Distinct Thalamo-Cortical Controls for Shoulder, Elbow, and Wrist during Locomotion

Recent data from this laboratory on differential controls for the shoulder, elbow, and wrist exerted by the thalamo-cortical network during locomotion is presented, based on experiments involving chronically instrumented cats walking on a flat surface and along a horizontal ladder. The activity of the following three groups of neurons is characterized: (1) neurons of the motor cortex that project to the pyramidal tract (PTNs), (2) neurons of the ventrolateral thalamus (VL), many identified as projecting to the motor cortex (thalamo-cortical neurons, TCs), and (3) neurons of the reticular nucleus of thalamus (RE), which inhibit TCs. Neurons were grouped according to their receptive field into shoulder-, elbow-, and wrist/paw-related categories. During simple locomotion, shoulder-related PTNs were most active in the late stance and early swing, and on the ladder, often increased activity and stride-related modulation while reducing discharge duration. Elbow-related PTNs were most active during late swing/early stance and typically remained similar on the ladder. Wrist-related PTNs were most active during swing, and on the ladder often decreased activity and increased modulation while reducing discharge duration. In the VL, shoulder-related neurons were more active during the transition from swing-to-stance. Elbow-related cells tended to be more active during the transition from stance-to-swing and on the ladder often decreased their activity and increased modulation. Wrist-related neurons were more active throughout the stance phase. In the RE, shoulder-related cells had low discharge rates and depths of modulation and long periods of activity distributed evenly across the cycle. In sharp contrast, wrist/paw-related cells discharged synchronously during the end of stance and swing with short periods of high activity, high modulation, and frequent sleep-type bursting. We conclude that thalamo-cortical network processes information related to different segments of the forelimb differently and exerts distinct controls over the shoulder, elbow, and wrist during locomotion.

[1]  M. Fabre-Thorpe,et al.  Visuomotor relearning after brain damage crucially depends on the integrity of the ventrolateral thalamic nucleus. , 1991, Behavioral neuroscience.

[2]  M. Horne,et al.  The role of the cerebello-thalamo-cortical pathway in skilled movement , 1995, Progress in Neurobiology.

[3]  T. Drew,et al.  Motor cortical activity during voluntary gait modifications in the cat. II. Cells related to the hindlimbs. , 1993, Journal of neurophysiology.

[4]  G. Orlovsky Activity of rubrospinal neurons during locomotion. , 1972, Brain research.

[5]  T. Drew Visuomotor coordination in locomotion , 1991, Current Opinion in Neurobiology.

[6]  Kiyoshi Kurata,et al.  Activity properties and location of neurons in the motor thalamus that project to the cortical motor areas in monkeys. , 2005, Journal of neurophysiology.

[7]  T. Drew,et al.  Differential activity-dependent development of corticospinal control of movement and final limb position during visually guided locomotion. , 2007, Journal of neurophysiology.

[8]  Mitchell Glickstein How are visual areas of the brain connected to motor areas for the sensory guidance of movement? , 2000, Trends in Neurosciences.

[9]  R. Dykes,et al.  Functional role of GABA in cat primary somatosensory cortex: shaping receptive fields of cortical neurons. , 1984, Journal of neurophysiology.

[10]  S. Grillner,et al.  On the central generation of locomotion in the low spinal cat , 1979, Experimental Brain Research.

[11]  S. Sherman,et al.  Functional Organization of the Thalamic Input to the Thalamic Reticular Nucleus , 2011, The Journal of Neuroscience.

[12]  M. Sirota,et al.  The role of the motor cortex in the control of accuracy of locomotor movements in the cat. , 1993, The Journal of physiology.

[13]  M. Sirota,et al.  Cortically Controlled Gait Adjustments in the Cat , 1998, Annals of the New York Academy of Sciences.

[14]  P. Strick,et al.  Activity of ventrolateral thalamic neurons during arm movement. , 1976, Journal of neurophysiology.

[15]  H. Asanuma,et al.  Relationship between afferent input and motor outflow in cat motorsensory cortex. , 1968, Journal of neurophysiology.

[16]  Natalia Dounskaia,et al.  Control of Human Limb Movements: The Leading Joint Hypothesis and Its Practical Applications , 2010, Exercise and sport sciences reviews.

[17]  P. Cheney,et al.  Corticomotoneuronal postspike effects in shoulder, elbow, wrist, digit, and intrinsic hand muscles during a reach and prehension task. , 1998, Journal of neurophysiology.

[18]  T. Drew,et al.  Role of the motor cortex in the control of visually triggered gait modifications. , 1996, Canadian journal of physiology and pharmacology.

[19]  A. Patla,et al.  Visual information from the lower visual field is important for walking across multi-surface terrain , 2008, Experimental Brain Research.

