Spinal and supraspinal postural networks

Abstract

Different species maintain a particular body orientation in space (upright in humans, dorsal-side-up in quadrupeds, fish and lamprey) due to the activity of a closed-loop postural control system. We will discuss operation of spinal and supraspinal postural networks studied in a lower vertebrate (lamprey) and in two mammals (rabbit and cat). In the lamprey, the postural control system is driven by vestibular input. The key role in the postural network belongs to the reticulospinal (RS) neurons. Due to vestibular input, deviation from the stabilized body orientation in any (roll, pitch, yaw) plane leads to generation of RS commands, which are sent to the spinal cord and cause postural correction. For each of the planes, there are two groups of RS neurons responding to rotation in the opposite directions; they cause a turn opposite to the initial one. The command transmitted by an individual RS neuron causes the motor response, which contributes to the correction of posture. In each plane, the postural system stabilizes the orientation at which the antagonistic vestibular reflexes compensate for each other. Thus, in lamprey the supraspinal networks play a crucial role in stabilization of body orientation, and the function of the spinal networks is transformation of supraspinal commands into the motor pattern of postural corrections. In terrestrial quadrupeds, the postural system stabilizing the trunk orientation in the transversal plane was analyzed. It consists of two relatively independent sub-systems stabilizing orientation of the anterior and posterior parts of the trunk. They are driven by somatosensory input from limb mechanoreceptors. Each sub-system consists of two closed-loop mechanisms - spinal and spino-supraspinal. Operation of the supraspinal networks was studied by recording the posture-related activity of corticospinal neurons. The postural capacity of spinal networks was evaluated in animals with lesions to the spinal cord. Relative contribution of spinal and supraspinal mechanisms to the stabilization of trunk orientation is discussed.

Figure 1

(A) During regular swimming, the lamprey stabilizes its orientation in the sagittal (pitch) plane, transversal (roll) plane, and horizontal (yaw) plane. 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. (B) Commands for correcting the orientation are formed on the basis of vestibular information, and transmitted from the brainstem to the spinal cord by reticulospinal (RS) neurons; many RS axons reach the most caudal spinal segments. Motor output of each segment is generated by four motoneuron (MN) pools controlling the dorsal and ventral parts of a myotome on the two sides (d and v pools). (C–H) Roll and pitch control systems. Key elements of each system are two groups of RS neurons. Due to vestibular inputs, activities of these two antagonistic groups are position-dependent; they cause rotation of the lamprey in opposite directions (arrows). Each system normally stabilizes the orientation with equal activities of the two groups (D,G). However, the stabilized orientation (equilibrium point) can be changed by a tonic drive to one of the groups (E,H).

Figure 2

(A,B) An RS neuron that contributed only to stabilization of the roll angle. (A) The neuron fired spikes in response 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. Arrows indicate the time of arrival of the RS spike to segment 30 (where motor output was monitored). (C,D) An RS neuron that contributed to stabilization of both roll and pitch angles. (C) The neuron fired spikes in response to left (contralateral) roll tilts and nose-up pitch tilts. (D) The neuron evoked excitation in the ipsilateral ventral branch of the ventral root, and inhibition in the ipsilateral dorsal branch. In B,D, a post-RS-spike histogram was generated for the spikes of motoneurons recorded in the dorsal and ventral branches of the left and right ventral roots. The moment of RS spike occurrence at the stimulated site was taken as the origin of the time axis in the histogram. Typically, responses to a few thousand RS spikes (up to 20 min of stimulation at 10 Hz) were used for generation of a histogram. (E) Relationships between vestibular responses and motor effects in individual RS neurons of the pitch control system. The neurons were divided into RS(UP) and RS(DOWN) groups according to their inputs (vestibular responses). For each group, the patterns of motor effects in 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 (excitation –red, inhibition – blue, no effect – white). Each RS neurons evoked a motor pattern (or a part of the pattern) opposing the initial turn that activated the neuron.

Figure 3

(A–D) Experimental design for testing postural responses to tilts in the cat. (A–C) the animal was standing on two platforms, one under the fore limbs and one under the hind limbs. Platforms could be tilted in the transverse plane (Tilt F and Tilt H) either in phase (C) or in anti-phase (D). Mechanical sensors BdF and BdH measured lateral displacements of the rostral and caudal parts of the trunk in relation to the corresponding platform. (E) Sensorimotor processing in the system stabilizing the back-up trunk orientation. The system consists of two sub-systems, one for the shoulder girdle and the other for the hip girdle (shown in A). They compensate for tilts of the anterior and posterior parts of the body, respectively. Each sub-system includes two controllers, one for the left limb and one for the right limb. Each limb controller contains a reflex mechanism driven by somatosensory input from its own limb. These local reflexes partly compensate for tilts. The limb controllers also receive somatosensory input from the contralateral limbs. The motor responses to these crossed influences are added to the local reflexes. The limb controllers exert influences on each other promoting their coordination. (F) Functional organization of the feedback mode of postural control in the hindquarters. Two closed-loop control systems (loops L1 and L2) stabilize the body orientation (see text for explanations).

Figure 4

Involvement of the motor cortex in postural control. (A) Activity of the forelimb pyramidal tract neuron (PTN) is modulated in relation to sinusoidal lateral tilts of the platform (Tilt) and postural corrections (Bd, lateral position of the body) in control (Test 1. Control) and during lifting of the hindlimbs (Test 2. Lift Hind). (B) Activity of the PTN (from the left forelimb representation) during different postural tests: Test 1 – control; Test 2 - lifting of the hindquarters; Test 3 - lifting of the forequarters; Test 4 - anti-phase tilts of the platforms under the forelimbs and hindlimbs; Test 5R - lifting of the hindquarters and left forelimb; Test 5L -lifting of the hindquarters and right forelimb; Test 7R – lifting of the left forelimb; Test 7L –lifting of the right forelimb. A phase histogram of spike activity in the tilt cycle is shown for each test. The activity was averaged over all consecutive cycles of a given test.