Gaze shifts and fixations dominate gaze behavior of walking cats.

Vision is important for locomotion in complex environments. How it is used to guide stepping is not well understood. We used an eye search coil technique combined with an active marker-based head recording system to characterize the gaze patterns of cats walking over terrains of different complexity: (1) on a flat surface in the dark when no visual information was available, (2) on the flat surface in light when visual information was available but not required for successful walking, (3) along the highly structured but regular and familiar surface of a horizontal ladder, a task for which visual guidance of stepping was required, and (4) along a pathway cluttered with many small stones, an irregularly structured surface that was new each day. Three cats walked in a 2.5-m corridor, and 958 passages were analyzed. Gaze activity during the time when the gaze was directed at the walking surface was subdivided into four behaviors based on speed of gaze movement along the surface: gaze shift (fast movement), gaze fixation (no movement), constant gaze (movement at the body's speed), and slow gaze (the remainder). We found that gaze shifts and fixations dominated the cats' gaze behavior during all locomotor tasks, jointly occupying 62-84% of the time when the gaze was directed at the surface. As visual complexity of the surface and demand on visual guidance of stepping increased, cats spent more time looking at the surface, looked closer to them, and switched between gaze behaviors more often. During both visually guided locomotor tasks, gaze behaviors predominantly followed a repeated cycle of forward gaze shift followed by fixation. We call this behavior "gaze stepping". Each gaze shift took gaze to a site approximately 75-80cm in front of the cat, which the cat reached in 0.7-1.2s and 1.1-1.6 strides. Constant gaze occupied only 5-21% of the time cats spent looking at the walking surface.

Activity of motor cortex neurons during backward locomotion.

Forward walking (FW) and backward walking (BW) are two important forms of locomotion in quadrupeds. Participation of the motor cortex in the control of FW has been intensively studied, whereas cortical activity during BW has never been investigated. The aim of this study was to analyze locomotion-related activity of the motor cortex during BW and compare it with that during FW. For this purpose, we recorded activity of individual neurons in the cat during BW and FW. We found that the discharge frequency in almost all neurons was modulated in the rhythm of stepping during both FW and BW. However, the modulation patterns during BW and FW were different in 80% of neurons. To determine the source of modulating influences (forelimb controllers vs. hindlimb controllers), the neurons were recorded not only during quadrupedal locomotion but also during bipedal locomotion (with either forelimbs or hindlimbs walking), and their modulation patterns were compared. We found that during BW (like during FW), modulation in some neurons was determined by inputs from limb controllers of only one girdle, whereas the other neurons received inputs from both girdles. The combinations of inputs could depend on the direction of locomotion. Most often (in 51% of forelimb-related neurons and in 34% of the hindlimb-related neurons), the neurons received inputs only from their own girdle when this girdle was leading and from both girdles when this girdle was trailing. This reconfiguration of inputs suggests flexibility of the functional roles of individual cortical neurons during different forms of locomotion.

Activity of pyramidal tract neurons in the cat during standing and walking on an inclined plane.

To keep balance when standing or walking on a surface inclined in the roll plane, the cat modifies its body configuration so that the functional length of its right and left limbs becomes different. The aim of the present study was to assess the motor cortex participation in the generation of this left/right asymmetry. We recorded the activity of fore- and hindlimb-related pyramidal tract neurons (PTNs) during standing and walking on a treadmill. A difference in PTN activity at two tilted positions of the treadmill (+/- 15 deg) was considered a positional response to surface inclination. During standing, 47% of PTNs exhibited a positional response, increasing their activity with either the contra-tilt (20%) or the ipsi-tilt (27%). During walking, PTNs were modulated in the rhythm of stepping, and tilts of the supporting surface evoked positional responses in the form of changes to the magnitude of modulation in 58% of PTNs. The contra-tilt increased activity in 28% of PTNs, and ipsi-tilt increased activity in 30% of PTNs. We suggest that PTNs with positional responses contribute to the modifications of limb configuration that are necessary for adaptation to the inclined surface. By comparing the responses to tilts in individual PTNs during standing and walking, four groups of PTNs were revealed: responding in both tasks (30%); responding only during standing (16%); responding only during walking (30%); responding in none of the tasks (24%). This diversity suggests that common and separate cortical mechanisms are used for postural adaptation to tilts during standing and walking.

