0736s748/91$3.00+0.00 Pergamon Press plc @ 1991ISDN

Inc. J. Devf. Neuroscience,Vol. 9, No. 5, pp. 479-491, 1991. Printed in Great Britain.

CONNECTIONS OF THE INSULAR CORTEX IN KITTENS: AN ANATOMICAL DEMONSTRATION WITH WHEATGERM AGGLUTININ CONJUGATED TO HORSERADISH PEROXIDASE TECHNIQUE HIDEAKI SHIMIZU* and MASAO NowTAt Department

of Anatomy and Embryology, Tokyo Metropolitan Institute for Neurosciences, Fuchu Tokyo 183, Japan (Received 28 November 1990; accepted 28 February 1991)

Abstract-The postnatal development of the afferent and efferent connections of the feline insular cortex was investigated using wheat germ agglutinin conjugated to horseradish peroxidase method. The overall pattern of connections was found to be substantially the same as that observed in adults. In the cortex, anterograde and retrograde labeling was found in the presylvian sulcus, cingulate gyrus, cruciate sulcus, mediat prefrontal area, lateral suprasylvian cortex, and posterior rhinal sulcus. Subcortical regions ~ntaining label included the lateralis mediali~suprageni~late nuclear complex, ventral medial thalamic nucleus, claustrum, lateral amygdaloid nucleus, hypothalamus, and raphe nuclei. In addition, axonal labeling was seen in the striatum, superior colliculus, and pontine nuclei. In contrast, the insular associational projections in kittens differed markedly from those found in adults. In the early postnatal period (1-14 days), dense terminal labeling was found in the cortical layers I, V and VI as well as in the underlying white matter, whereas only moderate to sparse labeling was observed in layers II, III and IV. By four-weeks, an adult-like distribution of terminals was present in each cortical areas: labeling was found mainly in layers I, II, III and IV, with less in layers V and VI. The present results suggest that the basic framework of the insular connections is formed prenatally and that the fine tuning of the axonal terminals and the formation of synapses occurs mainly during the first four postnatal weeks. Key wordr insular cortex, development, WGA-HRP, neonatal cat.

corticocortical

connections,

corticosubcortical

connections,

The development of the connections of various cortical sensory areas (e.g., visual cortex 1,6,15~‘8,31-35 auditory cortex6v33 and sensorimotor cortex22*43) has received considerable attentibn. A consistent finding is that while most of cortical projections are present at birth, considerable modification occurs during postnatal development. The insular cortex of the cat is situated on the anterior sylvian gyrus and is surrounded by the anterior ectosylvian sulcus dorsally, and the anterior rhinal sulcus and the sylvian sulcus ventrally. *’ Recently a distinct region within the insular cortex has been shown to be associated with the extragenicdlate visual system on the basis of anatomica1,7~‘6~2s~29~36,40 electrophysioand behavioral findings, 4,s However, data regarding the development and logical, 2*3~8~17*2s~26-31 postnatal maturation of the insular cortex is still sparse,6 especially when compared to other visual cortical regions. The purpose of the present study was, therefore, to investigate the postnatal development of the afferent and efferent connections of insular cortex using the wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP) technique, A preliminary report describing some of these findings has been published in abstract form.*’ EXPERIMENTAL

PROCEDURES

Twenty kittens between 1 and 56 days of age (birth on day 1) and two adult cats (1.7 and 2.8 kg) were used (see Table 1). The animals were anesthetized with sodium pentobarbital (35 mg/kg, i.p.) and placed in a stereotaxic head-holder frame. The body temperature was kept at 37-38°C by a thermostatically controlled heating pad placed under the body. The skull overlying the insular cortex was opened with a high-speed drill, and the dura was retracted. Pressure injections of *Dr H. Shimizu was on leave from Dept. Internal Medicine, Hamamatsu University School of Medicine, Hamamatsu Shizuoka 431-31, Japan. tAuthor to whom correspondence should be addressed. Abbreviations: LS, lateral suprasylvian cortex; SC, superior colliculus; WGA-HRP, wheat germ agglutinin conjugated to horseradish peroxidase.

