Signals from posterior parietal area 5 to motor cortex during locomotion.

Area 5 of the parietal cortex is part of the "dorsal stream" cortical pathway which processes visual information for action. The signals that area 5 ultimately conveys to motor cortex, the main area providing output to the spinal cord, are unknown. We analyzed area 5 neuronal activity during vision-independent locomotion on a flat surface and vision-dependent locomotion on a horizontal ladder in cats focusing on corticocortical neurons (CCs) projecting to motor cortex from the upper and deeper cortical layers and compared it to that of neighboring unidentified neurons (noIDs). We found that upon transition from vision-independent to vision-dependent locomotion, the low discharge of CCs in layer V doubled and the proportion of cells with 2 bursts per stride tended to increase. In layer V, the group of 2-bursters developed 2 activity peaks that coincided with peaks of gaze shifts along the surface away from the animal, described previously. One-bursters and either subpopulation in supragranular layers did not transmit any clear unified stride-related signal to the motor cortex. Most CC group activities did not mirror those of their noID counterparts. CCs with receptive fields on the shoulder, elbow, or wrist/paw discharged in opposite phases with the respective groups of pyramidal tract neurons of motor cortex, the cortico-spinal cells.

Activity of cat premotor cortex neurons during visually guided stepping.

Visual control of steps is critical in everyday life. Several motor centers are implicated in visual control of steps on a complex surface, however, participation of a large cortical motor area, the premotor cortex, in visual guidance of steps during overground locomotion has not been examined. Here, we analyzed the activity of neurons in feline premotor cortex areas 6aα and 6aγ as cats walked on the flat surface where visual guidance of steps is not needed and stepped on crosspieces of a horizontally placed ladder or over barriers where visual control of steps is required. The comparison of neuronal firing between vision-dependent and vision-independent stepping revealed components of the activity related to visual guidance of steps. We found that the firing activity of 59% of neurons was modulated with the rhythm of strides on the flat surface, and the activity of 83-86% of the population changed upon transition to locomotion on the ladder or with barriers. The firing rate and the depth of the stride-related activity modulation of 33-44% of neurons changed, and the stride phases where neurons preferred to fire changed for 58-73% of neurons. These results indicate that a substantial proportion of areas 6aα and 6aγ neurons is involved in visual guidance of steps. Compared with the primary motor cortex, the proportion of cells, the firing activity of which changed upon transition from vision-independent to vision-dependent stepping, was lower and the preferred phases of the firing activity changed more often between the tasks.NEW & NOTEWORTHY Visual control of steps is critical for daily living, however, how it is achieved is not well understood. Here, we analyzed how neurons in the premotor cortex respond to the demand for visual control of steps on a complex surface. We conclude that premotor cortex neurons participate in the cortical network supporting visual control of steps by modifying the phase, intensity, and salience of their firing activity.

When cats need to see to step accurately?

Locomotion on complex terrains often requires vision. However, how vision serves locomotion is not well understood. Here, we asked when visual information necessary for accurate stepping is collected and how its acquisition relates to the step cycle. In cats of both sexes, we showed that a brief (200-400 ms) interruption of visual input can rapidly influence cat's walking along a horizontal ladder. Depending on the phase within the step cycle, a 200 ms period of darkness could be tolerated fully without any changes to the strides or could lead to minor increases of stride duration. The effects of 300-400 ms of visual input denial, which typically prolonged stances and/or swings, also depended on the phase of the darkness onset. The increase of the duration of strides was always shorter than the duration of darkness. We conclude that visual information for planning a swing is collected starting from the middle of the preceding stance until the beginning of the current swing. For a stance (and/or a swing of the other paw), visual information is collected starting from the end of the previous stance and until the middle of the current stance. Acquisition of visual information during these windows is not uniform but depends on the phase of the step cycle. Notably, both the extension of these windows and their non-homogeneity are closely related to the pattern of gaze behaviour in cats, described previously. This new knowledge will help to guide research and understanding of neuronal mechanisms of visuomotor integration and modulation of visual function by strides during locomotion. KEY POINTS: Cats, like humans, rely on vision to navigate in complex environments. In cats walking along a horizontally placed ladder, we show that visual information required for accurate stepping is collected in a non-uniform manner throughout the stride cycle. Brief denial of visual input during a swing prolongs the next stance of that forelimb. Denial of visual input during a stance prolongs this stance, as well as the next swing and stance. Denial during the first half of a stance has a greater effect than during the second half. The phase dependence of the use of vision for accurate stepping and the pattern of affected swings and stances are closely related to the previously described pattern of gaze behaviour in cats. This new knowledge opens new perspectives for research into neuronal mechanisms of visuomotor coordination and visual function during walking and for understanding related disorders.

