mostly exerts its influence over M1 corticospinal neurons indirectly, through synapses in areas 6DC and 6Va (Burman et al., 2014b,c). In addition, the connections of area 6DR emphasize inputs from several posteromedial areas, including inputs from visual and putative eye fields (Burman et al., 2014b; Table 1). Oculomotorrelated fields have been described in some detail in the frontal cortex of new world monkeys (Blum et al., 1982; Gould et al., 1986; Huerta et al., 1987), but their number and precise architectonic borders are still not clear. Our anatomical studies suggesting that marmoset frontal cortex might contain eye-movement-related fields within two architecturally discrete regions (likely equivalents of the macaque frontal eye field and medial frontal eye field, Reser et al., 2013; Burman et al., 2014b) could provide a useful guide for future investigations. In addition, the description of a possible oculomotor region at the junction between dorsal and ventral premotor cortex (8C, Burman et al., 2014c), for which little information is currently available in other primates, requires further investigation. The last considerations become particularly relevant in light of a recent behavioral study which showed that marmoset eye movement performance is comparable to that of macaques (including good relationships between saccade amplitudes and velocities), despite the restricted oculomotor range of the former species (Mitchell et al., 2014).

Acknowledgements Supported by research grants from the National Health and Medical Research Council (1020839 and 545865) and Australian Research Council (DP110101200, DE120102883 and DP140101968). The skilled assistance of Karyn Richardson, David Reser, Hsin-Hao Yu, Tristan Chaplin, and Katrina Worthy, including support in several phases of this project, as well as the technical support by Heidi Gaulke, Amanda Worthy and Sherry Zhao are gratefully acknowledged. We also thank Rowan Tweedale for comments on the manuscript.

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References Abe, M., Hanakawa, T., 2009. Functional coupling underlying motor and cognitive functions of the dorsal premotor cortex. Behav. Brain Res. 198, 13–23. Akkal, D., Bioulac, B., Audin, J., Burbaud, P., 2002. Comparison of neuronal activity in the rostral supplementary and cingulate motor areas during a task with cognitive and motor demands. Eur. J. Neurosci. 15, 887–904. Andersen, R.A., Buneo, C.A., 2002. Intentional maps in posterior parietal cortex. Annu. Rev. Neurosci. 25, 189–220. Ashe, J., Lungu, O.V., Basford, A.T., Lu, X., 2006. Cortical control of motor sequences. Curr. Opin. Neurobiol. 16, 213–221. Baker, J.T., Patel, G.H., Corbetta, M., Snyder, L.H., 2006. Distribution of activity across the monkey cerebral cortical surface, thalamus and midbrain during rapid, visually guided saccades. Cereb. Cortex 16, 447–459. Bakola, S., Gamberini, M., Passarelli, L., Fattori, P., Galletti, C., 2010. Cortical connections of parietal field PEc in the macaque: linking vision and somatic sensation for the control of limb action. Cereb. Cortex 20, 2592–2604. Bakola, S., Passarelli, L., Gamberini, M., Fattori, P., Galletti, C., 2013. Cortical connectivity suggests a role in limb coordination for macaque area PE of the superior parietal cortex. J. Neurosci. 33, 6648–6658. Barbas, H., 1988. Anatomic organization of basoventral and mediodorsal visual recipient prefrontal regions in the rhesus monkey. J. Comp. Neurol. 276, 313–342. Barbas, H., Mesulam, M.M., 1981. Organization of afferent input to subdivisions of area 8 in the rhesus monkey. J. Comp. Neurol. 200, 407–431. Barbas, H., Pandya, D.N., 1987. Architecture and frontal cortical connections of the premotor cortex (area 6) in the rhesus monkey. J. Comp. Neurol. 