Motor Control, 2015, 19, 135 -141 http://dx.doi.org/10.1123/mc.2014-0055 © 2015 Human Kinetics, Inc.
COMMENTARIES
Neural Control of Hand Movements Monica A. Perez University of Pittsburgh Most of our daily actions involve movements of the hand. The neuronal pathway contributing to the control of hand movements are complex and not yet completely understood. Recent studies highlight how task-dependent changes in cortical and subcortical pathways driven by contralateral and ipsilateral influences may open avenues to further understand the complexity of hand actions in healthy and disease. In the following section studies using transcranial magnetic and electrical stimulation in healthy subjects and in individuals with chronic incomplete spinal cord injury will be highlighted to further understand neuronal pathways involved in the control of voluntary activity by hand muscles. Keywords: voluntary contraction, corticospinal drive, spinal motoneurons, primary motor cortex, precision grip, spinal cord injury
The neural control of precision hand movements has been associated with the contribution of the primary motor cortex (M1) and the corticospinal system (for review see Lemon, 2008). Electrophysiological studies in primates showed that monosynaptic corticomotoneuronal cells are significantly active during tasks requiring fractionated digit movements (Buys et al., 1986; Bennett & Lemon, 1996). Lesions of the M1 or the corticospinal tract at the brainstem level impaired dexterous finger movements (Lawrence & Kuypers, 1968; Galea & Darian-Smith, 1997; Zaaimi et al., 2012; Hoogewoud et al., 2013). Studies also have shown differences in the organization of rostral and caudal regions of the M1 based on the distribution of corticomotoneuronal cells, which might have broad implications for the generation and control of hand movements (Rathelot & Strick, 2006, 2009). Most corticospinal tract neurons located in the rostral region of the M1 made monosynaptic connections with interneurons in the intermediate region of the spinal cord, whereas corticospinal tract neurons in the caudal region made monosynaptic connections with motoneurons. It has been argued that the direct connection to motoneurons might enable a more flexible and complex pattern of muscle activity than less indirect inputs. In humans, the contribution of the M1 and the corticospinal system to the control of hand movements has been demonstrated in patients with damage to these CNS structures which results in a reduced ability to perform individuated finger movements (Lang and Schieber, 2003, 2004). Transcranial magnetic stimulation The author is with the Dept. of Physical Medicine and Rehabilitation, University of Pittsburgh, Pittsburgh, PA. Address author correspondence to Monica A. Perez at [email protected]. 135
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(TMS) has been employed for noninvasive and painless stimulation of the hand representation of the M1 of intact and injured subjects through the scalp. TMS has been used most extensively in the corticospinal system since the output of the motor cortex can be easily assessed in the form of a motor evoked potential (MEP) by using surface electromyographic (EMG) recording electrodes. Experimental studies using TMS have suggested that both the M1 contralateral and ipsilateral to a moving hand contribute to the generation of EMG responses in hand muscles in a task-specific manner. For example, during unilateral voluntary contraction of intrinsic finger muscles an increase in the amplitude of MEPs in finger muscles and a decrease in the magnitude of short (SICI) and long (LICI) interval intracortical inhibition compared with rest can be found (Wassermann et al., 1996; Ortu et al., 2008; Kouchtir-Devanne et al., 2012). The changes in SICI and LICI suggest that GABAergic activity is significantly weaker during voluntary activity compared with rest, which may contribute to modulation of excitability of corticospinal neurons involved in the intended movement. Interestingly, patients with chronic incomplete cervical spinal cord injury (SCI) showed a descrease in SICI (probably involving GABAA receptors) but not LICI (probably involving GABAB receptors) during small levels of isometric voluntary contraction with intrinsic finger muscles (Barry et al., 2013; Figure 1). The results from this study demonstrated that longterm use of baclofen selectively maintained activity of largely subcortical but not cortical GABAergic neuronal pathways during voluntary activity involving finger muscles after human SCI. Therefore, cortical GABAA circuits may be less sensitive to baclofen than spinal GABAB circuits, which might to some extent contribute to the limited effects of baclofen on voluntary motor output, including hand function, in subjects with motor disorders affected by spasticity. More recent studies proposed that subcortical neuronal networks also make a significant contribution to the control of precision hand movements. Single unit recordings in primates demonstrated that spinal interneurons exert postspike effects in hand muscles during a precision grip in a task-dependent manner (Takei & Seki, 2010, 2013). Lesions of the corticospinal tract at the cervical spinal cord level showed in most cases complete recovery of the ability to grasp with the index finger and thumb (Sasaki et al., 2004; Alstermark et al., 2011) which most likely reflects central compensatory mechanisms underlying the recovery of finger dexterity (for review see Isa et al., 2013). In agreement, a recent study demonstrated