Neuronal activity reorganization in motor cortex for successful locomotion after a lesion in the ventrolateral thalamus.

Thalamic stroke leads to ataxia if the cerebellum-receiving ventrolateral thalamus (VL) is affected. The compensation mechanisms for this deficit are not well understood, particularly the roles that single neurons and specific neuronal subpopulations outside the thalamus play in recovery. The goal of this study was to clarify neuronal mechanisms of the motor cortex involved in mitigation of ataxia during locomotion when part of the VL is inactivated or lesioned. In freely ambulating cats, we recorded the activity of neurons in layer V of the motor cortex as the cats walked on a flat surface and horizontally placed ladder. We first reversibly inactivated ∼10% of the VL unilaterally using glutamatergic transmission antagonist CNQX and analyzed how the activity of motor cortex reorganized to support successful locomotion. We next lesioned 50%-75% of the VL bilaterally using kainic acid and analyzed how the activity of motor cortex reorganized when locomotion recovered. When a small part of the VL was inactivated, the discharge rates of motor cortex neurons decreased, but otherwise the activity was near normal, and the cats walked fairly well. Individual neurons retained their ability to respond to the demand for accuracy during ladder locomotion; however, most changed their response. When the VL was lesioned, the cat walked normally on the flat surface but was ataxic on the ladder for several days after lesion. When ladder locomotion normalized, neuronal discharge rates on the ladder were normal, and the shoulder-related group was preferentially active during the stride's swing phase.NEW & NOTEWORTHY This is the first analysis of reorganization of the activity of single neurons and subpopulations of neurons related to the shoulder, elbow, or wrist, as well as fast- and slow-conducting pyramidal tract neurons in the motor cortex of animals walking before and after inactivation or lesion in the thalamus. The results offer unique insights into the mechanisms of spontaneous recovery after thalamic stroke, potentially providing guidance for new strategies to alleviate locomotor deficits after stroke.

Contribution of the ventrolateral thalamus to the locomotion-related activity of motor cortex.

The activity of motor cortex is necessary for accurate stepping on a complex terrain. How this activity is generated remains unclear. The goal of this study was to clarify the contribution of signals from the ventrolateral thalamus (VL) to formation of locomotion-related activity of motor cortex during vision-independent and vision-dependent locomotion. In two cats, we recorded the activity of neurons in layer V of motor cortex as cats walked on a flat surface and a horizontal ladder. We reversibly inactivated ~10% of the VL unilaterally with the glutamatergic transmission antagonist 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) and analyzed how this affected the activity of motor cortex neurons. We examined neuronal subpopulations with somatosensory receptive fields on different segments of the forelimb and pyramidal tract projecting neurons (PTNs). We found that the VL contribution to the locomotion-related activity of motor cortex is very powerful and has both excitatory and inhibitory components. The magnitudes of both the excitatory and inhibitory contributions fluctuate over the step cycle and depend on locomotion task. On a flat surface, the VL contributes more excitation to the shoulder- and elbow-related neurons than the wrist/paw-related cells. The VL excites the shoulder-related group the most during the transition from stance to swing phase, while most intensively exciting the elbow-related group during the transition from swing to stance. The VL contributes more excitation for the fast- than slow-conducting PTNs. Upon transition to vision-dependent locomotion on the ladder, the VL contribution increases more for the wrist/paw-related neurons and slow-conducting PTNs.NEW & NOTEWORTHY How the activity of motor cortex is generated and the roles that different inputs to motor cortex play in formation of response properties of motor cortex neurons during movements remain unclear. This is the first study to characterize the contribution of the input from the ventrolateral thalamus (VL), the main subcortical input to motor cortex, to the activity of motor cortex neurons during vision-independent and vision-dependent locomotion.

Gaze coordination with strides during walking in the cat.