256, 211–228. Bates, J.F., Goldman-Rakic, P.S., 1993. Prefrontal connections of medial motor areas in the rhesus monkey. J. Comp. Neurol. 336, 211–228. Belcher, A.M., Yen, C.C., Stepp, H., Gu, H., Lu, H., Yang, Y., Silva, A.C., Stein, E.A., 2013. Large-scale brain networks in the awake, truly resting marmoset monkey. J. Neurosci. 33, 16796–16804. Belmalih, A., Borra, E., Contini, M., Gerbella, M., Rozzi, S., Luppino, G., 2009. Multimodal architectonic subdivision of the rostral part (area F5) of the macaque ventral premotor cortex. J. Comp. Neurol. 512, 183–217. Blum, B., Kulikowski, J.J., Carden, D., Harwood, D., 1982. Eye movements induced by electrical stimulation of the frontal eye fields of marmosets and squirrel monkeys. Brain Behav. Evol. 21, 34–41. Bortoff, G.A., Strick, P.L., 1993. Corticospinal terminations in two new-world primates: further evidence that corticomotoneuronal connections provide part of the neural substrate for manual dexterity. J. Neurosci. 13, 5105–5118. Boussaoud, D., 2001. Attention versus intention in the primate premotor cortex. Neuroimage 14, 40–45. Bruce, C.J., Goldberg, M.E., 1985. Primate frontal eye fields. I. Single neurons discharging before saccades. J. Neurophysiol. 53, 603–635. Buckner, R.L., Andrews-Hanna, J.R., Schacter, D.L., 2008. The brain’s default network: anatomy, function, and relevance to disease. Ann. N.Y. Acad. Sci. 1124, 1–38. Burish, M.J., Stepniewska, I., Kaas, J.H., 2008. Microstimulation and architectonics of frontoparietal cortex in common marmosets (Callithrix jacchus). J. Comp. Neurol. 507, 1151–1168. Burman, K.J., Bakola, S., Richardson, K.E., Reser, D.H., Rosa, M.G.P., 2014a. Patterns of cortical input to the primary motor area in the marmoset monkey. J. Comp. Neurol. 522, 811–843. Burman, K.J., Bakola, S., Richardson, K.E., Reser, D.H., Rosa, M.G.P., 2014b. Patterns of afferent input to the caudal and rostral areas of the dorsal premotor cortex (6DC and 6DR) in the marmoset monkey. J. Comp. Neurol. 522, 3683–3716. Burman, K.J., Bakola, S., Richardson, K.E., Yu, H.H., Reser, D.H., Rosa, M.G.P., 2014c. Cortical and thalamic projections to cytoarchitectural areas 6Va and 8C of the marmoset monkey: connectionally distinct subdivisions of the lateral premotor cortex. J. Comp. Neurol. (in press). Burman, K.J., Palmer, S.M., Gamberini, M., Rosa, M.G.P., 2006. Cytoarchitectonic subdivisions of the dorsolateral frontal cortex of the marmoset monkey (Callithrix jacchus), and their projections to dorsal visual areas. J. Comp. Neurol. 495, 149–172. Burman, K.J., Palmer, S.M., Gamberini, M., Spitzer, M.W., Rosa, M.G.P., 2008. Anatomical and physiological definition of the motor cortex of the marmoset monkey. J. Comp. Neurol. 506, 860–876. Burman, K.J., Reser, D.H., Yu, H.H., Rosa, M.G.P., 2011. Cortical input to the frontal pole of the marmoset monkey. Cereb. Cortex 21, 1712–1737. Burman, K.J., Rosa, M.G.P., 2009. Architectural subdivisions of medial and orbital frontal cortices in the marmoset monkey (Callithrix jacchus). J. Comp. Neurol. 514, 11–29. Burton, H., Fabri, M., Alloway, K., 1995. Cortical areas within the lateral sulcus connected to cutaneous representations in areas 3b and 1: a revised interpretation of the second somatosensory area in macaque monkeys. J. Comp. Neurol. 355, 539–562. Caminiti, R., Chafee, M.V., Battaglia-Mayer, A., Averbeck, B.B., Crowe, D.A., Georgopoulos, A.P., 2010. Understanding the parietal lobe syndrome from a neurophysiological and evolutionary perspective. Eur. J. Neurosci. 31, 2320–2340. Carlson, M., Huerta, M.F., Cusick, C.G., Kaas, J.H., 1986. Studies on the evolution of multiple somatosensory representations in primates: the organization of anterior parietal cortex in the New World Callitrichid, Saguinus. J. Comp. Neurol. 246, 409–426. Cavada, C., Goldman-Rakic, P.S., 1989a. Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe. J. Comp. Neurol. 287, 422–445.

