Sensory-motor transformation by individual command neurons

Abstract

Animals and humans maintain a definite body orientation in space during locomotion. Here we analyze the system for the control of body orientation in the lamprey (a lower vertebrate). In the swimming lamprey, commands for changing the body orientation are based on vestibular information; they are transmitted to the spinal cord by reticulospinal (RS) neurons. The aim of this study was to characterize the sensory-motor transformation performed by individual RS neurons. The brainstem-spinal cord preparation with vestibular organs was used. For each RS neuron, we recorded (1) its vestibular responses to turns in different planes and (2) responses in different motoneuron pools of the spinal cord to stimulation of the same RS neuron; the latter data allowed us to estimate the direction of torque (caused by the RS neuron) that will rotate the animal's body during swimming. For each of the three main planes (roll, pitch, and yaw), two groups of RS neurons were found; they were activated by rotation in opposite directions and caused the torques counteracting the rotation that activated the neuron. In each plane, the system will stabilize the orientation at which the two groups are equally active; any deviation from this orientation will evoke a corrective motor response. Thus, individual RS neurons transform sensory information about the body orientation into the motor commands that cause corrections of orientation. The closed-loop mechanisms formed by individual neurons of a group operate in parallel to generate the resulting motor responses.

Figure 1.

A–C, During regular swimming, the lamprey stabilizes its orientation in the sagittal (pitch) plane (A), transversal (roll) plane (B), and horizontal (yaw) plane (C). Deviations from the stabilized orientation in these planes (angles α, β, and γ, respectively) evoke corrective motor responses (large arrows) aimed at restoration of the initial orientation. D, Commands for correcting the orientation are formed on the basis of vestibular information and transmitted from the brainstem to the spinal cord by RS neurons; many RS axons reach the most caudal spinal segments. Motor output of each segment is generated by four MN pools controlling the dorsal and ventral parts of a myotome on the two sides (d and v pools). E, The brainstem–spinal cord preparation with vestibular organs was used for studying vestibular inputs to individual RS neurons and their motor effects. The preparation was positioned in a chamber and perfused with Ringer's solution. The brainstem with vestibular organs could be rotated around three axes: transverse (pitch), longitudinal (roll), and vertical (yaw). d-Glutamate was applied to the spinal cord to elicit fictive locomotion. Individual neurons were recorded from their axons in the spinal cord. To stimulate a neuron, positive current pulses were passed through the recording intracellular microelectrode (ME). Activity of MNs was recorded bilaterally in segment 30 by suction electrodes, from the dorsal and ventral branches of a ventral root (id, ipsilateral dorsal branch; iv, ipsilateral ventral; cd, contralateral dorsal; cv, contralateral ventral). Electrodes placed on the spinal cord surface (SE1 in segment 1 and SE2 in segment 30) recorded antidromic and orhtodromic RS spikes, respectively.

Figure 2.

An RS neuron that contributed only to stabilization of the pitch angle. A, The neuron responded to nose-up pitch tilts only. B, The RS spike-triggered averaging has shown that the neuron evoked excitation in both ventral branches of ventral roots and did not influence both dorsal branches. The arrows in the histograms indicate the time of arrival of the RS spike to segment 30 (where motor output was monitored).

Figure 3.

An RS neuron that contributed only to stabilization of the roll angle. A, The neuron responded to right (contralateral) roll tilts only. B, The neuron evoked excitation in the left (ipsilateral) ventral and right (contralateral) dorsal branches of the ventral roots and inhibition in the right ventral and left dorsal branches.

Figure 4.

An RS neuron that contributed to stabilization of the roll and pitch angles. A, The neuron responded to the left (contralateral) roll tilts and nose-up pitch tilts. B, The neuron excited the ventral branch and inhibited the dorsal branch of the right (ipsilateral) ventral root. C, D, Motor effects of two symmetrical neurons of this type caused by rotation in the pitch plane (C) or roll plane (D). The patterns of motor effects are shown as circle diagrams, with the quadrants representing the MN pools projecting to the corresponding parts of myotomes. Different colors designate the type of effect (red, excitation; blue, inhibition; white, no effect). See Results for explanations.

Figure 5.

Relationships between vestibular responses and motor effects in individual RS neurons (n = 84). The neurons were grouped according to their inputs (vestibular responses). Groups 1–4 responded to turns in only one plane, groups 5–8 responded to turns in two planes, and group 9 responded to turns in all three planes. For each group, the patterns of motor effects produced by its neurons are shown as circle diagrams, with the quadrants representing the MN pools projecting to the corresponding parts of myotomes. Different colors designate the type of effect (red, excitation; blue, inhibition; white, no effect). Numbers below the diagrams show the number of neurons with a given pattern. contra, Contralateral; ipsi, ipsilateral.

Figure 6.

The combined effects of right (R) and left (L) RS neurons producing the same pattern in response to upward pitch turns (A), downward pitch turns (B), roll turns (C), and yaw turns (D). Designations are as in Figure 5. See Results for explanations.

Figure 7.

An RS neuron with non-specific vestibular inputs and motor effects. A, The neuron fired spikes in response to tilts in any direction. B, The neuron inhibited all MNs.

Figure 8.

The principle of stabilization of body orientation. The controlled variable φ is the pitch, roll, or yaw angle. Information about φ is delivered to RS neurons by the vestibular system (V). Two populations of neurons, RS(+) and RS(−), with opposite reactions to rotation and with opposite motor effects (arrows), constitute an essential part of the orientation control mechanism for each of the main planes. A deviation of φ from its stabilized value (φ = 0) toward positive or negative values will result in activation of a specific population of neurons, RS (+) (shown in red) or RS(−) (shown in blue), respectively. The activated RS neurons will cause a corrective motor response that counteracts the change in orientation and tends to return the animal to the initial position. In the pitch and roll planes, vestibular input provides information about the absolute value of φ. In these planes, the stabilized orientation (equilibrium point of the system) is the angle at which the activities of the two populations and therefore their motor effects are of the same magnitude. In the yaw plane, the vestibular system provides information only about dynamic changes of φ. To maintain a definite yaw angle, vestibular input should be supplemented by input from other sensory systems (e.g., visual) signaling the absolute value of φ.