that the control of precision grip in humans involves premotoneuronal subcortical mechanisms, which are deficient in patients with SCI and restored by long-term use of baclofen (Bunday et al., 2014). Thus, spinal GABAergic interneuronal circuits might be part of the subcortical premotoneuronal network shaping corticospinal output during human skilled hand actions. Spinal neuronal circuits, which can rapidly translate and shape inputs and outputs according to behavioral contexts (Cheney and Fetz, 1980; Prut and Perlmutter, 2003), might represent a critical source for the control of skilled hand movements. Evidence has shown that the M1 ipsilateral to a moving hand also contributes to the control of hand movements. During unilateral isometric voluntary contraction of intrinsic finger muscles, the excitability in the M1 that controls the resting hand changes in a task-dependent manner (Stedman, Davey, & Ellaway, 1998; Muellbacher et al., 2000; Perez & Cohen, 2008, 2009). A possible functional role of these interactions is to suppress unwanted EMG activity in the resting limb through interhemispheric MC Vol. 19, No. 2, 2015
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Figure 1 — The effect of voluntary contraction of intracortical inhibition in healthy controls and patients with SCI. Short-interval intracortical inhibition (SICI, A) and long-interval intracortical inhibition (LICI, B) were recorded at rest and during 25% of maximal voluntary contraction (MVC) of the first dorsal interosseous muscle. Traces show MEPs elicited at rest (top) and during 25% of MVC (bottom). Black and gray traces represent test MEP and conditioned MEP, respectively. Conditioning stimulation (black arrows) preceded test stimulation (gray arrows) by 2 ms for SICI and 100 ms for LICI. Note that SICI was decreased during voluntary contraction compared with at rest in both healthy controls and in SCI patients. However, LICI was decreased during voluntary contraction compared with at rest in healthy controls but not in SCI patients. (Modified with permission from Barry et al., 2013).
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Figure 2 — Ipsilateral silent period (iSP) during movement execution. A, B. Raw traces showing rectified EMG in representative subjects during iSP testing in self-paced and ballistic index finger (left traces) and elbow flexion (right traces) movements. Traces show the average 40 trials tested with (gray traces) and without (black traces) TMS. Traces below iSPs show the rectified EMG and angular displacement during each movement condition. Vertical solid lines show the time of TMS during testing and vertical dashed lines show onset and offset of the iSP. C, D. Group data (index finger task, n = 14, C; elbow task, n = 11, D). The abscissa shows all conditions tested (self-paced and ballistic). The ordinate shows the normalized iSP area. Note the increased in the iSP during ballistic index finger and elbow movements compared with self-paced movements. Error bars indicate SEs. *p < .05. (Modified with permission from Tazoe and Perez, 2013). 138
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inhibitory pathways (Cincotta & Ziemann, 2008; Hübers et al., 2008; Beaulé et al., 2012). More recent results showed that during unilateral isotonic hand movements the resting M1 contributes to modulate activity in the contralateral voluntarily active hand also in a task-specific manner (Tazoe and Perez, 2013; Figure 2). It has been shown that the contribution of transcallosal inhibition to ipsilateral movements at different speeds is widespread and has a functional role during rapid movements. Thus, at faster speeds transcallosal inhibition toward the moving hand decreases in the preparatory phase, which might contribute to starting movements rapidly. However, transcallosal inhibition toward the moving hand increases in the execution phase, which may contribute to stopping the movement. It is argued that transcallosal pathways enable signaling of the time of discrete behavioral events during ipsilateral movements, which is amplified by the speed of the movement. Importantly, the contribution of the ipsilateral M1 to modulate corticospinal excitability in the resting hand is impaired in humans with chronic incomplete SCI (Bunday & Perez, 2012; Bunday et al., 2013). In patients, strong voluntary contraction of a hand muscle was able to increase the corticospinal output in the contralateral resting hand, as in healthy controls, when the motoneurons for the hand muscle tested were located above the injury. However this modulation was absent in muscles at or within 5 segments below the injury and present in muscles beyond 5 segments below the injury. Importantly, crossed corticospinal facilitation was aberrantly high in muscles distant (>15 segments) from the injury and accompanied by increased motoneuronal excitability. In summary, the neuronal pathways contributing to the generation and control of hand movements are complex and involve cortical and subcortical structures from the contralateral and ipsilateral sides. Studies points to the view that transmission in pathways contributing to modulation of EMG activity in hand muscles changes in a task-dependent manner, which emphasizes the need for a careful interpretation when extrapolating results between different hand motor actions. Thus, a better understanding of the modulation of pathways contributing to the control of motor skills involving hand muscles may highlight new targets for recovery of the hand function after CNS injury.