Please cite this article in press as: Bakola, S., et al., The cortical motor system of the marmoset monkey (Callithrix jacchus). Neurosci. Res. (2014), http://dx.doi.org/10.1016/j.neures.2014.11.003

G Model NSR-3768; No. of Pages 10 8

ARTICLE IN PRESS S. Bakola et al. / Neuroscience Research xxx (2014) xxx–xxx

Cavada, C., Goldman-Rakic, P.S., 1989b. Posterior parietal cortex in rhesus monkey: I. Parcellation of areas based on distinctive limbic and sensory corticocortical connections. J. Comp. Neurol. 287, 393–421. Cavanna, A.E., Trimble, M.R., 2006. The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129, 564–583. Cipolloni, P.B., Pandya, D.N., 1999. Cortical connections of the frontoparietal opercular areas in the rhesus monkey. J. Comp. Neurol. 403, 431–458. Cisek, P., Kalaska, J.F., 2005. Neural correlates of reaching decisions in dorsal premotor cortex: specification of multiple direction choices and final selection of action. Neuron 45, 801–814. Coq, J.O., Qi, H., Collins, C.E., Kaas, J.H., 2004. Anatomical and functional organization of somatosensory areas of the lateral fissure of the New World titi monkey (Callicebus moloch). J. Comp. Neurol. 476, 363–387. Culham, J.C., Kanwisher, N.G., 2001. Neuroimaging of cognitive functions in human parietal cortex. Curr. Opin. Neurobiol. 11, 157–163. Dancause, N., Barbay, S., Frost, S.B., Plautz, E.J., Popescu, M., Dixon, P.M., Stowe, A.M., Friel, K.M., Nudo, R.J., 2006. Topographically divergent and convergent connectivity between premotor and primary motor cortex. Cereb. Cortex 16, 1057–1068. Dancause, N., Duric, V., Barbay, S., Frost, S.B., Stylianou, A., Nudo, R.J., 2008. An additional motor-related field in the lateral frontal cortex of squirrel monkeys. Cereb. Cortex 18, 2719–2728. de la Mothe, L.A., Blumell, S., Kajikawa, Y., Hackett, T.A., 2006. Cortical connections of the auditory cortex in marmoset monkeys: core and medial belt regions. J. Comp. Neurol. 496, 27–71. Dean, H.L., Crowley, J.C., Platt, M.L., 2004. Visual and saccade-related activity in macaque posterior cingulate cortex. J. Neurophysiol. 92, 3056–3068. Devinsky, O., Morrell, M.J., Vogt, B.A., 1995. Contributions of anterior cingulate cortex to behaviour. Brain 118 (Pt. 1), 279–306. Disbrow, E., Litinas, E., Recanzone, G.H., Padberg, J., Krubitzer, L., 2003. Cortical connections of the second somatosensory area and the parietal ventral area in macaque monkeys. J. Comp. Neurol. 462, 382–399. Donoghue, J.P., Leibovic, S., Sanes, J.N., 1992. Organization of the forelimb area in squirrel monkey motor cortex: representation of digit, wrist, and elbow muscles. Exp. Brain Res. 89, 1–19. Dum, R.P., Strick, P.L., 2002. Motor areas in the frontal lobe of the primate. Physiol. Behav. 77, 677–682. Dum, R.P., Strick, P.L., 2005. Frontal lobe inputs to the digit representations of the motor areas on the lateral surface of the hemisphere. J. Neurosci. 25, 1375–1386. Felleman, D.J., Nelson, R.J., Sur, M., Kaas, J.H., 1983. Representations of the body surface in areas 3b and 1 of postcentral parietal cortex of Cebus monkeys. Brain Res. 268, 15–26. Ferraina, S., Johnson, P.B., Garasto, M.R., Battaglia-Mayer, A., Ercolani, L., Bianchi, L., Lacquaniti, F., Caminiti, R., 1997. Combination of hand and gaze signals during reaching: activity in parietal area 7m of the monkey. J. Neurophysiol. 77, 1034–1038. Fogassi, L., Ferrari, P.F., Gesierich, B., Rozzi, S., Chersi, F., Rizzolatti, G., 2005. Parietal lobe: from action organization to intention understanding. Science 308, 662–667. Fogassi, L., Gallese, V., Fadiga, E., Luppino, G., Matelli, M., Rizzolatti, G., 1996. Coding of peripersonal space in inferior premotor cortex (area F4). J. Neurophysiol. 76, 141–157. Fouad, K., Klusman, I., Schwab, M.E., 2004. Regenerating corticospinal fibers in the Marmoset (Callithrix jacchus) after spinal cord lesion and treatment with the anti-Nogo-A antibody IN-1. Eur. J. Neurosci. 20, 2479–2482. Freret, T., Bouet, V., Toutain, J., Saulnier, R., Pro-Sistiaga, P., Bihel, E., Mackenzie, E.T., Roussel, S., Schumann-Bard, P., Touzani, O., 2008. Intraluminal thread model of focal stroke in the non-human primate. J. Cereb. Blood Flow Metab. 28, 786–796. Friedman, D.P., Jones, E.G., Burton, H., 1980. Representation pattern in the second somatic sensory area of the monkey cerebral cortex. J. Comp. Neurol. 192, 21–41. Friedman, D.P., Murray, E.A., O’Neill, J.B., Mishkin, M., 1986. Cortical connections of the somatosensory fields of the lateral sulcus of macaques: evidence for a corticolimbic pathway for touch. J. Comp. Neurol. 252, 323–347. Fukushima, K., Sato, T., Fukushima, J., Shinmei, Y., Kaneko, C.R., 2000. Activity of smooth pursuit-related neurons in the monkey periarcuate cortex during pursuit and passive whole-body rotation. J. Neurophysiol. 83, 563–587. Galea, M.P., Darian-Smith, I., 1994. Multiple corticospinal neuron populations in the macaque monkey are specified by their unique cortical origins, spinal terminations, and connections. Cereb. Cortex 4, 166–194. Gamberini, M., Passarelli, L., Fattori, P., Zucchelli, M., Bakola, S., Luppino, G., Galletti, C., 2009. Cortical connections of the visuomotor parieto-occipital area V6Ad of the macaque monkey. J. Comp. Neurol. 513, 622–642. Gattass, R., Rosa, M.G.P., Sousa, A.P., Pinon, M.C., Fiorani Junior, M., Neuenschwander, S., 1990. Cortical streams of visual information processing in primates. Braz. J. Med. Biol. Res. 23, 375–393. Gerbella, M., Belmalih, A., Borra, E., Rozzi, S., Luppino, G., 2011. Cortical connections of the anterior (F5a) subdivision of the macaque ventral premotor area F5. Brain Struct. Funct. 216, 43–65. Geyer, S., Matelli, M., Luppino, G., Zilles, K., 2000. Functional neuroanatomy of the primate isocortical motor system. Anat. Embryol. 202, 443–474. Gharbawie, O.A., Stepniewska, I., Kaas, J.H., 2011a. Cortical connections of functional zones in posterior parietal cortex and frontal cortex motor regions in new world monkeys. Cereb. Cortex 21, 1981–2002. Gharbawie, O.A., Stepniewska, I., Qi, H., Kaas, J.H., 2011b. Multiple parietal–frontal pathways mediate grasping in macaque monkeys. J. Neurosci. 31, 11660–11677.