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H. Shimizu and M. Notita Table 1. Summary of age at injection (birth on day 1). amount of WGAHRP injected and survival time for each cat examined Animal EXO-49 EXO-50 EXO-35 EXO-25 EXO-37 EXO-19 EXO-20 EXO-21 EXO-22 EXO-26 EXO-54 EXO-11 EXO-12 EXO-55 EXO-7 EXO-9 EXO-10 EXO-44 EXO-47 EXO-74 EXO-71 PGM-26

Age at operation (days)

Amount of WGA-HRP (CL])

Survival time (hours)

0.04

7 13 14 20 21 21 23 33 33 45 49 56 adult adult

0.03 0.02 0.01 0.02 0.03 0.03 0.02 0.02 0.01 0.04 0.03 0.03 0.05 0.03 0.03 0.03 0.04 0.07 0.03 0.05 0.02

4x 45 39 48 46 14 43 4.4 42 11 33 4-l 48 44 46 36 4s 4x 45 47 44 48

0.01-0.07 ~1 of 2% WGA-HRP (Sigma) dissolved in physiological saline were made through a glass micropipette (tip diameter 50-80 pm) attached to a l+l Hamilton syringe. The injection syringe was angled laterally in order to avoid injury to the adjacent white matter. After survival periods of 1 S-2 days, the animals were reanesthetized with an overdose of sodium pentobarbital and perfused transcardially with phosphate buffered 0.9% saline followed by a fixative containing 0.5% paraformaldehyde and 2.5% glutaraldehyde in 0.1 M phosphate buffer at pH 7.4. The fixative was removed by perfusion with a solution of 10% sucrose in 0.1 M phosphate buffer. The brains were removed immediately and stored for 1 day in a 30% solution of sucrose. Brains were blocked and sectioned coronally on a freezing microtome at 50 Frn. Every 4th section was selected for the following incubation procedures. The visualization of WGA-HRP was achieved by incubasections were tion with tetramethyl benzidine according to Mesulam et a1.24 WGA-HRP-reacted counterstained lightly with neutral red and examined microscopically under dark- or bright-field illumination. To aid in the identification of thalamic nuclei, adjacent sections were stained for acetylcholinesterase according to the method of Lewis and Shute.*’ Nomenclature for the thalamic nuclei was adapted from Graybiel and Berson,” while the delineation of the insular cortex was after Krettek and Price.” The laminar distribution of anterogradely transported WGA-HRP was analyzed quantitatively. Five sections of the representative cortical areas (see Results) were selected from animals of each age group. The number of HRP grains present in a 4000 km* rectangle with a single lamina were counted. The presence of retrogradely-labeled neurons and their neurites prevented unequivocal Abbreviations used in figures

AEs ARhs Cl CL cos Crs LG LM-Sg LPI LPm Ls

anterior ectosylvian sulcus anterior rhinal sulcus claustrum central lateral nucleus coronal sulcus cruciate sulcus lateral geniculate body lateralis medialis-suprageniculate nuclear complex nucleus lateralis posterior, pars lateralis nucleus lateralis posterior, pars medialis lateral sulcus

MD MG MSs PRhs PSS Pt Pul SC Sps VB VL VM

nucleus mediodorsalis medial geniculate body middle suprasylvian sulcus posterior rhinal sulcus presylvian sulcus pretectum pulvinar superior colliculus splenial sulcus ventrobasal complex ventral lateral nucleus ventral medial nucleus

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but care was taken not to count intracellular HRP grains. The cortex and underlying white matter was divided into four regions which included layer I, layers II-IV, layers V-VI, and subjacent white matter. Then the relative density (the total value of the four being 100%) of each component was calculated for ease of comparison. observation,

RESULTS Eight representative cases (EXO-10, -21, -35, -44, -47, -50, -54, -55) were selected to illustrate the general pattern of postnatal maturation. The relative position and extent of the WGA-HRP deposits are depicted schematically in Fig. 1; photomicrographs of corresponding representative cases are shown in Fig. 2. In each case, the injected tracer was restricted largely within the insular cortex. The distribution of retrogradely-labeled cells and anterogradely-labeled axon terminals was virtually identical in all of these cases. For clarity, case EXO-35 will be used as a representative case of cortical and subcortical connections in order to avoid unnecessary repetition.

Fig. 1. Lateral view of the left hemisphere showing the extent of the WGA-HRP injection in cases younger than 14 days old (left) and those older than 21 days old (right).