References Alstermark, B., Pettersson, L.G., Nishimura, Y., Yoshino-Saito, K., Tsuboi, F., Takahashi, M., & Isa, T. (2011). Motor command for precision grip in the macaque monkey can be mediated by spinal interneurons. Journal of Neurophysiology, 106, 122–126. PubMed doi:10.1152/jn.00089.2011 Barry, M.D., Bunday, K.L., Chen, R., & Perez, M.A. (2013). Selective Effects of Baclofen on Use-Dependent Modulation of GABAB Inhibition after Tetraplegia. The Journal of Neuroscience, 33, 12898–12907. PubMed doi:10.1523/JNEUROSCI.1552-13.2013 Beaulé, V., Tremblay, S., & Théoret, H. (2012). Interhemispheric control of unilateral movement. Neural Plasticity, 2012, 627816. PubMed Bennett, K.M., & Lemon, R.N. (1996). Corticomotoneuronal contribution to the fractionation of muscle activity during precision grip in the monkey. Journal of Neurophysiology, 75, 1826–1842. PubMed Bunday, K.L., & Perez, M.A. (2012). Impaired crossed facilitation of the corticospinal pathway after cervical spinal cord injury. Journal of Neurophysiology, 107, 2901–2911. PubMed doi:10.1152/jn.00850.2011 MC Vol. 19, No. 2, 2015
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Bunday, K.L., Oudega, M., & Perez, M.A. (2013). Aberrant Crossed Corticospinal Facilitation in Muscles Distant from a Spinal Cord Injury. PLoS ONE, 8, e76747. PubMed doi:10.1371/journal.pone.0076747 Bunday, K.L., Tazoe, T., Rothwell, J.C., & Perez, M.A. (in press).Subcortical control of precision grip after human spinal cord injury. The Journal of Neuroscience, 34(21), 7341–7350. PubMed Buys, E.J., Lemon, R.N., Mantel, G.W., & Muir, R.B. (1986). Selective facilitation of different hand muscles by single corticospinal neurones in the conscious monkey. The Journal of Physiology, 381, 529–549. PubMed doi:10.1113/jphysiol.1986. sp016342 Cheney, P.D., & Fetz, E.E. (1980). Functional classes of primate corticomotoneuronal cells and their relation to active force. Journal of Neurophysiology, 44, 773–791. PubMed Cincotta, M., & Ziemann, U. (2008). Neurophysiology of unimanual motor control and mirror movements. Clinical Neurophysiology, 119, 744–762. PubMed doi:10.1016/j. clinph.2007.11.047 Galea, M.P., & Darian-Smith, I. (1997). Manual dexterity and corticospinal connectivity following unilateral section of the cervical spinal cord in the macaque monkey. The Journal of Comparative Neurology, 381, 307–319. PubMed doi:10.1002/(SICI)10969861(19970512)381:33.0.CO;2-6 Hoogewoud, F., Hamadjida, A., Wyss, A.F., Mir, A., Schwab, M.E., Belhaj-Saif, A., & Rouiller, E.M. (2013). Comparison of functional recovery of manual dexterity after unilateral spinal cord lesion or motor cortex lesion in adult macaque monkeys. Frontiers in Neurology, 4, 101. PubMed doi:10.3389/fneur.2013.00101 Hübers, A., Orekhov, Y., & Ziemann, U. (2008). Interhemispheric motor inhibition: its role in controlling electromyographic mirror activity. The European Journal of Neuroscience, 28, 364–371. PubMed doi:10.1111/j.1460-9568.2008.06335.x Isa, T., Kinoshita, M., & Nishimura, Y. (2013). Role of direct vs. indirect pathways from the motor cortex to spinal motoneurons in the control of hand dexterity. Frontiers in Neurology, 4, 191. PubMed doi:10.3389/fneur.2013.00191 Kouchtir-Devanne, N., Capaday, C., Cassim, F., Derambure, P., & Devanne, H. (2012). Task-dependent changes of motor cortical network excitability during precision grip compared to isolated finger contraction. Journal of Neurophysiology, 107, 1522–1529. PubMed doi:10.1152/jn.00786.2011 Lang, C.E., & Schieber, M.H. (2003). Differential impairment of individuated finger movements in humans after damage to the motor cortex or the corticospinal tract. Journal of Neurophysiology, 90, 1160–1170. PubMed doi:10.1152/jn.00130.2003 Lang, C.E., & Schieber, M.H. (2004). Reduced muscle selectivity during individuated finger