Ghosh, S., Brinkman, C., Porter, R., 1987. A quantitive study of the distribution of neurons projecting to the precentral motor cortex in the monkey (M. fascicularis). J. Comp. Neurol. 259, 424–444. Ghosh, S., Gattera, R., 1995. A comparison of the ipsilateral cortical projections to the dorsal and ventral subdivisions of the macaque premotor cortex. Somatosens. Mot. Res. 12, 359–378. Godschalk, M., Mitz, A.R., Van Duin, B., Van der Burg, H., 1995. Somatotopy of monkey premotor cortex examined with microstimulation. Neurosci. Res. 23, 269–279. Gottlieb, J., 2007. From thought to action: the parietal cortex as a bridge between perception, action, and cognition. Neuron 53, 9–16. Gottlieb, J.P., MacAvoy, M.G., Bruce, C.J., 1994. Neural responses related to smoothpursuit eye movements and their correspondence with electrically elicited smooth eye movements in the primate frontal eye field. J. Neurophysiol. 72, 1634–1653. Gould, H.J., Cusick, C.G., Pons, T.P., Kaas, J.H., 1986. The relationship of corpus callosum connections to electrical stimulation maps of motor, supplementary motor, and the frontal eye fields in owl monkeys. J. Comp. Neurol. 247, 297–325. Graziano, M.S., Aflalo, T.N., 2007. Rethinking cortical organization: moving away from discrete areas arranged in hierarchies. Neuroscientist. 13, 138–147. Graziano, M.S.A., Gandhi, S., 2000. Location of the polysensory zone in the precentral gyrus of anesthetized monkeys. Exp. Brain Res. 135, 259–266. Graziano, M.S.A., Hu, X.T., Gross, C.G., 1997. Visuospatial properties of ventral premotor cortex. J. Neurophysiol. 77, 2268–2292. Grefkes, C., Fink, G.R., 2005. The functional organization of the intraparietal sulcus in humans and monkeys. J. Anat. 207, 3–17. Gregoriou, G.G., Savaki, H.E., 2003. When vision guides movement: a functional imaging study of the monkey brain. Neuroimage 19, 959–967. Guldin, W.O., Akbarian, S., Grüsser, O.J., 1992. Cortico-cortical connections and cytoarchitectonics of the primate vestibular cortex: a study in squirrel monkeys (Saimiri sciureus). J. Comp. Neurol. 326, 375–401. Hatanaka, N., Nambu, A., Yamashita, A., Takada, M., Tokuno, H., 2001. Somatotopic arrangement and corticocortical inputs of the hindlimb region of the primary motor cortex in the macaque monkey. Neurosci. Res. 40, 9–22. Hayden, B.Y., Smith, D.V., Platt, M.L., 2009. Electrophysiological correlates of defaultmode processing in macaque posterior cingulate cortex. Proc. Natl. Acad. Sci. U. S. A. 106, 5948–5953. He, S.-Q., Dum, R.P., Strick, P.L., 1995. Topographic organization of corticospinal projections from the frontal lobe: motor areas on the medial surface of the hemisphere. J. Neurosci. 15, 3284–3306. Huerta, M.F., Kaas, J.H., 1990. Supplementary eye field as defined by intracortical microstimulation: connections in macaque. J. Comp. Neurol. 330, 299–330. Huerta, M.F., Krubitzer, L.A., Kaas, J.H., 1987. Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys. II. Cortical connections. J. Comp. Neurol. 265, 332–361. Huerta, M.F., Pons, T.P., 1990. Primary motor cortex receives input from area 3a in macaques. Brain Res. 537, 367–371. Huffman, K.J., Krubitzer, L., 2001. Area 3a: topographic organization and cortical connections in marmoset monkeys. Cereb. Cortex 11, 849–867. Hutchins, K., Martino, A., Strick, P., 1988. Corticospinal projections from the medial wall of the hemisphere. Exp. Brain Res. 71, 667–672. Iyengar, S., Qi, H.X., Jain, N., Kaas, J.H., 2007. Cortical and thalamic connections of the representations of the teeth and tongue in somatosensory cortex of new world monkeys. J. Comp. Neurol. 501, 95–120. Jain, N., Qi, H.X., Catania, K.C., Kaas, J.H., 2001. Anatomic correlates of the face and oral cavity representations in the somatosensory cortical area 3b of monkeys. J. Comp. Neurol. 429, 455–468. Jones, E.G., Coulter, J.D., Hendry, H.C., 1978. Intracortical connectivity of architectonic fields in the somatic sensory, motor and parietal cortex of monkeys. J. Comp. Neurol. 181, 291–348. Kalaska, J.F., Scott, S.H., Cisek, P., Sergio, L.E., 1997. Cortical control of reaching movements. Curr. Opin. Neurobiol. 7, 849–859. Katsuki, F., Constantinidis, C., 2012. Early involvement of prefrontal cortex in visual bottom-up attention. Nat. Neurosci. 15, 1160–1166. Knight, T.A., Fuchs, A.F., 2007. Contribution of the frontal eye field to gaze shifts in the head-unrestrained monkey: effects of microstimulation. J. Neurophysiol. 97, 618–634. Kobayashi, Y., Amaral, D.G., 2000. Macaque monkey retrosplenial cortex: I. Threedimensional and cytoarchitectonic organization. J. Comp. Neurol. 426, 339–365. Kojima, T., Onoe, H., Hikosaka, K., Tsutsui, K., Tsukada, H., Watanabe, M., 2009. Default mode of brain activity demonstrated by positron emission tomography imaging in awake monkeys: higher rest-related than working memory-related activity in medial cortical areas. J. Neurosci. 29, 14463–14471. Konomi, T., Fujiyoshi, K., Hikishima, K., Komaki, Y., Tsuji, O., Okano, H.J., Toyama, Y., Okano, H., Nakamura, M., 2012. Conditions for quantitative evaluation of injured spinal cord by in vivo diffusion tensor imaging and tractography: preclinical longitudinal study in common marmosets. Neuroimage 63, 1841–1853. Kravitz, D.J., Saleem, K.S., Baker, C.I., Ungerleider, L.G., Mishkin, M., 2013. The ventral visual pathway: an expanded neural framework for the processing of object quality. Trends Cogn. Sci. 17, 26–49. Krubitzer, L., Clarey, J., Tweedale, R., Elston, G., Calford, M., 1995. A redefinition of somatosensory areas in the lateral sulcus of macaque monkeys. J. Neurosci. 15, 3821–3839. Krubitzer, L., Huffman, K.J., Disbrow, E., Recanzone, G., 2004. Organization of area 3a in macaque monkeys: contributions to the cortical phenotype. J. Comp. Neurol. 471, 97–111.

Please cite this article in press as: Bakola, S., et al., The cortical motor system of the marmoset monkey (Callithrix jacchus). Neurosci. Res. (2014), http://dx.doi.org/10.1016/j.neures.2014.11.003