[20]  Doris Y. Tsao,et al.  Mechanisms of face perception. , 2008, Annual review of neuroscience.

[21]  A. Sillito The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat. , 1975, The Journal of physiology.

[22]  T. Drew,et al.  Electromyographic responses evoked in muscles of the forelimb by intracortical stimulation in the cat. , 1985, The Journal of physiology.

[23]  K. Kultas‐Ilinsky,et al.  An autoradiographic study of topographical relationships between pallidal and cerebellar projections to the cat thalamus , 2004, Experimental Brain Research.

[24]  C. G. Phillips,et al.  PYRAMIDAL SECTION IN THE CAT , 1944 .

[25]  G. Koshland,et al.  General coordination of shoulder, elbow and wrist dynamics during multijoint arm movements , 2001, Experimental Brain Research.

[26]  Daniel S. Marigold,et al.  Keep looking ahead? Re-direction of visual fixation does not always occur during an unpredictable obstacle avoidance task , 2006, Experimental Brain Research.

[27]  H. Sakata,et al.  Topographic relationship between the receptive fields of neurons in the motor cortex and the movements elicited by focal stimulation in freely moving cats. , 1968, The Japanese journal of physiology.

[28]  D. G. Lawrence . The effects of bilateral pyramidal lesions . II . The effects of lesions of the descending brainstem pathways , 2022 .

[29]  M. Sirota,et al.  Integration of motor and visual information in the parietal area 5 during locomotion. , 2003, Journal of neurophysiology.

[30]  S. Grillner,et al.  The locomotion of the low spinal cat. I. Coordination within a hindlimb. , 1980, Acta physiologica Scandinavica.

[31]  A. Sillito,et al.  The role of the thalamic reticular nucleus in visual processing , 2008 .

[32]  M. Sirota,et al.  Activity of Different Classes of Neurons of the Motor Cortex during Locomotion , 2003, The Journal of Neuroscience.

[33]  T. Drew,et al.  Locomotor‐related neuronal discharges in cat motor cortex compared with peripheral receptive fields and evoked movements. , 1984, The Journal of physiology.

[34]  J. Thomson,et al.  The role of visual information in control of a constrained locomotor task. , 1988, Journal of motor behavior.

[35]  S Murray Sherman,et al.  Different topography of the reticulothalmic inputs to first- and higher-order somatosensory thalamic relays revealed using photostimulation. , 2007, Journal of neurophysiology.

[36]  J. Stein,et al.  Role of the cerebellum in the visual guidance of movement. , 1992, Nature.

[37]  M. Sirota,et al.  Three Channels of Corticothalamic Communication during Locomotion , 2005, The Journal of Neuroscience.

[38]  D. Simons,et al.  State-Dependent Processing of Sensory Stimuli by Thalamic Reticular Neurons , 2003, The Journal of Neuroscience.

[39]  Pavel V Zelenin,et al.  Signals from the ventrolateral thalamus to the motor cortex during locomotion. , 2012, Journal of neurophysiology.

[40]  D. McCrea,et al.  Organization of mammalian locomotor rhythm and pattern generation , 2008, Brain Research Reviews.

[41]  A R Gibson,et al.  Visual cells in the pons of the brain. , 1976, Scientific American.

[42]  A. Karayannidou,et al.  Influences of sensory input from the limbs on feline corticospinal neurons during postural responses , 2008, The Journal of physiology.

[43]  I. Beloozerova,et al.  Pyramidal tract neurons receptive to different forelimb joints act differently during locomotion. , 2012, Journal of neurophysiology.

[44]  M. Sirota,et al.  Differential Gating of Thalamocortical Signals by Reticular Nucleus of Thalamus during Locomotion , 2012, The Journal of Neuroscience.

[45]  B. Heller Circular Statistics in Biology, Edward Batschelet. Academic Press, London & New York (1981), 371, Price $69.50 , 1983 .

[46]  Y Shinoda,et al.  Thalamocortical organization in the cerebello-thalamo-cortical system. , 1993, Cerebral cortex.

[47]  E. Batschelet Circular statistics in biology , 1981 .

[48]  S. Rossignol,et al.  On the initiation of the swing phase of locomotion in chronic spinal cats , 1978, Brain Research.

[49]  H. Sakata,et al.  Functional Organization of a Cortical Efferent System Examined with Focal Depth Stimulation in Cats , 1967 .

[50]  A Prochazka,et al.  Flexible fusimotor control of muscle spindle feedback during a variety of natural movements. , 1989, Progress in brain research.

[51]  Activity of cerebellar nuclei neurons during locomotion , 1972 .