movements in humans after damage to the motor cortex or corticospinal tract. Journal of Neurophysiology, 91, 1722–1733. PubMed doi:10.1152/jn.00805.2003 Lawrence, D.G., & Kuypers, H.G. (1968). The functional organization of the motor system in the monkey. I. The effects of bilateral pyramidal lesions. Brain, 91, 1–14. PubMed doi:10.1093/brain/91.1.1 Lemon, R.N. (2008). Descending pathways in motor control. Annual Review of Neuroscience, 31, 195–218. PubMed doi:10.1146/annurev.neuro.31.060407.125547 Ortu, E., Deriu, F., Suppa, A., Tolu, E., & Rothwell, J.C. (2008). Effects of volitional contraction on intracortical inhibition and facilitation in the human motor cortex. The Journal of Physiology, 586, 5147–5159. PubMed doi:10.1113/jphysiol.2008. 158956 Muellbacher, W., Facchini, S., Boroojerdi, B., & Hallett, M. (2000). Changes in motor cortex excitability during ipsilateral hand muscle activation in humans. Clinical Neurophysiology, 111, 344–349. PubMed doi:10.1016/S1388-2457(99)00243-6 Perez, M.A., & Cohen, L.G. (2009). Scaling of motor cortical excitability during unimanual force generation. Cortex, 45, 1065–1071. PubMed doi:10.1016/j.cortex.2008.12.006 MC Vol. 19, No. 2, 2015
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Perez, M.A., & Cohen, L.G. (2008). Mechanisms underlying functional changes in the primary motor cortex ipsilateral to an active hand. The Journal of Neuroscience, 28, 5631–5640. PubMed doi:10.1523/JNEUROSCI.0093-08.2008 Prut, Y., & Perlmutter, S.I. (2003). Firing properties of spinal interneurons during voluntary movement. I. State-dependent regularity of firing. The Journal of Neuroscience, 23, 9600–9610. PubMed Rathelot, J.A., & Strick, P.L. (2006). Muscle representation in the macaque motor cortex: an anatomical perspective. Proceedings of the National Academy of Sciences of the United States of America, 103, 8257–8262. PubMed doi:10.1073/pnas.0602933103 Rathelot, J.A., & Strick, P.L. (2009). Subdivisions of primary motor cortex based on corticomotoneuronal cells. Proceedings of the National Academy of Sciences of the United States of America, 106, 918–923. PubMed doi:10.1073/pnas.0808362106 Sasaki, S., Isa, T., Pettersson, L.G., Alstermark, B., Naito, K., Yoshimura, K., . . . Ohki, Y. (2004). Dexterous finger movements in primate without monosynaptic corticomotoneuronal excitation. Journal of Neurophysiology, 92, 3142–3147. PubMed doi:10.1152/ jn.00342.2004 Stedman, A., Davey, N.J., & Ellaway, P.H. (1998). Facilitation of human first dorsal interosseous muscle responses to transcranial magnetic stimulation during voluntary contraction of the contralateral homonymous muscle. Muscle & Nerve, 21, 1033–1039. PubMed doi:10.1002/(SICI)1097-4598(199808)21:83.0.CO;2-9 Takei, T., & Seki, K. (2010). Spinal interneurons facilitate coactivation of hand muscles during a precision grip task in monkeys. The Journal of Neuroscience, 30, 17041–17050. PubMed doi:10.1523/JNEUROSCI.4297-10.2010 Takei, T., & Seki, K. (2013). Spinal premotor interneurons mediate dynamic and static motor commands for precision grip in monkeys. The Journal of Neuroscience, 33, 8850–8860. PubMed doi:10.1523/JNEUROSCI.4032-12.2013 Tazoe, T., & Perez, M.A. (2013). Speed-Dependent Contribution of Callosal Pathways to Ipsilateral Movements. The Journal of Neuroscience, 33, 16178–16188. PubMed doi:10.1523/JNEUROSCI.2638-13.2013 Wassermann, E.M., Samii, A., Mercuri, B., Ikoma, K., Oddo, D., Grill, S.E., & Hallett, M. (1996). Responses to paired transcranial magnetic stimuli in resting, active, and recently activated muscles. Experimental Brain Research, 109, 158–163. PubMed doi:10.1007/BF00228638 Zaaimi, B., Edgley, S.A., Soteropoulos, D.S., & Baker, S.N. (2012). Changes in descending motor pathway connectivity after corticospinal tract lesion in macaque monkey. Brain, 135, 2277–2289. PubMed doi:10.1093/brain/aws115