G Model NSR-3768; No. of Pages 10

ARTICLE IN PRESS S. Bakola et al. / Neuroscience Research xxx (2014) xxx–xxx

Krubitzer, L.A., Calford, M.B., 1992. Five topographically organized fields in the somatosensory cortex of the flying fox: microelectrode maps, myeloarchitecture, and cortical modules. J. Comp. Neurol. 317, 1–30. Krubitzer, L.A., Kaas, J.H., 1990. The organization and connections of somatosensory cortex in marmosets. J. Neurosci. 10, 952–974. Künzle, H., 1978. Cortico-cortical efferents of primary motor and somatosensory regions of the cerebral cortex in Macaca facicularis. Neuroscience 3, 25–39. Kurata, K., 1991. Corticocortical inputs to the dorsal and ventral aspects of the premotor cortex of macaque monkeys. Neurosci. Res. 12, 263–280. Kuwabara, M., Mansouri, F.A., Buckley, M.J., Tanaka, K., 2014. Cognitive control functions of anterior cingulate cortex in macaque monkeys performing a Wisconsin Card Sorting Test analog. J. Neurosci. 34, 7531–7547. Kwan, H.C., MacKay, W.A., Murphy, J.T., Wong, Y.C., 1978. Spatial organization of precentral cortex in awake primates. II. Motor outputs. J. Neurophysiol. 41, 1120–1131. Leichnetz, G.R., 1986. Afferent and efferent connections of the dorsolateral precentral gyrus (area 4, hand/arm region) in the macaque monkey, with comparisons to area 8. J. Comp. Neurol. 254, 460–492. Leichnetz, G.R., 2001. Connections of the medial posterior parietal cortex (area 7m) in the monkey. Anat. Rec. 263, 215–236. Lemon, R.N., Griffiths, J., 2005. Comparing the function of the corticospinal system in different species: organizational differences for motor specialization? Muscle Nerve 32, 261–279. Lemon, R.N., Kirkwood, P.A., Maier, M.A., Nakajima, K., Nathan, P., 2004. Direct and indirect pathways for corticospinal control of upper limb motoneurons in the primate. Prog. Brain Res. 143, 263–279. Levy, R., Goldman-Rakic, P.S., 2000. Segregation of working memory functions within the dorsolateral prefrontal cortex. Exp. Brain Res. 133, 23–32. Lewis, J.W., Van Essen, D.C., 2000. Corticocortical connections of visual, sensorimotor, and multimodal processing area in the parietal lobe of the macaque monkey. J. Comp. Neurol. 428, 112–137. Lu, M.T., Preston, J.B., Strick, P.L., 1994. Interconnections between the prefrontal cortex and the premotor areas in the frontal lobe. J. Comp. Neurol. 341, 375–392. Lucchetti, C., Lanzilotto, M., Bon, L., 2008. Auditory-motor and cognitive aspects in area 8B of macaque monkey’s frontal cortex: a premotor ear-eye field (PEEF). Exp. Brain Res. 186, 131–141. Luppino, G., Ben Hamed, S., Gamberini, M., Matelli, M., Galletti, C., 2005. Occipital (V6) and parietal (V6A) areas in the anterior wall of the parieto-occipital sulcus of the macaque: a cytoarchitectonic study. Eur. J. Neurosci. 21, 3056–3076. Luppino, G., Calzavara, R., Rozzi, S., Matelli, M., 2001. Projections from the superior temporal sulcus to the agranular frontal cortex in the macaque. Eur. J. Neurosci. 14, 1035–1040. Luppino, G., Matelli, M., Camarda, R., Gallese, V., Rizzolatti, G., 1991. Multiple representations of body movements in mesial area 6 and the adjacent cingulate cortex: intracortical microstimulation study in the macaque monkey. J. Comp. Neurol. 311, 463–482. Luppino, G., Matelli, M., Camarda, R., Rizzolatti, G., 1993. Coricocortical connections of area F3 (SMA-proper) and area F6 (pre-SMA) in the macaque monkey. J. Comp. Neurol. 338, 114–140. Luppino, G., Rozzi, S., Calzavara, R., Matelli, M., 2003. Prefrontal and agranular cingulate projections to the dorsal premotor areas F2 and F7 in the macaque monkey. Eur. J. Neurosci. 17, 559–578. Maggi, P., Macri, S.M., Gaitan, M.I., Leibovitch, E., Wholer, J.E., Knight, H.L., Ellis, M., Wu, T., Silva, A.C., Massacesi, L., Jacobson, S., Westmoreland, S., Reich, D.S., 2014. The formation of inflammatory demyelinated lesions in cerebral white matter. Ann. Neurol. 76, 594–608. Mantini, D., Gerits, A., Nelissen, K., Durand, J.B., Joly, O., Simone, L., Sawamura, H., Wardak, C., Orban, G.A., Buckner, R.L., Vanduffel, W., 2011. Default mode of brain function in monkeys. J. Neurosci. 31, 12954–12962. Maranesi, M., Roda, F., Bonini, L., Rozzi, S., Ferrari, P.F., Fogassi, L., Coude, G., 2012. Anatomo-functional organization of the ventral primary motor and premotor cortex in the macaque monkey. Eur. J. Neurosci. 36, 3376–3387. Marconi, B., Genovesio, A., Battaglia-Mayer, A., Ferraina, S., Squatrito, S., Molinari, M., Laquaniti, L., Caminiti, R., 2001. Eye-hand coordination during reaching. I. Anatomical relationships between parietal and frontal cortex. Cereb. Cortex 11, 513–527. Marshall, J.W., Ridley, R.M., 2003. Assessment of cognitive and motor deficits in a marmoset model of stroke. ILAR. 44, 153–160. Matelli, M., Camarda, R., Glickstein, M., Rizzolatti, G., 1986. Afferent and efferent projections of the inferior area 6 in the macaque monkey. J. Comp. Neurol. 251, 281–298. Matelli, M., Govoni, P., Galletti, C., Kutz, D.F., Luppino, G., 1998. Superior area 6 afferents from the superior parietal lobule in the macaque monkey. J. Comp. Neurol. 402, 327–352. Matelli, M., Luppino, G., Rizzolatti, G., 1985. Patterns of cytochrome oxidase activity in the frontal agranular cortex of the macaque monkey. Behav. Brain Res. 18, 125–136. Matelli, M., Luppino, G., Rizzolatti, G., 1991. Architecture of superior and mesial area 6 and the adjacent cingulate cortex in the macaque monkey. J. Comp. Neurol. 311, 445–462. Merzenich, M.M., Kaas, J.H., Sur, M., Lin, C.S., 1978. Double representation of the body surface within cytoarchitectonic areas 3b and 1 in “SI” in the owl monkey (Aotus trivirgatus). J. Comp. Neurol. 181, 41–73. Mitchell, J.F., Reynolds, J.H., Miller, C.T., 2014. Active vision in marmosets: a model system for visual neuroscience. J. Neurosci. 34, 1183–1194.