Cortical connections Numerous retrogradely-labeled cells and anterogradely-labeled terminals were found in the presylvian sulcus, lateral suprasylvian cortex (LS), cruciate sulcus, and posterior rhinal sulcus. Moderate labeling was seen in the anterior ectosylvian gyrus, posterior suprasylvian gyrus, medial prefrontal area, cingulate gyrus, and splenial sulcus. Light labeling was observed in the coronal sulcus, sigmoid gyrus, and the anterior part of the lateral sulcus (Fig. 3). The labels were distributed bilaterally, but were predominant ipsilaterally. The laminar distribution of terminal labeling in each of the areas changed with postnatal maturation (see below) while the labeled cells were located mainly in the supragranular layers, with a sparse distribution in the infragranular layers in all cases. Subcortical connections In the thalamus (Fig. 4), numerous retrogradely-labeled neurons and anterogradely-labeled terminals were seen in the lateralis medialis-suprageniculate nuclear complex and the ventral medial nucleus. Moderate to sparse labeling was found in the ventrobasal complex, the dorsal part of medial geniculate body, mediodorsal nucleus, the medial division of the lateral posterior nucleus, and central lateral nucleus. Sparse labeling was also observed in the lateral and posterior hypothalamic area, lateral amygdaloid nucleus, claustrum, diagonal band of Broca, area septalis, subthalamic nucleus, and raphe nuclei. Only anterogradely-labeled terminals were found in the striatum (caudate nucleus and putamen), superior colliculus (SC), and pontine nuclei (Fig. 4). In the striatum, label was seen mainly in the posterior two-thirds of the head of the caudate nucleus and the middle part of the putamen. In the superior colliculus, the labeling was found in and around the intermediate and deep gray layers through the rostrocaudal extent. The labeling described above was ipsilateral in thalamic and hypothalamic regions, while in other structures the labeling was bilateral with ipsilateral labeling predominant.

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Fig. 3. Schematic drawings showing the injection site of WGA-HRP and distribution of labeling in the cerebral cortex of the representative case EXO35. The WGA-HRP injection site is depicted in black and representation of the distribution of its diffusion is shown b cross-hatchin . Upper right: di~~atic retrogradely labeled ce rIs (dots) in the f ateral and medial views of the cerebral hemisphere, reconstructed from serial sections. Center: coronal sections, showing the distribution of labekd cells (dots) in the cerebral cortex. One dot represents two to four labeled c&k. Arabic numerals refer to the section number frontal levels are shown as the vertical tines of the lateral and medial views. Lower left:

Insular connections

in kittens

Fig. 2. Bright-field photomicrographs showing WGA-HRP injection sites in the insular cortex of ‘L-dayold kitten (A: case EXO-351 and adult (B: case PGM-261. The reaction nroduct of the former was . slightly spread into underling white matter and claustrum, whereas that of the latter was confined in the insular cortex. Stained with neutral red. Bar = I mm.

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Fig. 4. Schematic drawings showing distribution of retrogradely labeled cells (large dots) and anterogradely labeled terminals (small dots) in the caudate nucleus (CN), putamen (Put), thalamus and superior colliculus of the representative case EXO-35 in coronal sections. Arabic numerals refer to the section number and D, M indicate the dorsal, medial direction, respectively. In the caudate nucleus and putamen, the labeled terminals are distributed throughout these structures. The thalamic labeling is densest by far in VM and LM-Sg.

Developmental changes As described above, the basic pattern of corticocortical and corticosubcortical connections of the insular cortex in the l-day-old kitten was the same as adult; no marked differences of the area1 distributions were found irrespective of age. Moreover, the laminar distribution of the retrogradely-labeled cells in the kitten was essentially the same as that in the adult. There were, however, marked differences in the laminar distributions of labeled terminals between kittens and adults. In order to assess the postnatal maturational changes in the laminar distribution of labeled terminals, we examined three cortical areas that are known to be intimately associated with insular cortex. The first region was the medial wall of the presylvian sulcus, which is a part of the frontal eye field; i1*i2the second was the lateral wall of the LS which is a part of the lateral supra-

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Fig. 5. Postnatal changes of the laminar distribution of labeled terminals in the medial bank of presylvian sulcus (upper), the lateral bank of lateral suprasylvian cortex (middle), and the lateral bank of posterior rhinal sulcus (lower) after WGA-HRP injections into the insular cortex. In cases younger than 14-dayold (open circle, open square, open triangle), the relative density is higher in layers I, V, VI and underlying white matter, whereas in cases older than 49-day-old (filled square, filled triangle), it tends to be higher in layers I-IV.

sylvian visual area;32 and the third was the lateral bank of the posterior rhinal sulcus which is a part of perirhinal cortex.44.4s A summary of the observations in this layer analysis is shown in Fig. 5. In all three cases, the laminar pattern of the labeling changed with maturation. In animals younger than 14 days (e.g., EXO-21, -50, -54), labeled terminals were distributed densely in layers I, V and VI and underlying white matter, but moderately in layers II-IV (Fig. 6A). In contrast, in animals older than 49 days (e.g., EXO-47, PGM-26), the incidence of labeled terminals increased in layers II-IV and decreased in layers V-VI and underlying white matter, so that the supragranular layers were more densely labeled than infragranular layers and underlying white matter (Fig. 6B). There appeared to be a similar tendency in the laminar distribution of labeled terminals for the other corticocortical projections.

