Spinal Commissural Connections to Motoneurons Controlling the Primate Hand and Wrist

Left–right coordination is essential for locomotor movements and is partly mediated by spinal commissural systems. Such coordination is also essential for reaching and manipulation in primates, but the role of spinal commissural systems here has not been studied. We investigated commissural connectivity to motoneurons innervating forelimb muscles using intracellular recordings in acutely anesthetized macaque monkeys. In 57 of 81 motoneurons, synaptic responses (52 of 57 excitatory) were evoked after contralateral intraspinal microstimulation in the gray matter (cISMS; 300 μA maximum current intensity). Some responses (15 of 57) occurred at latencies compatible with a monosynaptic linkage, including in motoneurons projecting to intrinsic hand muscles (9 cells). Three pieces of evidence suggest that these effects reflected the action of commissural interneurons. In two cells, preceding cISMS with stimulation of the contralateral medial brainstem descending pathways facilitated the motoneuron responses, suggesting that cISMS acted on cell bodies whose excitability was increased by descending inputs. Pairing cISMS with stimulation of the contralateral corticospinal tract yielded no evidence of response occlusion in 16 cells tested, suggesting that the effects were not merely axon reflexes generated by stimulation of corticospinal axon branches, which cross the midline. Finally, stimulation of contralateral peripheral nerves evoked responses in 28 of 52 motoneurons (7 of 9 projecting to the hand). Our results demonstrate the existence of commissural neurons with access to spinal motoneurons in primate cervical spinal cord that receive inputs from the periphery as well as descending pathways. Most importantly, commissural neurons also innervate motoneurons of intrinsic hand muscles.

[1]  B W Peterson,et al.  Reticulospinal projections to spinal motor nuclei. , 1979, Annual review of physiology.

[2]  Stuart N Baker,et al.  Cells in the monkey ponto-medullary reticular formation modulate their activity with slow finger movements , 2012, The Journal of physiology.

[3]  E. Jankowska,et al.  Ipsilateral Actions of Feline Corticospinal Tract Neurons on Limb Motoneurons , 2004, The Journal of Neuroscience.

[4]  Stuart N. Baker,et al.  Direct and Indirect Connections with Upper Limb Motoneurons from the Primate Reticulospinal Tract , 2009, The Journal of Neuroscience.

[5]  E. Vaadia,et al.  Single-unit activity related to bimanual arm movements in the primary and supplementary motor cortices. , 2002, Journal of neurophysiology.

[6]  M. Perreault,et al.  Organization of Functional Synaptic Connections between Medullary Reticulospinal Neurons and Lumbar Descending Commissural Interneurons in the Neonatal Mouse , 2011, The Journal of Neuroscience.

[7]  S. Baker,et al.  Different contributions of the corpus callosum and cerebellum to motor coordination in monkey. , 2007, Journal of neurophysiology.

[8]  M. Carpenter,et al.  Afferent and efferent connections of the medial, inferior and lateral vestibular nuclei in the cat and monkey , 1983, Brain Research.

[9]  K. Takakusaki,et al.  Multi‐segmental innervation of single pontine reticulospinal axons in the cervico‐thoracic region of the cat: Anterograde PHA‐L tracing study , 1997, The Journal of comparative neurology.

[10]  R. Ivry,et al.  Callosotomy patients exhibit temporal uncoupling during continuous bimanual movements , 2002, Nature Neuroscience.

[11]  Y. Shinoda,et al.  Spinal commissural neurons mediating vestibular input to neck motoneurons in the cat upper cervical spinal cord , 1992, Neuroscience Letters.

[12]  G. Spidalieri,et al.  Motor responses mediated by orthodromic and antidromic activation of the rostral portion of the cat corpus callosum , 2004, Experimental Brain Research.

[13]  K. Pearson,et al.  Corrective responses to loss of ground support during walking. II. Comparison of intact and chronic spinal cats. , 1994, Journal of neurophysiology.

[14]  S. Mori,et al.  Morphology of single pontine reticulospinal axons in the lumbar enlargement of the cat: A study using the anterograde tracer PHA‐L , 1999, The Journal of comparative neurology.

[15]  Elzbieta Jankowska,et al.  Networks of inhibitory and excitatory commissural interneurons mediating crossed reticulospinal actions , 2003, The European journal of neuroscience.

[16]  H. Kuypers,et al.  Cells of origin of propriospinal fibers and of fibers ascending to supraspinal levels. A HRP study in cat and rhesus monkey , 1978, Brain Research.

[17]  Trevor Drew,et al.  Independent and convergent signals from the pontomedullary reticular formation contribute to the control of posture and movement during reaching in the cat. , 2004, Journal of neurophysiology.

[18]  P. Goldman-Rakic,et al.  Synaptic development of the cerebral cortex: implications for learning, memory, and mental illness. , 1994, Progress in brain research.

