Activity of different classes of neurons of the motor cortex during postural corrections

Abstract

The dorsal side-up body orientation in quadrupeds is maintained by a postural system that is driven by sensory feedback signals. The spinal cord, brainstem, and cerebellum play essential roles in postural control, whereas the role of the forebrain is unclear. In the present study we investigated whether the motor cortex is involved in maintenance of the dorsal side-up body orientation. We recorded activity of neurons in the motor cortex in awake rabbits while animals maintained balance on a platform periodically tilting in the frontal plane. The tilts evoked postural corrections, i.e., extension of the limbs on the side moving down and flexion on the opposite side. Because of these limb movements, rabbits maintained body orientation close to the dorsal side up. Four classes of efferent neurons were studied: descending corticofugal neurons of layer V (CF5s), those of layer VI (CF6s), corticocortical neurons with ipsilateral projection (CCIs), and those with contralateral projection (CCCs). One class of inhibitory interneurons [suspected inhibitory neurons (SINs)] was also investigated. CF5 neurons and SINs were strongly active during postural corrections. In most of these neurons, a clear-cut modulation of discharge in the rhythm of tilting was observed. This finding suggests that the motor cortex is involved in postural control. In contrast to CF5 neurons, other classes of efferent neurons (CCI, CCC, CF6) were much less active during postural corrections. This suggests that corticocortical interactions, both within a hemisphere (mediated by CCIs) and between hemispheres (mediated by CCCs), as well as corticothalamic interactions via CF6 neurons are not essential for motor coordination during postural corrections.

Figure 1.

Experimental arrangement. A, Types of neurons that were recorded in the forelimb representation of the left motor cortex (MC). CCI, Corticocortical neurons projecting to the ipsilateral primary somatosensory cortex (S1); CCC, corticocortical neurons projecting to the contralateral motor (MC) or primary somatosensory cortex (S1); CF6, corticofugal neurons of layer VI projecting to the ventrolateral thalamus (VL); CF5, corticofugal neurons of layer V with collaterals projecting to the ventrolateral thalamus. These neuron types were identified by their antidromic responses to electrical stimulation of the corresponding structures (Stim 1-Stim 4). SIN, Putative inhibitory interneurons were identified by their high-frequency orthodromic responses to stimulation of ventrolateral thalamus or a cortical site (Stim 1-Stim 4). B, C, Location of the motor limb representation in the rabbit (a typical example). B, Schematic drawing of the hemispheres (dorsal view) and the limb representations. The dashed horizontal line indicates the zero anteroposterior coordinate. The square area shown in B is represented in C with a higher magnification to show the relative positions of motor representation of the forelimb (1), the primary somatosensory representations of the forelimb (2a) and the hind limb (2b), as well as that of the whiskers (3). D, E, A rabbit with implanted electrodes was positioned on a platform that was tilted periodically in the frontal (roll) plane (amplitude, ±15°). The rabbit tended to maintain the dorsal side-up orientation on the platform by extending the limbs on the side moving down. The forelimb with high extensor activity is shown in black in E. F, Periodic tilts of the platform caused alternating EMG responses of the left and right m. triceps and periodic responses of a CF5 neuron from the left motor cortex. The EMGs are presented as time histograms (Deliagina et al. 2000a); the spikes of the neuron were transformed into standard pulses for subsequent data processing. G, A frequency histogram for the CF5 neuron shown in D, averaged over eight tilt cycles. The cycle phase (φ) is indicated; the peak of the left tilt was taken as the cycle onset. The activity of the neuron exceeding the threshold (interrupted line) was considered as a burst.

Figure 6.

Responses of different classes of cortical neurons to trapezoid tilts. A, Activity of the left and right m. triceps during tilts. The EMG signals were rectified and smoothed. (Note dynamic and static components in the EMGs.) B, Schematic representation of the tilt cycle and of a response of a neuron (co and i = contralateral and ipsilateral tilt, respectively). The discharge frequency was calculated separately for each of the intervals (1-4) and then averaged over the successive tilt cycles. C, Relative number of neurons in each class (CF5, SIN, NI) responding preferentially to contralateral tilt (co group) and ipsilateral tilt (i group). For each group, a proportion of neurons with a dynamic response prevailing over a static response (D>S) and that with a static response prevailing over a dynamic response (S>D) are indicated. D, The discharge frequency in the dynamic and static responses evoked by tilt in a preferred direction, in different classes of neurons.

Figure 3.

Phase characteristics of CF5 neurons. A, Phase distribution of bursts of individual neurons in the tilt cycle, with the mid-burst phase indicated. The activity of each neuron is presented in bold only one time in the cycle. The neurons are rank ordered according to the mid-burst phase of the first burst. B, A histogram of the relative number of active neurons in different phases of the tilt cycle. C, A histogram of the mean frequency of active neurons in different phases of the tilt cycle. In A, the periods of increased and decreased activity of the right and left m. triceps (Tric R and Tric L) are shown schematically. In this and subsequent figures, φ is the cycle phase, and the peak left tilt is taken as the cycle onset.

Figure 4.

Phase characteristics of SINs. A, Phase distribution of bursts of individual neurons in the tilt cycle, with the mid-burst phase indicated. B, A histogram of the relative number of active neurons in different phases of the tilt cycle. C, A histogram of the mean frequency of active neurons in different phases of the tilt cycle. Designations are as in Fig. 3.

Figure 5.

Phase characteristics of NI neurons. A, Phase distribution of bursts of individual neurons in the tilt cycle, with the mid-burst phase indicated. B, A histogram of the relative number of active neurons in different phases of the tilt cycle. C, A histogram of the mean frequency of active neurons in different phases of the tilt cycle. Designations are as in Fig. 3.

Figure 2.

Population characteristics of different classes of neurons. A, Proportion of neurons responding to tilts in relation of their total number. B, Frequency in the burst and between the bursts. C, Coefficient of frequency modulation M = 1 - F_inter/F_burst. (Mean ± SEM are shown.)

Figure 7.

Comparison of activity of cortical neurons in postural and locomotor tasks. A, B, A histogram of activity of the CF5 neuron recorded initially in the postural task (A) and then in the locomotor task (B). In B, the swing and stance phases of the step cycle of the contralateral (right) forelimb are indicated, as well as an approximate phase of the extensor activity. C, Position of the mid-burst point in the tilt cycle and in the step cycle for 11 neurons recorded in the two motor tasks. The phase of increased extensor activity is indicated for both cycles (shaded area).