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COMMENTARIES
Neural Control of Hand Movements Monica A. Perez University of Pittsburgh Most of our daily actions involve movements of the hand. The neuronal pathway contributing to the control of hand movements are complex and not yet completely understood. Recent studies highlight how task-dependent changes in cortical and subcortical pathways driven by contralateral and ipsilateral influences may open avenues to further understand the complexity of hand actions in healthy and disease. In the following section studies using transcranial magnetic and electrical stimulation in healthy subjects and in individuals with chronic incomplete spinal cord injury will be highlighted to further understand neuronal pathways involved in the control of voluntary activity by hand muscles. Keywords: voluntary contraction, corticospinal drive, spinal motoneurons, primary motor cortex, precision grip, spinal cord injury
The neural control of precision hand movements has been associated with the contribution of the primary motor cortex (M1) and the corticospinal system (for review see Lemon, 2008). Electrophysiological studies in primates showed that monosynaptic corticomotoneuronal cells are significantly active during tasks requiring fractionated digit movements (Buys et al., 1986; Bennett & Lemon, 1996). Lesions of the M1 or the corticospinal tract at the brainstem level impaired dexterous finger movements (Lawrence & Kuypers, 1968; Galea & Darian-Smith, 1997; Zaaimi et al., 2012; Hoogewoud et al., 2013). Studies also have shown differences in the organization of rostral and caudal regions of the M1 based on the distribution of corticomotoneuronal cells, which might have broad implications for the generation and control of hand movements (Rathelot & Strick, 2006, 2009). Most corticospinal tract neurons located in the rostral region of the M1 made monosynaptic connections with interneurons in the intermediate region of the spinal cord, whereas corticospinal tract neurons in the caudal region made monosynaptic connections with motoneurons. It has been argued that the direct connection to motoneurons might enable a more flexible and complex pattern of muscle activity than less indirect inputs. In humans, the contribution of the M1 and the corticospinal system to the control of hand movements has been demonstrated in patients with damage to these CNS structures which results in a reduced ability to perform individuated finger movements (Lang and Schieber, 2003, 2004). Transcranial magnetic stimulation The author is with the Dept. of Physical Medicine and Rehabilitation, University of Pittsburgh, Pittsburgh, PA. Address author correspondence to Monica A. Perez at [email protected]. 135
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(TMS) has been employed for noninvasive and painless stimulation of the hand representation of the M1 of intact and injured subjects through the scalp. TMS has been used most extensively in the corticospinal system since the output of the motor cortex can be easily assessed in the form of a motor evoked potential (MEP) by using surface electromyographic (EMG) recording electrodes. Experimental studies using TMS have suggested that both the M1 contralateral and ipsilateral to a moving hand contribute to the generation of EMG responses in hand muscles in a task-specific manner. For example, during unilateral voluntary contraction of intrinsic finger muscles an increase in the amplitude of MEPs in finger muscles and a decrease in the magnitude of short (SICI) and long (LICI) interval intracortical inhibition compared with rest can be found (Wassermann et al., 1996; Ortu et al., 2008; Kouchtir-Devanne et al., 2012). The changes in SICI and LICI suggest that GABAergic activity