[19]  P. Harrison,et al.  Crossed actions on group II‐activated interneurones in the midlumbar segments of the cat spinal cord. , 1992, The Journal of physiology.

[20]  Adam G. Davidson,et al.  Movement-related and preparatory activity in the reticulospinal system of the monkey , 2004, Experimental Brain Research.

[21]  O Kiehn,et al.  Characterization of commissural interneurons in the lumbar region of the neonatal rat spinal cord , 1999, The Journal of comparative neurology.

[22]  J. Yokota,et al.  Divergent projection of individual corticospinal axons to motoneurons of multiple muscles in the monkey , 1981, Neuroscience Letters.

[23]  H. Kuypers,et al.  Cerebral control of contralateral and ipsilateral arm, hand and finger movements in the split-brain rhesus monkey. , 1973, Brain : a journal of neurology.

[24]  Stuart N Baker,et al.  Lack of Evidence for Direct Corticospinal Contributions to Control of the Ipsilateral Forelimb in Monkey , 2011, The Journal of Neuroscience.

[25]  K. Stecina,et al.  Premotor interneurones contributing to actions of feline pyramidal tract neurones on ipsilateral hindlimb motoneurones , 2008, The Journal of physiology.

[26]  R. Porter,et al.  Corticomotoneuronal synapses in the monkey: Light microscopic localization upon motoneurons of intrinsic muscles of the hand , 1985, The Journal of comparative neurology.

[27]  B. Alstermark,et al.  Transneuronal labelling of neurones projecting to forelimb motoneurones in cats performing different movements , 1986, Brain Research.

[28]  E. Jankowska,et al.  Functional differentiation and organization of feline midlumbar commissural interneurones , 2005, The Journal of physiology.

[29]  J. Tanji,et al.  Neuronal activity in cortical motor areas related to ipsilateral, contralateral, and bilateral digit movements of the monkey. , 1988, Journal of neurophysiology.

[30]  M. Fitzgerald,et al.  Influences of contralateral nerve and skin stimulation on neurones in the substantia gelatinosa of the rat spinal cord , 1983, Neuroscience Letters.

[31]  T. Hongo,et al.  Convergent effects from bilateral vestibulospinal tracts on spinal interneurons. , 1971, Brain research.

[32]  Romeo Chua,et al.  Human interlimb reflexes evoked by electrical stimulation of cutaneous nerves innervating the hand and foot , 2001, Experimental Brain Research.

[33]  E. Jankowska,et al.  Both dorsal horn and lamina VIII interneurones contribute to crossed reflexes from feline group II muscle afferents , 2003, The Journal of physiology.

[34]  M. Gorassini,et al.  Corrective responses to loss of ground support during walking. I. Intact cats. , 1994, Journal of neurophysiology.

[35]  M S Gazzaniga,et al.  Anterior and posterior callosal contributions to simultaneous bimanual movements of the hands and fingers. , 2000, Brain : a journal of neurology.

[36]  S. Rossignol,et al.  Contralateral hindlimb responses to cutaneous stimulation during locomotion in high decerebrate cats , 1981, Brain Research.

[37]  M. Wiesendanger,et al.  Transcallosal connections of the distal forelimb representations of the primary and supplementary motor cortical areas in macaque monkeys , 2004, Experimental Brain Research.

[38]  O. Devinsky,et al.  Callosal lesions and behavior: history and modern concepts , 2003, Epilepsy & Behavior.

[39]  E. Jankowska,et al.  Relative contribution of Ia inhibitory interneurones to inhibition of feline contralateral motoneurones evoked via commissural interneurones , 2005, The Journal of physiology.

[40]  Y. Shinoda,et al.  The morphology of single lateral vestibulospinal tract axons in the lower cervical spinal cord of the cat , 1986, The Journal of comparative neurology.

[41]  J. Duysens,et al.  Modulation of ipsi- and contralateral reflex responses in unrestrained walking cats. , 1980, Journal of neurophysiology.

[42]  K. Fukushima,et al.  Vestibulospinal, reticulospinal and interstitiospinal pathways in the cat. , 1979, Progress in brain research.

[43]  E. Paul Zehr,et al.  Modulation of cutaneous reflexes in arm muscles during walking: further evidence of similar control mechanisms for rhythmic human arm and leg movements , 2003, Experimental Brain Research.

[44]  B. Hyland,et al.  Neural activity of supplementary and primary motor areas in monkeys and its relation to bimanual and unimanual movement sequences , 1999, Neuroscience.

[45]  V. J. Wilson,et al.  Response of commissural and other upper cervical ventral horn neurons to vestibular stimuli in vertical planes. , 1994, Journal of neurophysiology.