Insular connections

in kittens

Fig. 6. Dark-field photomicrographs of anterograde and retrograde labeling of l-day-old kitten (A: EXO-50) and 4%day-old kitten (B: EXO-47) in the lateral bank of the middle suprasylvian sulcus following tracer injections into the insular cortex. Retrogradely labeled cells are located mainly in the supragranular layers in both cases. In the l-day-old kitten, labeled terminals are found predominantly in layers I, V, VI and underlying white matter, whereas in the 49-day-old kitten, labeled terminals are seen mainly in Iayers I-IV. Boundaries of cortical layers are indicated by Roman numerals. Bar = 100 pm.

487

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DISCUSSION The present investigation has produced two principal findings. First, the area1 distribution of the insular connections are adult-like at the time of birth. Second, the laminar distribution of the corticocortical projections changes during the first four postnatal weeks. The area1 distribution The afferent and efferent connections of the insular cortex were present at the time of birth in the present study. Thus, our observations in newborns and adults are in general agreement with a number of previous horseradish peroxidase studies on the insular connections in adult cats (for example, see Refs 13, 14, 28, 29). have studied the development of the connections of the Previous investigators 1~6~*5~18~22*33-35~43 visual, auditory, and sensorimotor cortex in the cat. They have shown that many connections are established during late fetal maturation. Thus, the basic pattern of these connections is in place at the time of birth. However, many regions are known to undergo significant postnatal changes. For example, Price and Zumbroich 35 have observed that the basic pattern of the corticocortical projections from area 17 to areas 19,21a, and the LS is not fully established until 12 days of age. With regard to the present findings, we could not find any postnatal change of the basic pattern. Since the insular cortex is associational cortex, which integrates visual, auditory, sensorimotor, and other inputs, it is reasonable to suppose that its connections are necessary for the highly organized behavior which is already present at birth. The laminar distribution

We have described here a marked progressive change in the laminar distribution of corticocortical fibers in the kitten, especially during the first four postnatal weeks. The present findings revealed that corticocortical projections from the insular cortex terminate mainly in layers I, V and VI and underlying white matter in kittens, whereas they terminate mainly in the supragranular layers in older kittens and adults. Some studies exist about the postnatal development of the axonal terminals of the corticocortical projections in the visual system. Kato et all8 reported that the cortical projections from areas 17 and 18 to the LS in kittens younger than 2 weeks were distributed in both superficial and deep cortical layers, whereas those in kittens older than 1 month and in adults were distributed only in deep layers. Price and Zumbroich3’ observed the projections from area 17 to areas 18 and 19 and the LS. They found that the terminals were initially located in the infragranular layers, but during the second and third postnatal weeks, the terminals began to appear in more superficial layers, and by 70 days, an adult-like distribution of terminals was found in each extrastriate area. These two studies of striate cortical projections showed different results, and our results differ significantly from both. Thus, the insular associational projections described here may be at a different level in the ‘hierarchy’ of the visual system, so that the details of the terminal pattern also differ (see Results). Nevertheless it is of interest that the development of the laminar change occurred mainly in the first and second postnatal months. We could not detect any developmental changes in subcortical structures; these may be more precisely specified and rigidly determined by the time of birth than projections to other cortical areas. However, it is worth remarking that there are several studies which show postnatal development of the corticosubcortical terminals.4*‘42 There is still the possibility of postnatal changes of the corticosubcortical connections which we could not observe in our experiments. Finally, we try to consider a possible functional role for insular association projections in relation to the visual development. The insular cortex has interconnections with the LS.‘3*14.26*28,29,31.36*40 Both the insula and the LS send projections to the deep layers of the SC’9.28.29.37 which mediate behaviors that orient the eyes, pinnae, and head toward the source of visual, auditory and somatosensory stimuli. 23*38Previous electrophysiological studies30*39have reported that the visual response properties, such as direction selectivity, of the SC neurons first appear at the end of the second week, and the proportion of such specific cells becomes virtually adult-like by the fourth week, suggesting that the maturation of visual response properties of the SC neurons depends on the postnatal development of corticotectal cells.42 Furthermore, behavioral study has shown that the visual orientation, consisting of head turning toward a

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laterally placed light and visual following, is first seen at postnatal 14 days and is well developed in the third week of life.’ From the present findings, together with previous electrophysiological and behavioural data, it is strongly suggested that the insular cortex plays a role in orientation behavior. Acknowledgements-The

authors wish to acknowledge with gratitude the technical assistance of MS Megu Odagiri.

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Connections of the insular cortex in kittens: an anatomical demonstration with wheatgerm agglutinin conjugated to horseradish peroxidase technique.

The postnatal development of the afferent and efferent connections of the feline insular cortex was investigated using wheat germ agglutinin conjugate...
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