KEY POINTS: Vision plays a crucial role in guiding locomotion in complex environments, but the coordination between gaze and stride is not well understood. The coordination of gaze shifts, fixations, constant gaze and slow gaze with strides in cats walking on different surfaces were examined. It was found that gaze behaviours are coordinated with strides even when walking on a flat surface in the complete darkness, occurring in a sequential order during different phases of the stride. During walking on complex surfaces, gaze behaviours are typically more tightly coordinated with strides, particularly at faster speeds, only slightly shifting in phase. These findings indicate that the coordination of gaze behaviours with strides is not vision-driven, but is a part of the whole body locomotion synergy; the visual environment and locomotor task modulate it. The results may be relevant to developing diagnostic tools and rehabilitation approaches for patients with locomotor deficits. ABSTRACT: Vision plays a crucial role in guiding locomotion in complex environments. However, the coordination between the gaze and stride is not well understood. We investigated this coordination in cats walking on a flat surface in darkness or light, along a horizontal ladder and on a pathway with small stones. We recorded vertical and horizontal eye movements and 3-D head movement, and calculated where gaze intersected the walkway. The coordination of gaze shifts away from the animal, gaze shifts toward, fixations, constant gaze, and slow gaze with strides was investigated. We found that even during walking on the flat surface in the darkness, all gaze behaviours were coordinated with strides. Gaze shifts and slow gaze toward started in the beginning of each forelimb's swing and ended in its second half. Fixations peaked throughout the beginning and middle of swing. Gaze shifts away began throughout the second half of swing of each forelimb and ended when both forelimbs were in stance. Constant gaze and slow gaze away occurred in the beginning of stance. However, not every behaviour occurred during every stride. Light had a small effect. The ladder and stones typically increased the coordination and caused gaze behaviours to occur 3% earlier in the cycle. At faster speeds, the coordination was often tighter and some gaze behaviours occurred 2-16% later in the cycle. The findings indicate that the coordination of gaze with strides is not vision-driven, but is a part of the whole body locomotion synergy; the visual environment and locomotor task modulate it.

The role of intersegmental dynamics in coordination of the forelimb joints during unperturbed and perturbed skilled locomotion.

Joint coordination during locomotion and how this coordination changes in response to perturbations remains poorly understood. We investigated coordination among forelimb joints during the swing phase of skilled locomotion in the cat. While cats walked on a horizontal ladder, one of the cross-pieces moved before the cat reached it, requiring the cat to alter step size. Direction and timing of the cross-piece displacement were manipulated. We found that the paw was transported in space through body translation and shoulder and elbow rotations, whereas the wrist provided paw orientation required to step on cross-pieces. Kinetic analysis revealed a consistent joint control pattern in all conditions. Although passive interaction and gravitational torques were the main sources of shoulder and elbow motions for most of the movement time, shoulder muscle torque influenced movement of the entire limb at the end of the swing phase, accelerating the shoulder and causing interaction torque that determined elbow motion. At the wrist, muscle and passive torques predominantly compensated for each other. In all perturbed conditions, although all joints and the body slightly contributed to changes in the step length throughout the entire movement, the major adjustment was produced by the shoulder at the movement end. We conclude that joint coordination during the swing phase is produced mainly passively, by exploiting gravity and the limb's intersegmental dynamics, which may simplify the neural control of locomotion. The use of shoulder musculature at the movement end enables flexible responses to environmental disturbances. NEW & NOTEWORTHY This is the first study to investigate joint control during the swing phase of skilled, accuracy-dependent locomotion in the cat and how this control is altered to adapt to known and unexpected perturbations. We demonstrate that a pattern of joint control that exploits gravitational and interaction torques is used in all conditions and that movement modifications are produced mainly by shoulder muscle torque during the last portion of the movement.

Strategies for obstacle avoidance during walking in the cat.