Maintenance of lateral stability during standing and walking in the cat.

During free behaviors animals often experience lateral forces, such as collisions with obstacles or interactions with other animals. We studied postural reactions to lateral pulses of force (pushes) in the cat during standing and walking. During standing, a push applied to the hip region caused a lateral deviation of the caudal trunk, followed by a return to the initial position. The corrective hindlimb electromyographic (EMG) pattern included an initial wave of excitation in most extensors of the hindlimb contralateral to push and inhibition of those in the ipsilateral limb. In cats walking on a treadmill with only hindlimbs, application of force also caused lateral deviation of the caudal trunk, with subsequent return to the initial position. The type of corrective movement depended on the pulse timing relative to the step cycle. If the force was applied at the end of the stance phase of one of the limbs or during its swing phase, a lateral component appeared in the swing trajectory of this limb. The corrective step was directed either inward (when the corrective limb was ipsilateral to force application) or outward (when it was contralateral). The EMG pattern in the corrective limb was characterized by considerable modification of the hip abductor and adductor activity in the perturbed step. Thus the basic mechanisms for balance control in these two forms of behavior are different. They perform a redistribution of muscle activity between symmetrical limbs (in standing) and a reconfiguration of the base of support during a corrective lateral step (in walking).

Influences of sensory input from the limbs on feline corticospinal neurons during postural responses.

The dorsal-side-up body posture of standing quadrupeds is maintained by coordinated activity of all limbs. Somatosensory input from the limbs evokes postural responses when the supporting surface is perturbed. The aim of this study was to reveal the contribution of sensory inputs from individual limbs to the posture-related modulation of pyramidal tract neurons (PTNs) arising in the primary motor cortex. We recorded the activity of PTNs from the limb representation of motor cortex in the cat maintaining balance on a platform periodically tilted in the frontal plane. Each PTN was recorded during standing on four limbs, and when two or three limbs were lifted from the platform and thus did not signal its displacement to motor cortex. By comparing PTN responses to tilts in different tests we found that the amplitude and the phase of the response in the majority of them were determined primarily by the sensory input from the corresponding contralateral limb. In a portion of PTNs, this input originated from afferents of the peripheral receptive field. Sensory input from the ipsilateral limb, as well as input from limbs of the other girdle made a much smaller contribution to the PTN modulation. These results show that, during postural activity, a key role of PTNs is the feedback control of the corresponding contralateral limb and, to a lesser extent, the coordination of posture within a girdle and between the two girdles.

Activity of pyramidal tract neurons in the cat during postural corrections.

The dorsal side-up body orientation in quadrupeds is maintained by a postural control system. We investigated participation of the motor cortex in this system by recording activity of pyramidal tract neurons (PTNs) from limb representations of the motor cortex during postural corrections. The cat was standing on the platform periodically tilting in the frontal plane, and maintained equilibrium at different body configurations: with the head directed forward (symmetrically alternating loading of the left and right fore limbs), or with the head voluntary turned to the right or to the left (asymmetrical loading). We found that postural corrective responses to tilts included an increase of the contact forces and activity of limb extensors on the side moving down, and their decrease on the opposite side. The activity of PTNs was strongly modulated in relation to the tilt cycle. Phases of activity of individual PTNs were distributed over the cycle. Thus the cortical output mediated by PTNs appeared closely related to a highly automatic motor activity, the maintenance of the body posture. An asymmetrical loading of limbs, caused by head turns, resulted in the corresponding changes of motor responses to tilts. These voluntary postural modifications were also well reflected in the PTNs' activity. The activity of a part of PTNs correlated well with contact forces, in some others with the limb muscle activity; in still others no correlation with these variables was observed. This heterogeneity of the PTNs population suggests a different functional role of individual PTNs.

Stimulation of the mesencephalic locomotor region elicits controlled swimming in semi-intact lampreys.