9

Mitz, A.R., Wise, S.P., 1987. The somatotopic organization of the supplementary motor area: intracortical microstimulation mapping. J. Neurosci. 7, 1010–1021. Morecraft, R.J., Cipolloni, P.B., Stilwell-Morecraft, K.S., Gedney, M.T., Pandya, D.N., 2004. Cytoarchitecture and cortical connections of the posterior cingulate and adjacent somatosensory fields in the rhesus monkey. J. Comp. Neurol. 469, 37–69. Morecraft, R.J., Stilwell-Morecraft, K.S., Cipolloni, P.B., Ge, J., McNeal, D.W., Pandya, D.N., 2012. Cytoarchitecture and cortical connections of the anterior cingulate and adjacent somatomotor fields in the rhesus monkey. Brain Res. Bull. 87, 457–497. Morecraft, R.J., Van Hoesen, G.W., 1992. Cingulate input to the primary and supplementary motor cortices in the Rhesus Monkey: evidence for somatotopy in areas 24c and 23c. J. Comp. Neurol. 322, 471–489. Moschovakis, A.K., Gregoriou, G.G., Ugolini, G., Doldan, M., Graf, W., Guldin, W., Hadjidimitrakis, K., Savaki, H.E., 2004. Oculomotor areas of the primate frontal lobes: a transneuronal transfer of rabies virus and [14C]-2-deoxyglucose functional imaging study. J. Neurosci. 24, 5726–5740. Muakkassa, K.F., Strick, P.L., 1979. Frontal lobe inputs to primate motor cortex: evidence for four somatotopically organized ‘premotor’ areas. Brain Res. 177, 176–182. Murray, E.A., Coulter, J.D., 1981. Organization of corticospinal neurons in the monkey. J. Comp. Neurol. 195, 339–365. Murray, E.A., Mishkin, M., 1984. Relative contributions of SII and area 5 to tictile discrimination in monkeys. Behav. Brain Res. 11, 67–83. Nakano, K., Tokushige, A., Kohno, M., Hasegawa, Y., Kayahara, T., Sasaki, K., 1992. An autoradiographic study of cortical projections from motor thalamic nuclei in the macaque monkey. Neurosci. Res. 13, 119–137. Nelson, R.J., Sur, M., Felleman, D.J., Kaas, J.H., 1980. Representations of the body surface in postcentral parietal cortex of Macaca fascicularis. J. Comp. Neurol. 192, 611–643. Olson, C.R., Musil, S.Y., Goldberg, M.E., 1996. Single neurons in posterior cingulate cortex of behaving macaque: eye movement signals. J. Neurophysiol. 76, 3285–3300. Padberg, J., Disbrow, E., Krubitzer, L., 2005. The organization and connections of anterior and posterior parietal cortex in titi monkeys: do New World monkeys have an area 2? Cereb. Cortex 15, 1938–1963. Padberg, J., Franca, J.G., Cooke, D.F., Soares, J.G.M., Rosa, M.G.P., Fiorani, M.J., Gattass, R., Krubitzer, L., 2007. Parallel evolution of cortical areas involved in skilled hand use. J. Neurosci. 27, 10106–10115. Palmer, S.M., Rosa, M.G.P., 2006a. A distinct anatomical network of cortical areas for analysis of motion in far peripheral vision. Eur. J. Neurosci. 24, 2389–2405. Palmer, S.M., Rosa, M.G.P., 2006b. Quantitative analysis of the corticocortical projections to the middle temporal area in the marmoset monkey: evolutionary and functional implications. Cereb. Cortex 16, 1361–1375. Pandya, D.N., Seltzer, B., 1982. Intrinsic connections and architectonics of posterior parietal cortex in the rhesus monkey. J. Comp. Neurol. 204, 196–210. Passarelli, L., Bakola, S., Gamberini, M., Burman, K.J., Richardson, K.E., Fattori, P., Rosa, M.G.P., Galletti, C., 2013. Precuneate cortical connections in the macaque monkey. Society for Neuroscience, San Diego. Paxinos, G., Watson, C., Petrides, M., Rosa, M., Tokuno, H., 2012. The marmoset brain in stereotaxic coordinates. Academic Press, San Diego. Petrides, M., 2005. Lateral prefrontal cortex: architectonic and functional organization. Phil. Trans. R. Soc. B. 360, 781–795. Petrides, M., Pandya, D.N., 1984. Projections to the frontal cortex from the posterior parietal region in the rhesus monkey. J. Comp. Neurol. 228, 105–116. Petrides, M., Pandya, D.N., 1999. Dorsolateral prefrontal cortex: comparative cytoarchitectonic analysis in the human and the macaque brain and corticocortical connection patterns. Eur. J. Neurosci. 11, 1011–1036. Petrides, M., Pandya, D.N., 2002. Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey. Eur. J. Neurosci. 16, 291–310. Picard, N., Strick, P.L., 2001. Imaging the premotor areas. Curr. Opin. Neurobiol. 11, 663–672. Pohlmeyer, E.A., Mahmoudi, B., Geng, S., Prins, N.W., Sanchez, J.C., 2014. Using reinforcement learning to provide stable brain-machine interface control despite neural input reorganization. PLoS ONE. 9, e87253. Pons, T.P., Garraghty, P.E., Cusick, C.G., Kaas, J.H., 1985. The somatotopic organization of area 2 in macaque monkeys. J. Comp. Neurol. 241, 445–466. Preuss, T.M., Goldman-Rakic, P.S., 1989. Evidence for forelimb and orofacial representation in macaque granular frontal cortex: connections of the ventral rim of the principal sulcus with perisylvian premotor and somatosensory areas. J. Comp. Neurol. 282, 293–316. Preuss, T.M., Goldman-Rakic, P.S., 1991. Myelo- and cytoarchitecture of the granular frontal cortex and surrounding regions in the strepsirhine primate Galago and the anthropoid primate Macaca. J. Comp. Neurol. 310, 429–474. Purvis, A., Nee, S., Harvey, P.H., 1995. Macroevolutionary inferences from primate phylogeny. Proc. Biol. Sci. 260, 329–333. Qi, H.X., Lyon, D.C., Kaas, J.H., 2002. Cortical and thalamic connections of the parietal ventral somatosensory area in marmoset monkeys (Callithrix jacchus). J. Comp. Neurol. 443, 168–182. Raichle, M.E., 2001. A default mode of brain function. Proc. Natl. Acad. Sci. U. S. A. 98, 4259–4264. Reser, D.H., Burman, K.J., Richardson, K.E., Spitzer, M.W., Rosa, M.G.P., 2009. Connections of the marmoset rostrotemporal auditory area: express pathways for analysis of affective content in hearing. Eur. J. Neurosci. 30, 578–592.