Avoiding obstacles is essential for successful navigation through complex environments. This study aimed to clarify what strategies are used by a typical quadruped, the cat, to avoid obstacles during walking. Four cats walked along a corridor 2.5 m long and 25 or 15 cm wide. Obstacles, small round objects 2.5 cm in diameter and 1 cm in height, were placed on the floor in various locations. Movements of the paw were recorded with a motion capture and analysis system (Visualeyez, PTI). During walking in the wide corridor, cats' preferred strategy for avoiding a single obstacle was circumvention, during which the stride direction changed while stride duration and swing-to-stride duration ratio were preserved. Another strategy, stepping over the obstacle, was used during walking in the narrow corridor, when lateral deviations of walking trajectory were restricted. Stepping over the obstacle involved changes in two consecutive strides. The stride preceding the obstacle was shortened, and swing-to-stride ratio was reduced. The obstacle was negotiated in the next stride of increased height and normal duration and swing-to-stride ratio. During walking on a surface with multiple obstacles, both strategies were used. To avoid contact with the obstacle, cats placed the paw away from the object at a distance roughly equal to the diameter of the paw. During obstacle avoidance cats prefer to alter muscle activities without altering the locomotor rhythm. We hypothesize that a choice of the strategy for obstacle avoidance is determined by minimizing the complexity of neuro-motor processes required to achieve the behavioral goal.NEW & NOTEWORTHY In a study of feline locomotor behavior we found that the preferred strategy to avoid a small obstacle is circumvention. During circumvention, stride direction changes but length and temporal structure are preserved. Another strategy, stepping over the obstacle, is used in narrow walkways. During overstepping, two strides adjust. A stride preceding the obstacle decreases in length and duration. The following stride negotiating the obstacle increases in height while retaining normal temporal structure and nearly normal length.

Activity of somatosensory-responsive neurons in high subdivisions of SI cortex during locomotion.

Responses of neurons in the primary somatosensory cortex during movements are poorly understood, even during such simple tasks as walking on a flat surface. In this study, we analyzed spike discharges of neurons in the rostral bank of the ansate sulcus (areas 1-2) in 2 cats while the cats walked on a flat surface or on a horizontal ladder, a complex task requiring accurate stepping. All neurons (n = 82) that had receptive fields (RFs) on the contralateral forelimb exhibited frequency modulation of their activity that was phase locked to the stride cycle during simple locomotion. Neurons with proximal RFs (upper arm/shoulder) and pyramidal tract-projecting neurons (PTNs) with fast-conducting axons tended to fire at peak rates in the middle of the swing phase, whereas neurons with RFs on the distal limb (wrist/paw) and slow-conducting PTNs typically showed peak firing at the transition between swing and stance phases. Eleven of 12 neurons with tactile RFs on the volar forepaw began firing toward the end of swing, with peak activity occurring at the moment of foot contact with floor, thereby preceding the evoked sensory volley from touch receptors. Requirement to step accurately on the ladder affected 91% of the neurons, suggesting their involvement in control of accuracy of stepping. During both tasks, neurons exhibited a wide variety of spike distributions within the stride cycle, suggesting that, during either simple or ladder locomotion, they represent the cycling somatosensory events in their activity both predictively before and reflectively after these events take place.

Accurate stepping on a narrow path: mechanics, EMG, and motor cortex activity in the cat.

How do cats manage to walk so graciously on top of narrow fences or windowsills high above the ground while apparently exerting little effort? In this study we investigated cat full-body mechanics and the activity of limb muscles and motor cortex during walking along a narrow 5-cm path on the ground. We tested the hypotheses that during narrow walking 1) lateral stability would be lower because of the decreased base-of-support area and 2) the motor cortex activity would increase stride-related modulation because of imposed demands on lateral stability and paw placement accuracy. We measured medio-lateral and rostro-caudal dynamic stability derived from the extrapolated center of mass position with respect to the boundaries of the support area. We found that cats were statically stable in the frontal plane during both unconstrained and narrow-path walking. During narrow-path walking, cats walked slightly slower with more adducted limbs, produced smaller lateral forces by hindlimbs, and had elevated muscle activities. Of 174 neurons recorded in cortical layer V, 87% of forelimb-related neurons (from 114) and 90% of hindlimb-related neurons (from 60) had activities during narrow-path walking distinct from unconstrained walking: more often they had a higher mean discharge rate, lower depth of stride-related modulation, and/or longer period of activation during the stride. These activity changes appeared to contribute to control of accurate paw placement in the medio-lateral direction, the width of the stride, rather than to lateral stability control, as the stability demands on narrow-path and unconstrained walking were similar.

Known and unexpected constraints evoke different kinematic, muscle, and motor cortical neuron responses during locomotion.