[46]  Elzbieta Jankowska,et al.  Neuronal Basis of Crossed Actions from the Reticular Formation on Feline Hindlimb Motoneurons , 2003, The Journal of Neuroscience.

[47]  S. Baker,et al.  Bilateral representation in the deep cerebellar nuclei , 2008, The Journal of physiology.

[48]  S. Baker,et al.  Cortico-cerebellar coherence during a precision grip task in the monkey. , 2006, Journal of neurophysiology.

[49]  M. Wiesendanger,et al.  Role of the corpus callosum in bimanual coordination: a comparison of patients with congenital and acquired callosal damage , 2001, The European journal of neuroscience.

[50]  E Jankowska,et al.  Excitatory and inhibitory intermediate zone interneurons in pathways from feline group I and II afferents: differences in axonal projections and input , 2009, The Journal of physiology.

[51]  R. McCarley,et al.  Descending projections from the gigantocellular tegmental field in the cat: Cells of origin and their brainstem and spinal cord trajectories , 1988, The Journal of comparative neurology.

[52]  B. W. Peterson,et al.  Patterns of projection and branching of reticulospinal neurons , 1975, Experimental Brain Research.

[53]  Adam R. Ferguson,et al.  Extensive Spontaneous Plasticity of Corticospinal Projections After Primate Spinal Cord Injury , 2010, Nature Neuroscience.

[54]  V Reggie Edgerton,et al.  Extensive spinal decussation and bilateral termination of cervical corticospinal projections in rhesus monkeys , 2009, The Journal of comparative neurology.

[55]  Stuart N. Baker,et al.  Changes in descending motor pathway connectivity after corticospinal tract lesion in macaque monkey , 2012, Brain : a journal of neurology.

[56]  W. D. Thompson,et al.  Excitation of pyramidal tract cells by intracortical microstimulation: effective extent of stimulating current. , 1968, Journal of neurophysiology.

[57]  Jean Bullier,et al.  Spread of stimulating current in the cortical grey matter of rat visual cortex studied on a new in vitro slice preparation , 1996, Journal of Neuroscience Methods.

[58]  I. Kermadi,et al.  Do bimanual motor actions involve the dorsal premotor (PMd), cingulate (CMA) and posterior parietal (PPC) cortices? Comparison with primary and supplementary motor cortical areas. , 2000, Somatosensory & motor research.

[59]  Elzbieta Jankowska,et al.  Differential Projections of Excitatory and Inhibitory Dorsal Horn Interneurons Relaying Information from Group II Muscle Afferents in the Cat Spinal Cord , 2006, The Journal of Neuroscience.

[60]  Trevor Drew,et al.  Descending signals from the pontomedullary reticular formation are bilateral, asymmetric, and gated during reaching movements in the cat. , 2006, Journal of neurophysiology.

[61]  T. Roberts NEUROPHYSIOLOGY OF POSTURAL MECHANISMS , 1968, The Ulster Medical Journal.

[62]  K. Stecina,et al.  Commissural interneurons with input from group I and II muscle afferents in feline lumbar segments: neurotransmitters, projections and target cells , 2009, Journal of Physiology.

[63]  Maurizio Gentilucci,et al.  Object motor representation and language , 2003, Experimental Brain Research.

[64]  K. Stecina,et al.  Neuronal relays in double crossed pathways between feline motor cortex and ipsilateral hindlimb motoneurones , 2006, The Journal of physiology.

[65]  E. Jankowska Spinal interneuronal networks in the cat: Elementary components , 2008, Brain Research Reviews.

[66]  Stuart N. Baker,et al.  Convergence of Pyramidal and Medial Brain Stem Descending Pathways Onto Macaque Cervical Spinal Interneurons , 2010, Journal of neurophysiology.

[67]  E. Fetz,et al.  Activity of forelimb motor units and corticomotoneuronal cells during ramp-and-hold torque responses: comparisons with oculomotor cells. , 1986, Progress in brain research.

[68]  M. Ito,et al.  Interaction between the horizontal vestibulo-ocular reflex and optokinetic response in rabbits , 1979, Experimental Brain Research.

[69]  K. Stecina,et al.  Differential modulation by monoamine membrane receptor agonists of reticulospinal input to lamina VIII feline spinal commissural interneurons , 2007, The European journal of neuroscience.

[70]  B. W. Peterson,et al.  Reticulospinal connections with limb and axial motoneurons , 1979, Experimental Brain Research.

[71]  T. Drew,et al.  Contributions of the reticulospinal system to the postural adjustments occurring during voluntary gait modifications. , 2001, Journal of neurophysiology.

[72]  E. Jankowska,et al.  The actions of monoamines and distribution of noradrenergic and serotoninergic contacts on different subpopulations of commissural interneurons in the cat spinal cord , 2004, The European journal of neuroscience.