[52]  K. Nakano,et al.  Distribution of cerebellothalamic neurons projecting to the ventral nuclei of the thalamus: An HRP study in the cat , 1980, The Journal of comparative neurology.

[53]  J. Schlag,et al.  Determination of antidromic excitation by the collision test: Problems of interpretation , 1976, Brain Research.

[54]  R. Dykes,et al.  Receptive field size for certain neurons in primary somatosensory cortex is determined by GABA-mediated intracortical inhibition , 1983, Brain Research.

[55]  M. Steriade Two channels in the cerebellothalamocortical system , 1995, The Journal of comparative neurology.

[56]  S. Grillner,et al.  Neuronal Control of Locomotion 'From Mollusc to Man ' , 1999 .

[57]  M. L. Shik,et al.  Neurophysiology of locomotor automatism. , 1976, Physiological reviews.

[58]  Raymond F Reynolds,et al.  Visual guidance of the human foot during a step , 2005, The Journal of physiology.

[59]  D. McCormick,et al.  Sleep and arousal: thalamocortical mechanisms. , 1997, Annual review of neuroscience.

[60]  Natalia Dounskaia,et al.  The internal model and the leading joint hypothesis: implications for control of multi-joint movements , 2005, Experimental Brain Research.

[61]  W. Chambers,et al.  Cortico‐spinal tract of the cat. An attempt to correlate the pattern of degeneration with deficits in reflex activity following neocortical lesions , 1957, The Journal of comparative neurology.

[62]  Nicholas I. Fisher,et al.  Statistical Analysis of Circular Data , 1993 .

[63]  D. McCormick,et al.  On the cellular and network bases of epileptic seizures. , 2001, Annual review of physiology.

[64]  A. Keller,et al.  Somatosensory response properties of excitatory and inhibitory neurons in rat motor cortex. , 2011, Journal of neurophysiology.

[65]  Y. Arshavsky,et al.  Cerebellum and Rhythmical Movements , 1986 .

[66]  Ray S. Snider,et al.  A stereotaxic atlas of the cat brain , 1987 .

[67]  D. Armstrong,et al.  Discharges of interpositus and Purkinje cells of the cat cerebellum during locomotion under different conditions. , 1988, The Journal of physiology.

[68]  U. Eysel,et al.  Inverse correlation of firing patterns of single topographically matched perigeniculate neurons and cat dorsal lateral geniculate relay cells , 1998, Visual Neuroscience.

[69]  J. Edeline,et al.  Tonotopic control of auditory thalamus frequency tuning by reticular thalamic neurons. , 2008, Journal of neurophysiology.

[70]  S. Rossignol,et al.  The locomotion of the low spinal cat. II. Interlimb coordination. , 1980, Acta physiologica Scandinavica.

[71]  M. Hollands,et al.  Visually guided stepping under conditions of step cycle-related denial of visual information , 1996, Experimental Brain Research.

[72]  D. G. Lawrence,et al.  The functional organization of the motor system in the monkey. II. The effects of lesions of the descending brain-stem pathways. , 1968, Brain : a journal of neurology.

[73]  S. Scott,et al.  Reaching movements with similar hand paths but different arm orientations. I. Activity of individual cells in motor cortex. , 1997, Journal of neurophysiology.

[74]  Grigori N. Orlovsky,et al.  Activity of Different Classes of Neurons of the Motor Cortex during Postural Corrections , 2003, The Journal of Neuroscience.

[75]  N. Fisher,et al.  Statistical Analysis of Circular Data , 1993 .

[76]  D. G. Lawrence,et al.  The functional organization of the motor system in the monkey. I. The effects of bilateral pyramidal lesions. , 1968, Brain : a journal of neurology.

[77]  D. Armstrong,et al.  Discharges of nucleus interpositus neurones during locomotion in the cat. , 1984, The Journal of physiology.

[78]  J. Massion The thalamus in the motor system. , 1976, Applied neurophysiology.

[79]  G. Orlovsky,et al.  Activity of pyramidal tract neurons in the cat during postural corrections. , 2005, Journal of neurophysiology.

[80]  G. Orlovsky,et al.  Activity of vestibulospinal neurons during locomotion. , 1972, Brain research.

[81]  J. Konczak,et al.  The development toward stereotypic arm kinematics during reaching in the first 3 years of life , 1997, Experimental Brain Research.

[82]  S Murray Sherman,et al.  Mapping by laser photostimulation of connections between the thalamic reticular and ventral posterior lateral nuclei in the rat. , 2005, Journal of neurophysiology.

[83]  C. A. Marsan Topographischer Hirnatlas der Katze für experimental-physiologische Untersuchungen , 1963 .

[84]  Irina N. Beloozerova,et al.  Role of Motor Cortex in Control of Locomotion , 1988 .