During navigation through complex natural environments, people and animals must adapt their movements when the environment changes. The neural mechanisms of such adaptations are poorly understood, especially with respect to constraints that are unexpected and must be adapted to quickly. In this study, we recorded forelimb-related kinematics, muscle activity, and the activity of motor cortical neurons in cats walking along a raised horizontal ladder, a complex locomotion task requiring accurate limb placement. One of the crosspieces was motorized, and displaced before the cat stepped on the ladder or at different points along the cat's progression over the ladder, either towards or away from the cat. We found that, when the crosspiece was displaced before the cat stepped onto the ladder, the kinematic modifications were complex and involved all forelimb joints. When the crosspiece displaced unexpectedly while the cat was on the ladder, the kinematic modifications were minimalistic and primarily involved distal joints. The activity of M. triceps and M. extensor digitorum communis differed based on the direction of displacement. Out of 151 neurons tested, 69% responded to at least one condition; however, neurons were significantly more likely to respond when crosspiece displacement was unexpected. Most often they responded during the swing phase. These results suggest that different neural mechanisms and motor control strategies are used to overcome constraints for locomotor movements depending on whether they are known or emerge unexpectedly.

Burst firing of neurons in the thalamic reticular nucleus during locomotion.

This study examined the burst firing of neurons in the motor sector of the thalamic reticular nucleus (RE) of the cat. These neurons are inhibitory cells that project to the motor thalamus. The firing activity of RE neurons was studied during four behaviors: sleep, standing, walking on a flat surface, and accurate stepping on crosspieces of a horizontal ladder. Extracellularly recorded firing activity was analyzed in 58 neurons that were identified according to their receptive fields on the contralateral forelimb. All neurons generated bursts of spikes during sleep, half generated bursts of spikes during standing, and one-third generated bursts of spikes during walking. The majority of bursts were sequences of spikes with an exponential buildup of the firing rate followed by exponential decay with time constants in the range of 10-30 ms. We termed them "full-scale" bursts. All neurons also generated "atypical" bursts, in which the buildup of the firing rate deviated from the characteristic order. Burst firing was most likely to occur in neurons with receptive fields on the distal forelimb and least likely in neurons related to the proximal limb. Full-scale bursts were more frequent than atypical bursts during unconstrained walking on the flat surface. Bursts of both types occurred with similar probability during accurate stepping on the horizontal ladder, a task that requires forebrain control of locomotion. We suggest that transformations of the temporal pattern of bursts in the inhibitory RE neurons facilitate the tuning of thalamo-cortical signals to the complexity of ongoing locomotor tasks.

Stabilization of cat paw trajectory during locomotion.

We investigated which of cat limb kinematic variables during swing of regular walking and accurate stepping along a horizontal ladder are stabilized by coordinated changes of limb segment angles. Three hypotheses were tested: 1) animals stabilize the entire swing trajectory of specific kinematic variables (performance variables); and 2) the level of trajectory stabilization is similar between regular and ladder walking and 3) is higher for forelimbs compared with hindlimbs. We used the framework of the uncontrolled manifold (UCM) hypothesis to quantify the structure of variance of limb kinematics in the limb segment orientation space across steps. Two components of variance were quantified for each potential performance variable, one of which affected it ("bad variance," variance orthogonal to the UCM, VORT) while the other one did not ("good variance," variance within the UCM, VUCM). The analysis of five candidate performance variables revealed that cats during both locomotor behaviors stabilize 1) paw vertical position during the entire swing (VUCM > VORT, except in mid-hindpaw swing of ladder walking) and 2) horizontal paw position in initial and terminal swing (except for the entire forepaw swing of regular walking). We also found that the limb length was typically stabilized in midswing, whereas limb orientation was not (VUCM ≤ VORT) for both limbs and behaviors during entire swing. We conclude that stabilization of paw position in early and terminal swing enables accurate and stable locomotion, while stabilization of vertical paw position in midswing helps paw clearance. This study is the first to demonstrate the applicability of the UCM-based analysis to nonhuman movement.

Body stability and muscle and motor cortex activity during walking with wide stance.