is significantly weaker during voluntary activity compared with rest, which may contribute to modulation of excitability of corticospinal neurons involved in the intended movement. Interestingly, patients with chronic incomplete cervical spinal cord injury (SCI) showed a descrease in SICI (probably involving GABAA receptors) but not LICI (probably involving GABAB receptors) during small levels of isometric voluntary contraction with intrinsic finger muscles (Barry et al., 2013; Figure 1). The results from this study demonstrated that longterm use of baclofen selectively maintained activity of largely subcortical but not cortical GABAergic neuronal pathways during voluntary activity involving finger muscles after human SCI. Therefore, cortical GABAA circuits may be less sensitive to baclofen than spinal GABAB circuits, which might to some extent contribute to the limited effects of baclofen on voluntary motor output, including hand function, in subjects with motor disorders affected by spasticity. More recent studies proposed that subcortical neuronal networks also make a significant contribution to the control of precision hand movements. Single unit recordings in primates demonstrated that spinal interneurons exert postspike effects in hand muscles during a precision grip in a task-dependent manner (Takei & Seki, 2010, 2013). Lesions of the corticospinal tract at the cervical spinal cord level showed in most cases complete recovery of the ability to grasp with the index finger and thumb (Sasaki et al., 2004; Alstermark et al., 2011) which most likely reflects central compensatory mechanisms underlying the recovery of finger dexterity (for review see Isa et al., 2013). In agreement, a recent study demonstrated that the control of precision grip in humans involves premotoneuronal subcortical mechanisms, which are deficient in patients with SCI and restored by long-term use of baclofen (Bunday et al., 2014). Thus, spinal GABAergic interneuronal circuits might be part of the subcortical premotoneuronal network shaping corticospinal output during human skilled hand actions. Spinal neuronal circuits, which can rapidly translate and shape inputs and outputs according to behavioral contexts (Cheney and Fetz, 1980; Prut and Perlmutter, 2003), might represent a critical source for the control of skilled hand movements. Evidence has shown that the M1 ipsilateral to a moving hand also contributes to the control of hand movements. During unilateral isometric voluntary contraction of intrinsic finger muscles, the excitability in the M1 that controls the resting hand changes in a task-dependent manner (Stedman, Davey, & Ellaway, 1998; Muellbacher et al., 2000; Perez & Cohen, 2008, 2009). A possible functional role of these interactions is to suppress unwanted EMG activity in the resting limb through interhemispheric MC Vol. 19, No. 2, 2015
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Figure 1 — The effect of voluntary contraction of intracortical inhibition in healthy controls and patients with SCI. Short-interval intracortical inhibition (SICI, A) and long-interval intracortical inhibition (LICI, B) were recorded at rest and during 25% of maximal voluntary contraction (MVC) of the first dorsal interosseous muscle. Traces show MEPs elicited at rest (top) and during 25% of MVC (bottom). Black and gray traces represent test MEP and conditioned MEP, respectively. Conditioning stimulation (black arrows) preceded test stimulation (gray arrows) by 2 ms for SICI and 100 ms for LICI. Note that SICI was decreased during voluntary contraction compared with at rest in both healthy controls and in SCI patients. However, LICI was decreased during voluntary contraction compared with at rest in healthy controls but not in SCI patients. (Modified with permission from Barry et al., 2013).