The role of the mesencephalic locomotor region (MLR) in initiating and controlling the power of swimming was studied in semi-intact preparations of larval and adult sea lampreys. The brain and the rostral portion of the spinal cord were exposed in vitro, while the intact caudal two-thirds of the body swam freely in the Ringer's-containing chamber. Electrical microstimulation (2-10 Hz; 0. 1-5.0 microA) within a small periventricular region in the caudal mesencephalon elicited well-coordinated and controlled swimming that began within a few seconds after the onset of stimulation and lasted throughout the stimulation period. Swimming stopped several seconds after the end of stimulation. The power of swimming, expressed by the strength of the muscle contractions and the frequency and the amplitude of the lateral displacement of the body or tail, increased as the intensity or frequency of the stimulating current were increased. Micro-injection of AMPA, an excitatory amino acid agonist, into the MLR also elicited active swimming. Electrical stimulation of the MLR elicited large EPSPs in reticulospinal neurons (RS) of the middle rhombencephalic reticular nucleus (MRRN), which also displayed rhythmic activity during swimming. The retrograde tracer cobalt-lysine was injected into the MRRN and neurons (dia. 10-20 microm) were labelled in the MLR, indicating that this region projects to the rhombencephalic reticular formation. Taken together, the present results indicate that, as higher vertebrates, lampreys possess a specific mesencephalic region that controls locomotion, and the effects onto the spinal cord are relayed by brainstem RS neurons.

Role of different sensory inputs for maintenance of body posture in sitting rat and rabbit.

In this paper, we describe the postural activity in sitting rats and rabbits. An animal was positioned on the platform that could be tilted in the frontal plane for up to +/-20-30 degrees, and postural corrections were video recorded. We found that in both rat and rabbit, the postural reactions led to stabilization of the dorsal-side-up trunk orientation. The result of this was that the trunk tilt constituted only approximately 50% (rat) and 25% (rabbit) of the platform tilt. In addition, in the rabbit the head orientation was also stabilized. Trunk stabilization persisted in the animals subjected to the bilateral labyrinthectomy and blindfolding, suggesting that the somatosensory input is primarily responsible for trunk stabilization. Trunk stabilization was due to extension of the limbs on the side moving down, and flexion of the opposite limbs. EMG recordings showed that the limb extension was caused by the active contraction of extensor muscles. We argue that signals from the Golgi tendon organs of the extensor muscles may considerably contribute to elicitation of postural corrective responses to the lateral tilt.

Sharp, local synchrony among putative feed-forward inhibitory interneurons of rabbit somatosensory cortex.

Many suspected inhibitory interneurons (SINs) of primary somatosensory cortex (S1) receive a potent monosynaptic thalamic input (thalamocortical SINs, SINstc). It has been proposed that nearly all such SINstc of a S1 barrel column (BC) receive excitatory synaptic input from each member of a subpopulation of neurons within the topographically aligned ventrobasal (VB) thalamic barreloid. Such a divergent and convergent network leads to several testable predictions: sharply synchronous activity should occur between SINstc of a BC, sharp synchrony should not occur between SINstc of neighboring BCs, and sharp synchrony should not occur between SINs or other neurons of the same BC that do not receive potent monosynaptic thalamic input. These predictions were tested by cross-correlating the activity of SINstc of the same and neighboring BCs. Correlations among descending corticofugal neurons of layer 5 (CF-5 neurons, identified by antidromic activation) and other neurons that receive little or no monosynaptic VB input also were examined. SINs were identified by a high-frequency (>600 Hz) burst of three or more spikes elicited by VB stimulation and had action potentials of short duration. SINstc were further differentiated by short synaptic latencies to electrical stimulation of VB thalamus (<1.7 ms) and to peripheral stimulation (<7.5 ms). The above predictions were confirmed fully. 1) Sharp synchrony (+/-1 ms) was seen between all SINstc recorded within the same BC (a mean of 4.26% of the spikes of each SINtc were synchronized sharply with the spikes of the paired SINtc). Sharp synchrony was not dependent on peripheral stimulation, was not oscillatory, and survived general anesthesia. Sharp synchrony was superimposed on a broader synchrony, with a time course of tens of milliseconds. 2) Little or no sharp synchrony was seen when CF-5 neurons were paired with SINstc or other neurons of the same BC. 3) Little or no sharp synchrony was seen when SINstc were paired with other SINstc located in neighboring BCs. Intracellular recordings obtained from three SINs in the fully awake state supported the assertion that SINs are GABAergic interneurons. Each of these cells met our extracellular criteria for identification as a SIN, each had a spike of short duration (0.4-0.5 ms), and each responded to a depolarizing current pulse with a nonadapting train of action potentials. These results support the proposed network linking VB barreloid neurons with SINstc within the topographically aligned BC. We suggest that sharp synchrony among SINstc results in highly synchronous inhibitory postsynpatic potentials (IPSPs)in the target neurons of these cells and that these summated IPSPs may be especially effective when excitatory drive to target cells is weak and asynchronous.