Biomechanical and neural mechanisms of balance control during walking are still poorly understood. In this study, we examined the body dynamic stability, activity of limb muscles, and activity of motor cortex neurons [primarily pyramidal tract neurons (PTNs)] in the cat during unconstrained walking and walking with a wide base of support (wide-stance walking). By recording three-dimensional full-body kinematics we found for the first time that during unconstrained walking the cat is dynamically unstable in the forward direction during stride phases when only two diagonal limbs support the body. In contrast to standing, an increased lateral between-paw distance during walking dramatically decreased the cat's body dynamic stability in double-support phases and prompted the cat to spend more time in three-legged support phases. Muscles contributing to abduction-adduction actions had higher activity during stance, while flexor muscles had higher activity during swing of wide-stance walking. The overwhelming majority of neurons in layer V of the motor cortex, 82% and 83% in the forelimb and hindlimb representation areas, respectively, were active differently during wide-stance walking compared with unconstrained condition, most often by having a different depth of stride-related frequency modulation along with a different mean discharge rate and/or preferred activity phase. Upon transition from unconstrained to wide-stance walking, proximal limb-related neuronal groups subtly but statistically significantly shifted their activity toward the swing phase, the stride phase where most of body instability occurs during this task. The data suggest that the motor cortex participates in maintenance of body dynamic stability during locomotion.

Differential gating of thalamocortical signals by reticular nucleus of thalamus during locomotion.

The thalamic reticular nucleus (RE) provides inhibition to the dorsal thalamus, and forms a crucial interface between thalamocortical and corticothalamic signals. Whereas there has been significant interest in the role of the RE in organizing thalamocortical signaling, information on the activity of the RE in the awake animal is scant. Here we investigated the activity of neurons within the "motor" compartment of the RE in the awake, unrestrained cat during simple locomotion on a flat surface and complex locomotion along a horizontal ladder that required visual control of stepping. The activity of 88% of neurons in this region was modulated during locomotion. Neurons with receptive fields on the shoulder were located dorsally in the nucleus and had regular discharges; during locomotion they had relatively low activity and modest magnitudes of stride-related modulation, and their group activity was distributed over the stride. In contrast, neurons with receptive fields on the wrist/paw were located more ventrally, often discharged sleep-type bursts during locomotion, were very active and profoundly modulated, and their group activity was concentrated in the swing and end of stance. Seventy-five percent of RE neurons had different activity during the two locomotion tasks. We conclude that during locomotion the RE differentially gates thalamocortical signals transmitted during different phases of the stride, in relation to different parts of the limb, and the type of locomotion task.

Differential responses of fast- and slow-conducting pyramidal tract neurons to changes in accuracy demands during locomotion.

Most movements need to be accurate. The neuronal mechanisms controlling accuracy during movements are poorly understood. In this study we compare the activity of fast- and slow-conducting pyramidal tract neurons (PTNs) of the motor cortex in cats as they walk over both a flat surface, a task that does not require accurate stepping and can be accomplished without the motor cortex, as well as along a horizontal ladder, a task that requires accuracy and the activity of the motor cortex to be successful. Fast- and slow-conducting PTNs are known to have distinct biophysical properties as well as different afferent and efferent connections. We found that while the activity of all PTNs changes substantially upon transition from simple locomotion to accurate stepping on the ladder, slow-conducting PTNs respond in a much more concerted manner than fast-conducting ones. As a group, slow-conducting PTNs increase discharge rate, especially during the late stance and early swing phases, decrease discharge variability, have a tendency to shift their preferred phase of the discharge into the swing phase, and almost always produce a single peak of activity per stride during ladder locomotion. In contrast, the fast-conducting PTNs do not display such concerted changes to their activity. In addition, upon transfer from simple locomotion to accurate stepping on the ladder slow-conducting PTNs more profoundly increase the magnitude of their stride-related frequency modulation compared with fast-conducting PTNs. We suggest that slow-conducting PTNs are involved in control of accuracy of locomotor movements to a greater degree than fast-conducting PTNs.

Contribution of different limb controllers to modulation of motor cortex neurons during locomotion.

During locomotion, neurons in motor cortex exhibit profound step-related frequency modulation. The source of this modulation is unclear. The aim of this study was to reveal the contribution of different limb controllers (locomotor mechanisms of individual limbs) to the periodic modulation of motor cortex neurons during locomotion. Experiments were conducted in chronically instrumented cats. The activity of single neurons was recorded during regular quadrupedal locomotion (control), as well as when only one pair of limbs (fore, hind, right, or left) was walking while another pair was standing. Comparison of the modulation patterns in these neurons (their discharge profile with respect to the step cycle) during control and different bipedal locomotor tasks revealed several groups of neurons that receive distinct combinations of inputs from different limb controllers. In the majority (73%) of neurons from the forelimb area of motor cortex, modulation during control was determined exclusively by forelimb controllers (right, left, or both), while in the minority (27%), hindlimb controllers also contributed. By contrast, only in 30% of neurons from the hindlimb area was modulation determined exclusively by hindlimb controllers (right or both), while in 70% of them, the controllers of forelimbs also contributed. We suggest that such organization of inputs allows the motor cortex to contribute to the right-left limbs' coordination within each of the girdles during locomotion, and that it also allows hindlimb neurons to participate in coordination of the movements of the hindlimbs with those of the forelimbs.