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Figure 2 — Ipsilateral silent period (iSP) during movement execution. A, B. Raw traces showing rectified EMG in representative subjects during iSP testing in self-paced and ballistic index finger (left traces) and elbow flexion (right traces) movements. Traces show the average 40 trials tested with (gray traces) and without (black traces) TMS. Traces below iSPs show the rectified EMG and angular displacement during each movement condition. Vertical solid lines show the time of TMS during testing and vertical dashed lines show onset and offset of the iSP. C, D. Group data (index finger task, n = 14, C; elbow task, n = 11, D). The abscissa shows all conditions tested (self-paced and ballistic). The ordinate shows the normalized iSP area. Note the increased in the iSP during ballistic index finger and elbow movements compared with self-paced movements. Error bars indicate SEs. *p < .05. (Modified with permission from Tazoe and Perez, 2013). 138
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inhibitory pathways (Cincotta & Ziemann, 2008; Hübers et al., 2008; Beaulé et al., 2012). More recent results showed that during unilateral isotonic hand movements the resting M1 contributes to modulate activity in the contralateral voluntarily active hand also in a task-specific manner (Tazoe and Perez, 2013; Figure 2). It has been shown that the contribution of transcallosal inhibition to ipsilateral movements at different speeds is widespread and has a functional role during rapid movements. Thus, at faster speeds transcallosal inhibition toward the moving hand decreases in the preparatory phase, which might contribute to starting movements rapidly. However, transcallosal inhibition toward the moving hand increases in the execution phase, which may contribute to stopping the movement. It is argued that transcallosal pathways enable signaling of the time of discrete behavioral events during ipsilateral movements, which is amplified by the speed of the movement. Importantly, the contribution of the ipsilateral M1 to modulate corticospinal excitability in the resting hand is impaired in humans with chronic incomplete SCI (Bunday & Perez, 2012; Bunday et al., 2013). In patients, strong voluntary contraction of a hand muscle was able to increase the corticospinal output in the contralateral resting hand, as in healthy controls, when the motoneurons for the hand muscle tested were located above the injury. However this modulation was absent in muscles at or within 5 segments below the injury and present in muscles beyond 5 segments below the injury. Importantly, crossed corticospinal facilitation was aberrantly high in muscles distant (>15 segments) from the injury and accompanied by increased motoneuronal excitability. In summary, the neuronal pathways contributing to the generation and control of hand movements are complex and involve cortical and subcortical structures from the contralateral and ipsilateral sides. Studies points to the view that transmission in pathways contributing to modulation of EMG activity in hand muscles changes in a task-dependent manner, which emphasizes the need for a careful interpretation when extrapolating results between different hand motor actions. Thus, a better understanding of the modulation of pathways contributing to the control of motor skills involving hand muscles may highlight new targets for recovery of the hand function after CNS injury.
References Alstermark, B., Pettersson, L.G., Nishimura, Y., Yoshino-Saito, K., Tsuboi, F., Takahashi, M., & Isa, T. (2011). Motor command for precision grip in the macaque monkey can be mediated by spinal interneurons. Journal of Neurophysiology, 106, 122–126. PubMed doi:10.1152/jn.00089.2011 Barry, M.D., Bunday, K.L., Chen, R., & Perez, M.A. (2013). Selective Effects of Baclofen on Use-Dependent Modulation of GABAB Inhibition after Tetraplegia. The Journal of Neuroscience, 33, 12898–12907. PubMed doi:10.1523/JNEUROSCI.1552-13.2013 Beaulé, V., Tremblay, S., & Théoret, H. (2012). Interhemispheric control of unilateral movement. Neural Plasticity, 2012, 627816. PubMed Bennett, K.M., & Lemon, R.N. (1996). Corticomotoneuronal contribution to the fractionation of muscle activity during precision grip in the monkey. Journal of Neurophysiology, 75, 1826–1842. PubMed Bunday, K.L., & Perez, M.A. (2012). Impaired crossed facilitation of the corticospinal pathway after cervical spinal cord injury. Journal of Neurophysiology, 107, 2901–2911. PubMed doi:10.1152/jn.00850.2011 MC Vol. 19, No. 2, 2015
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