The role of the motor cortex in the control of accuracy of locomotor movements in the cat.

1. The impulse activity of single neurones in the motor cortex (MC) was recorded extracellularly, using movable varnish-insulated tungsten microelectrodes, in six adult, freely moving cats. Neuronal activity was recorded while the cats walked on a flat floor, as they stepped over a series of barriers, and as they walked on the flat rungs of a horizontal ladder. The mean discharge rate (mR) and the depth of frequency modulation (dM) in each cell were estimated over 10-100 steps. 2. The activity of ninety-eight MC cells (Including thirteen pyramidal tract neurones (PTNs)) was recorded during stepping over barriers 25 cm apart. The mR in 66% and the dM in 61% of these cells changed by more than 20% during locomotion with barriers compared to locomotion on the flat (an increase was more often the case). 3. The activity of nine cells was recorded during stepping over barriers 12 cm apart, and the activity of twenty-seven cells (including five PTNs) during walking with barriers only 6 cm apart. The mR in 67% and in 59% of the cells, respectively, and the dM in 56% and in 67% of the cells, respectively, were greater in these locomotor tasks than during locomotion on the flat. 4. The activity of twenty cells was recorded during walking and compared in experiments with different distances between barriers. The mR in 50% and the dM in 75% of the neurones progressively increased when the distance between successive barriers was diminished. 5. The discharge rates of thirteen cells were compared in two different locomotor tasks: (i) when the cat stepped over barriers requiring hyperflexion of the limbs and (ii) when it walked on the flat with loads attached to the distal forelimbs causing a hyperactivity of flexor muscles. The activity of nine cells was different during stepping over the barriers compared to locomotion with loadings on the forelimbs. 6. The activity of 108 cells (twenty-four PTNs) was recorded during walking along a horizontal ladder with flat rungs. The mR of 61% and the dM of 72% of cells changed by more than 20% during locomotion on the ladder compared with that on the flat (most often they increased). 7. The position of the peak rate relative to the step cycle did not differ in the majority of cells (in 78-91% depending on the task) during locomotion on the flat, with the barriers or on the ladder.(ABSTRACT TRUNCATED AT 400 WORDS)

The role of the motor cortex in the control of vigour of locomotor movements in the cat.

1. The impulse activity of single neurones in the motor cortex (MC) was recorded extracellularly using movable varnish-insulated tungsten microelectrodes in four adult freely moving cats. The cats walked inside the experimental box with various loadings in the swing or stance phases of the step cycle. The mean discharge rate (mR) and the depth of frequency modulation (dM) in each neurone were estimated over 10-100 steps. 2. The activity of thirty-one cells (including eighteen pyramidal tract neurones (PTNs)) was recorded during uphill walking on a 10 deg inclined floor. The mR in 68%, and the dM in 77% of neurones changed by less than 20% during uphill locomotion compared to walking on a level surface. 3. The activity of the same neurones was also recorded during downhill walking, also on a 10 deg inclined plane. The mR in 69% and the dM in 78% of neurones changed by less than 20% during downhill locomotion compared with walking on a level surface. 4. The activity of twenty-three (the left hemisphere) cells (sixteen PTNs) during walking with the floor swaying to the right (R) and to the left (L) was compared to activity during locomotion on a stable surface. The mR in 83% and the dM in 83% of cells in R-steps, and in 82 and 77% of cells, respectively, in L-steps changed by less than 20%. 5. The activity of thirty-seven cells was studied during locomotion at various speeds. The mR in 68% and the dM in 38% of cells changed by less than 20% during fast and slow locomotion compared to middle-speed locomotion. The dM in 46% of neurones increased with the transfer from slow to fast walking. 6. The activity of thirty-one MC cells was recorded during locomotion with loads of 85 g attached to the distal part of each elbow. The mR in 52% and the dM in 48% of neurones changed by more than 20%. 7. The activity of twenty-eight cells (six PTNs) was studied in steps when an animal turned. The swing of the limb contralateral to the recorded MC was shorter (condition 1) in turning steps in one direction, and was longer (condition 2) in turning steps in the opposite direction. The mR in 50% and the dM in 50% of cells in condition 1 and in 52% and 59%, respectively, of cells in condition 2 changed by more than 20%.(ABSTRACT TRUNCATED AT 400 WORDS)

Changes in monkey horizontal semicircular canal afferent responses after spaceflight.