Please cite this article in press as: Bakola, S., et al., The cortical motor system of the marmoset monkey (Callithrix jacchus). Neurosci. Res. (2014), http://dx.doi.org/10.1016/j.neures.2014.11.003

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ARTICLE IN PRESS S. Bakola et al. / Neuroscience Research xxx (2014) xxx–xxx

Reser, D.H., Burman, K.J., Yu, H.H., Chaplin, T.A., Richardson, K.E., Worthy, K.H., Rosa, M.G.P., 2013. Contrasting patterns of cortical input to architectural subdivisions of the area 8 complex: a retrograde tracing study in marmoset monkeys. Cereb. Cortex 23, 1901–1922. Rizzolatti, G., Luppino, G., 2001. The cortical motor system. Neuron 31, 889–901. Rizzolatti, G., Scandolara, C., Gentilucci, M., Camarda, R., 1981a. Responce properties and behavioral modulation of mouth neurons of the postarcuate cortex (area 6) in macaque monkeys. Brain Res. 255, 421–424. Rizzolatti, G., Scandolara, C., Mitelli, M., Gentilucci, M., 1981b. Afferent properties of periarcuate neurons in macaque monkeys I. Somato-sensory responses. Behav. Brain Res. 2, 125–146. Roberts, A.C., Tomic, D.L., Parkinson, C.H., Roeling, T.A., Cutter, D.J., Robbins, T.W., Everitt, B.J., 2007. Forebrain connectivity of the prefrontal cortex in the marmoset monkey (Callithrix jacchus): an anterograde and retrograde tract-tracing study. J. Comp. Neurol. 502, 86–112. Robinson, C.J., Burton, H., 1980. Somatotopographic organization in the second somatosensory area of M. fascicularis. J. Comp. Neurol. 192, 43–67. Robinson, D.A., Fuchs, A.F., 1969. Eye movements evoked by stimulation of frontal eye fields. J. Neurophysiol. 32, 637–648. Rosa, M.G.P., Angelucci, A., Jeffs, J., Pettigrew, J.D., 2013. The case for a dorsomedial area in the primate ‘third-tier’ visual cortex. Proc. Biol. Sci. 280, 20121372. Rosa, M.G.P., Elston, G.N., 1998. Visuotopic organisation and neuronal response selectivity for direction of motion in visual areas of the caudal temporal lobe of the marmoset monkey (Callithrix jacchus): middle temporal area, middle temporal crescent, and surrounding cortex. J. Comp. Neurol. 393, 505–527. Rosa, M.G.P., Palmer, S.M., Gamberini, M., Burman, K.J., Yu, H.-H., Reser, D.H., Bourne, J.A., Tweedale, R., Galletti, C., 2009. Connections of the dorsomedial visual area: pathways for early integration of dorsal and ventral streams in extrastriate cortex. J. Neurosci. 29, 4548–4563. Rosa, M.G.P., Palmer, S.M., Gamberini, M., Tweedale, R., Pi␳on, M.C., Bourne, J.A., 2005. Resolving the organization of the New World monkey third visual complex: the dorsal extrastriate cortex of the marmoset (Callithrix jacchus). J. Comp. Neurol. 483, 164–191. Rosa, M.G.P., Schmid, L.M., 1995. Visual areas in the dorsal and medial extrastriate cortices of the marmoset. J. Comp. Neurol. 359, 272–299. Rosa, M.G.P., Tweedale, R., 2000. Visual areas in lateral and ventral extrastriate cortices of the marmoset monkey. J. Comp. Neurol. 422, 621–651. Rozzi, S., Calzavara, R., Belmalih, A., Borra, E.G.G., Matelli, G.M., Luppino, G., 2006. Cortical connections of the inferior parietal cortical convexity of the macaque monkey. Cereb. Cortex 16, 1389–1417. Savaki, H.E., Gregoriou, G.G., Bakola, S., Moschovakis, A.K., 2014. Topography of visuomotor parameters in the frontal and premotor eye fields. Cereb. Cortex, http://dx.doi.org/10.1093/cercor/bhu106. Scangos, K.W., Aronberg, R., Stuphorn, V., 2013. Performance monitoring by presupplementary and supplementary motor area during an arm movement countermanding task. J. Neurophysiol. 109, 1928–1939. Schall, J.D., Morel, A., Kaas, J.H., 1993. Topography of supplementary eye field afferents to frontal eye field in macaque: implications for mapping between saccade coordinate systems. Vis. Neurosci. 10, 385–393. Schall, J.D., Morel, A., King, D.J., Bullier, J., 1995. Topography of visual cortex connections with frontal eye field in macaque: convergence and segregation of processing streams. J. Neurosci. 15, 4464–4487. Schlag, J., Schlag-Rey, M., 1987. Evidence for a supplementary eye field. J. Neurophysiol. 57, 179–200. Seltzer, B., Pandya, D.N., 1989. Frontal lobe connections of the superior temporal sulcus in the rhesus monkey. J. Comp. Neurol. 281, 97–113. Sereno, M.I., Huang, R.S., 2014. Multisensory maps in parietal cortex. Curr. Opin. Neurobiol. 24, 39–46. Shima, K., Tanji, J., 1998. Role for cingulate motor area cells in voluntary movement selection based on reward. Science 282, 1335–1338. Shima, K., Tanji, J., 2000. Neuronal activity in the supplementary and presupplementary motor areas for temporal organization of multiple movements. J. Neurophysiol. 84, 2148–2160. Shriver, J.E., Matzke, H.A., 1965. Corticobulbar and corticospinal tracts in the marmoset monkey (Oedipomidas oedipus). Anat. Rec. 151, 416. Solomon, S.G., Rosa, M.G., 2014. A simpler primate brain: the visual system of the marmoset monkey. Front Neural Circuits. 8, 96. Stepniewska, I., Gharbawie, O.A., Burish, M.J., Kaas, J.H., 2014. Effects of muscimol inactivations of functional domains in motor, premotor, and posterior parietal cortex on complex movements evoked by electrical stimulation. J. Neurophysiol. 111, 1100–1119. Stepniewska, I., Preuss, T.M., Kaas, J.H., 1993. Architectonics, somatotopic organization, and ipsilateral cortical connections of the primary motor area (M1) of owl monkeys. J. Comp. Neurol. 330, 238–271.