[85]  J. Martin,et al.  Postnatal development of the motor representation in primary motor cortex. , 2000, Journal of neurophysiology.

[86]  T. Drew,et al.  Discharges of pyramidal tract and other motor cortical neurones during locomotion in the cat. , 1984, The Journal of physiology.

[87]  D. Hoffman,et al.  Sensorimotor transformations in cortical motor areas , 2003, Neuroscience Research.

[88]  M. Hulliger,et al.  Dynamic and Static Fusimotor Set in Various Behavioural Contexts , 1988 .

[89]  W. Burke,et al.  The identification of single units in central visual pathways , 1962, The Journal of physiology.

[90]  A. Craig,et al.  Retrograde analysis of the cerebellar projections to the posteroventral part of the ventral lateral thalamic nucleus in the macaque monkey , 2008, The Journal of comparative neurology.

[91]  J. Massion,et al.  Stance and Motion , 1988, Springer US.

[92]  T. Sawaguchi,et al.  GABAergic inhibition of neuronal activity in the primate motor and premotor cortex during voluntary movement. , 1992, Journal of neurophysiology.

[93]  [Visually guided movement in the cat: difference in the effects of a bilateral lesion of the thalamic nucleus ventralis lateralis performed either before or after training]. , 1979, Comptes rendus des seances de l'Academie des sciences. Serie D, Sciences naturelles.

[94]  H. Asanuma,et al.  Peripheral afferent inputs to the forelimb area of the monkey motor cortex: Input-output relations , 2004, Experimental Brain Research.

[95]  T. Sejnowski,et al.  Thalamocortical Assemblies: How Ion Channels, Single Neurons and Large-Scale Networks Organize Sleep Oscillations , 2001 .

[96]  G. Orlovsky,et al.  Role of GABAA inhibition in modulation of pyramidal tract neuron activity during postural corrections , 2007, The European journal of neuroscience.

[97]  Orlovskiĭ Gn [Cerebellar influence on the reticulo-spinal neurons during locomotion]. , 1970 .

[98]  Harvey A Swadlow,et al.  Thalamocortical control of feed-forward inhibition in awake somatosensory 'barrel' cortex. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[99]  I. Grofová,et al.  Cerebellar projections to the nuclei ventralis lateralis and ventralis anterior thalami , 2004, Brain Structure and Function.

[100]  A. Grangetto,et al.  The cerebello-thalamo-cortical pathway. Topographical investigation at the unitary level in the cat , 1977, Experimental Brain Research.

[101]  T. P. S. Powell The Thalamus and Basal Telencephalon of the Cat. A Cytoarchitectonic Atlas with Stereotaxic Coordinates , 1986 .

[102]  R. Lemon,et al.  Selective facilitation of different hand muscles by single corticospinal neurones in the conscious monkey. , 1986, The Journal of physiology.

[103]  T. Drew,et al.  Forelimb electromyographic responses to motor cortex stimulation during locomotion in the cat. , 1985, The Journal of physiology.

[104]  M. Sirota,et al.  The role of the motor cortex in the control of vigour of locomotor movements in the cat. , 1993, The Journal of physiology.

[105]  E. G. Jones,et al.  Thalamic oscillations and signaling , 1990 .

[106]  H Sherk,et al.  Neural analysis of visual information during locomotion. , 2001, Progress in brain research.

[107]  J. Murphy,et al.  Afferent-efferent linkages in motor cortex for single forelimb muscles. , 1975, Journal of neurophysiology.

[108]  I. Whishaw,et al.  Cortical and subcortical lesions impair skilled walking in the ladder rung walking test: a new task to evaluate fore- and hindlimb stepping, placing, and co-ordination , 2002, Journal of Neuroscience Methods.

[109]  T. Drew,et al.  Contribution of the motor cortex to the structure and the timing of hindlimb locomotion in the cat: a microstimulation study. , 2005, Journal of neurophysiology.

[110]  Trevor Drew,et al.  Application of circular statistics to the study of neuronal discharge during locomotion , 1991, Journal of Neuroscience Methods.

[111]  G Mann,et al.  ON THE THALAMUS * , 1905, British medical journal.

[112]  M. Sirota,et al.  Differences in movement mechanics, electromyographic, and motor cortex activity between accurate and nonaccurate stepping. , 2010, Journal of neurophysiology.

[113]  T. Drew Motor cortical activity during voluntary gait modifications in the cat. I. Cells related to the forelimbs. , 1993, Journal of neurophysiology.

[114]  M. Sirota,et al.  Quantification of motor cortex activity and full-body biomechanics during unconstrained locomotion. , 2005, Journal of neurophysiology.