Extracellular responses from single horizontal semicircular canal afferents in two rhesus monkeys were studied after recovery from a 14-day biosatellite (COSMOS 2044) orbital spaceflight. On the 1st postflight day, the mean gain for 9 different horizontal canal afferents, tested using one or several different passive yaw rotation waveforms, was nearly twice that for 20 horizontal canal afferents similarly tested during preflight and postflight control studies. Adaptation of the afferent response to passive yaw rotation on the 1st postflight day was also greater. These results suggest that at least one component of the vestibular end organ (the semicircular canals) is transiently modified after exposure to 14 days of microgravity. It is unclear whether the changes are secondary to other effects of microgravity, such as calcium loss, or an adaptive response. If the response is adaptive, then this report is the first evidence that the response of the vestibular end organ may be modified (presumably by the central nervous system via efferent connections) after prolonged unusual vestibular stimulation. If this is the case, the sites of plasticity of vestibular responses may not be exclusively within central nervous system vestibular structures, as previously believed.

[Activity of neurons of the motor-sensory cortex of the cat during natural walking on the rungs of a horizontal ladder]. / Aktivnost' neironov motosensornoi kory koshki vo vremia estestvennoi khod'by po perekladinam gorizontal'noi lestnitsy.

During locomotion on a flat surface and walking on crosspieces of a horizontal ladder the activity of 56 motor cortex neurons in the cat (5 identified cortico-spinal and 6 cortico-rubral neurons among them) was modulated in the rhythm of steps, i.e. it increased in one phase of a step and decreased in the other. The results of complication of locomotion task by the necessity of putting paws right on the support (fulcrum) while walking on the horizontal ladder were as follows: an increase of average activity of 19 neurons by 60 +/- 8% and a decrease of average activity of 19 neurons by 29 +/- 4%; growth of the modulation depth of 41 neurons (5 cortico-spinal and 6 cortico-rubral neurons) on the average by 68 +/- 19% for CS, 34 +/- 18% for CR and 36 +/- 5% for nonidentified neurons; temporary distribution of activity of 88% neurons in the step cycle while walking on the crosspieces of a horizontal ladder was that of walking on the flat surface.

[Activity of neurons of the motor-sensory cortex of the cat during natural locomotion while stepping over obstacles]. / Aktivnost' neironov motosensornoi kory koshki vo vremia estestvennoi khod'by s pereshagivaniem cherez prepiatstviia.

During locomotion on flat surface and while walking with stepping over obstacles the activity of 68 motor cortex neurons in cat (there were 12 pyramidal tract neurons (PTN) among them) was modulated in the rhythm of steps, i.e. it increased in one phase of a step and decreased in the other. The results of complication of locomotion task by the necessity to swing of the limbs over obstacles were as follows: an increase of average activity of 34 neurons by 75 +/- 15% and a decrease of the activity of 20 neurons by 30 +/- 4%; growth of modulation depth of 40 neurons (9 PTN) by 35 +/- 5% on the average for non-PTN and by 67 +/- 32% on the average for PTN; temporary distribution of the activity of 81 neurons in the step cycle while walking with stepping over obstacles was that of walking on the flat surface.

[Effect of immersion hypokinesia on the characteristics of programmed-type voluntary movements]. / Vliianie immersionnoi gipokinezii na kharakteristiki proizvol'nykh dvizhenii programmnogo tipa.

The effect of immersion hypokinesia on the precision of programme-type voluntary movements was investigated using standard test movements and quantitative analytical methods. The exposure did not cause disorders in the programme mechanisms but reduced significantly the precision range of the motor control system. The loss of precision was at its maximum (by 100% and over) on immersion day 3. The universality and consistency of the above changes indicated their close association with the specific exposure while the fast rate of their development suggested their reflex nature.