Stepniewska, I., Preuss, T.M., Kaas, J.H., 2006. Ipsilateral cortical connections of dorsal and ventral premotor areas in New World owl monkeys. J. Comp. Neurol. 495, 691–708. Sur, M., Nelson, R.J., Kaas, J.H., 1982. Representations of the body surface in cortical areas 3b and 1 of squirrel monkeys: comparisons with other primates. J. Comp. Neurol. 211, 177–192. Sussman, R.W., Kinzey, W.G., 1984. The ecological role of the callitrichidae: a review. Am. J. Phys. Anthropol. 64, 419–449. Tanaka, M., Fukushima, K., 1998. Neuronal responses related to smooth pursuit eye movements in the periarcuate cortical area of monkeys. J. Neurophysiol. 80, 28–47. Tanji, J., 1996. New concepts of the supplementary motor area. Curr. Opin. Neurobiol. 6, 782–787. Tanji, J., Kurata, K., 1982. Comparison of movement-related activity in two cortical motor areas of primates. J. Neurophysiol. 48, 633–653. Tanji, J., Shima, K., 1994. Role for supplementary motor area cells in planning several movements ahead. Nature 371, 413–416. Tanne-Gariepy, J., Rouiller, E.M., Boussaoud, D., 2002. Parietal inputs to dorsal versus ventral premotor areas in the macaque monkey: evidence for largely segregated visuomotor pathways. Exp. Brain Res. 145, 91–103. Taoka, M., Toda, T., Iriki, A., Tanaka, M., Iwamura, Y., 2000. Bilateral receptive field neurons in the hindlimb region of the postcentral somatosensory cortex in awake macaque monkeys. Exp. Brain Res. 134, 139–146. Taoka, M., Toda, T., Iwamura, Y., 1998. Representation of the midline trunk, bilateral arms, and shoulders in the monkey postcentral somatosensory cortex. Exp. Brain Res. 123, 315–322. Thier, P., Andersen, A., 1998. Electrial microstimulation distinguishes distinct saccade-related areas in the posterior parietal cortex. J. Neurophysiol. 80, 1713–1735. Tokuno, H., Takada, M., Nambu, A., Inase, M., 1997. Reevaluation of ipsilateral corticocortical inputs to the orofacial region of the primary motor cortex in the macaque monkey. J. Comp. Neurol. 389, 34–48. Ungerleider, L.G., Courtney, S.M., Haxby, J.V., 1998. A neural system for human visual working memory. Proc. Natl. Acad. Sci. U. S. A. 95, 883–890. van der Steen, J., Russell, I.S., James, G.O., 1986. Effects of unilateral frontal eye-field lesions on eye-head coordination in monkey. J. Neurophysiol. 55, 696–714. Vann, S.D., Aggleton, J.P., Maguire, E.A., 2009. What does the retrosplenial cortex do? Nat. Rev. Neurosci. 10, 792–802. Virley, D., Hadingham, S.J., Roberts, J.C., Farnfield, B., Elliott, H., Whelan, G., Golder, J., David, C., Parsons, A.A., Hunter, A.J., 2004. A new primate model of focal stroke: endothelin-1-induced middle cerebral artery occlusion and reperfusion in the common marmoset. J. Cereb. Blood Flow Metab. 24, 24–41. Vogt, B.A., Finch, D.M., Olson, C.R., 1992. Functional heterogeneity in cingulate cortex: the anterior executive and posterior evaluative regions. Cereb. Cortex 2, 435–443. Vogt, B.A., Laureys, S., 2005. Posterior cingulate, precuneal and retrosplenial cortices: cytology and components of the neural network correlates of consciousness. Prog. Brain Res. 150, 205–217. Wang, Y., Shima, K., Isoda, M., Sawamura, H., Tanji, J., 2002. Spatial distribution and density of prefrontal cortical cells projecting to three sectors of the premotor cortex. Neuroreport 13, 1341–1344. Wardak, C., Vanduffel, W., Orban, G.A., 2010. Searching for a salient target involves frontal regions. Cereb. Cortex 20, 2464–2477. Watanabe-Sawaguchi, K., Kubota, K., Arikuni, T., 1991. Cytoarchitecture and intrafrontal connections of the frontal cortex of the brain of the hamadryas baboon (Papio hamadryas). J. Comp. Neurol. 311, 108–133. Wilson, F.A., Scalaidhe, S.P., Goldman-Rakic, P.S., 1993. Dissociation of object and spatial processing domains in primate prefrontal cortex. Science 260, 1955–1958. Wise, S.P., Boussaoud, D., Johnson, P.B., Caminiti, R., 1997. Premotor and parietal cortex: corticortical connectivity and combinatorial computations. Annu. Rev. Neurosci. 20, 25–42. Yamane, J., Nakamura, M., Iwanami, A., Sakaguchi, M., Katoh, H., Yamada, M., Momoshima, S., Miyao, S., Ishii, K., Tamaoki, N., Nomura, T., Okano, H.J., Kanemura, Y., Toyama, Y., Okano, H., 2010. Transplantation of galectin-1-expressing human neural stem cells into the injured spinal cord of adult common marmosets. J. Neurosci. Res. 88, 1394–1405. Yokochi, H., Tanaka, M., Kumashiro, M., Iriki, A., 2003. Inferior parietal somatosensory neurons coding face-hand coordination in Japanese macaques. Somatosens. Mot. Res. 20, 115–125. Yu, H.H., Chaplin, T.A., Davies, A.J., Verma, R., Rosa, M.G.P., 2012. A specialized area in limbic cortex for fast analysis of peripheral vision. Curr. Biol. 22, 1351–1357.

Please cite this article in press as: Bakola, S., et al., The cortical motor system of the marmoset monkey (Callithrix jacchus). Neurosci. Res. (2014), http://dx.doi.org/10.1016/j.neures.2014.11.003

The cortical motor system of the marmoset monkey (Callithrix jacchus).

Precise descriptions of the anatomical pathways that link different areas of the cerebral cortex are essential to the understanding of the sensorimoto...
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