Pyramidal tract neurons receptive to different forelimb joints act differently during locomotion.

During locomotion, motor cortical neurons projecting to the pyramidal tract (PTNs) discharge in close relation to strides. How their discharges vary based on the part of the body they influence is not well understood. We addressed this question with regard to joints of the forelimb in the cat. During simple and ladder locomotion, we compared the activity of four groups of PTNs with somatosensory receptive fields involving different forelimb joints: 1) 45 PTNs receptive to movements of shoulder, 2) 30 PTNs receptive to movements of elbow, 3) 40 PTNs receptive to movements of wrist, and 4) 30 nonresponsive PTNs. In the motor cortex, a relationship exists between the location of the source of afferent input and the target for motor output. On the basis of this relationship, we inferred the forelimb joint that a PTN influences from its somatosensory receptive field. We found that different PTNs tended to discharge differently during locomotion. During simple locomotion shoulder-related PTNs were most active during late stance/early swing, and upon transition from simple to ladder locomotion they often increased activity and stride-related modulation while reducing discharge duration. Elbow-related PTNs were most active during late swing/early stance and typically did not change activity, modulation, or discharge duration on the ladder. Wrist-related PTNs were most active during swing and upon transition to the ladder often decreased activity and increased modulation while reducing discharge duration. These data suggest that during locomotion the motor cortex uses distinct mechanisms to control the shoulder, elbow, and wrist.

Signals from the ventrolateral thalamus to the motor cortex during locomotion.

The activity of the motor cortex during locomotion is profoundly modulated in the rhythm of strides. The source of modulation is not known. In this study we examined the activity of one of the major sources of afferent input to the motor cortex, the ventrolateral thalamus (VL). Experiments were conducted in chronically implanted cats with an extracellular single-neuron recording technique. VL neurons projecting to the motor cortex were identified by antidromic responses. During locomotion, the activity of 92% of neurons was modulated in the rhythm of strides; 67% of cells discharged one activity burst per stride, a pattern typical for the motor cortex. The characteristics of these discharges in most VL neurons appeared to be well suited to contribute to the locomotion-related activity of the motor cortex. In addition to simple locomotion, we examined VL activity during walking on a horizontal ladder, a task that requires vision for correct foot placement. Upon transition from simple to ladder locomotion, the activity of most VL neurons exhibited the same changes that have been reported for the motor cortex, i.e., an increase in the strength of stride-related modulation and shortening of the discharge duration. Five modes of integration of simple and ladder locomotion-related information were recognized in the VL. We suggest that, in addition to contributing to the locomotion-related activity in the motor cortex during simple locomotion, the VL integrates and transmits signals needed for correct foot placement on a complex terrain to the motor cortex.

Activity of red nucleus neurons in the cat during postural corrections.

The dorsal-side-up body posture in standing quadrupeds is maintained by the postural system, which includes spinal and supraspinal mechanisms driven by somatosensory inputs from the limbs. A number of descending tracts can transmit supraspinal commands for postural corrections. The first aim of this study was to understand whether the rubrospinal tract participates in their transmission. We recorded activity of red nucleus neurons (RNNs) in the cat maintaining balance on the periodically tilting platform. Most neurons were identified as rubrospinal ones. It was found that many RNNs were profoundly modulated by tilts, suggesting that they transmit postural commands. The second aim of this study was to examine the contribution of sensory inputs from individual limbs to posture-related RNN modulation. Each RNN was recorded during standing on all four limbs, as well as when two or three limbs were lifted from the platform and could not signal platform displacements. By comparing RNN responses in different tests, we found that the amplitude and phase of responses in the majority of RNNs were determined primarily by sensory input from the corresponding (fore or hind) contralateral limb, whereas inputs from other limbs made a much smaller contribution to RNN modulation. These findings suggest that the rubrospinal system is primarily involved in the intralimb postural coordination, i.e., in the feedback control of the corresponding limb and, to a lesser extent, in the interlimb coordination. This study provides a new insight into the formation of supraspinal motor commands for postural corrections.