Neuronal mechanisms of feedback postural control

Abstract

Different species maintain a basic body posture due to the activity of the postural control system. An efficient control of the body orientation, as well as the body configuration, is important for standing and during locomotion. A general goal of the present study was to analyze neuronal feedback mechanisms contributing to stabilization of the trunk orientation in space, as well as those controlling the body configuration. Two animal models of different complexity, the lamprey (a lower vertebrate) and the rabbit (a mammal), were used.

Neuronal mechanisms underlying lateral stability were analyzed in rabbits. The dorsalside- up trunk orientation in standing quadrupeds is maintained by the postural system driven mainly by somatosensory inputs from the limbs. Postural limb reflexes (PLRs) represent a substantial component of this system. To characterize spinal neurons of the postural networks, in decerebrate rabbit, activity of individual spinal neurons in L4-L6 was recorded during PLRs caused by lateral tilts of the supporting platform. Spinal neurons mediating PLRs have been revealed, and different parameters of their activity were characterized. All neurons were classified into four types according to the combination of tilt-related sensory inputs to a neuron from the ipsi- and contralateral limb (determining the modulation of a neuron). A hypothesis about the role of different types of PLR-related neurons for trunk stabilization in different planes has been proposed.

To reveal contribution of supraspinal influences to modulation of PLR-related neurons, the activity of individual spinal neurons was recorded during stimulation causing PLRs under two conditions: (i) when spinal neurons received supraspinal influences, and (ii) when these influences were temporarily abolished by a cold block of spike propagation in spinal pathways at T12 (“reversible spinalization”). The effects of reversible spinalization on individual neurons were diverse. Neurons, which did not receive supraspinal influences, were located mainly in the dorsal horn, whereas most neurons, receiving excitatory supraspinal influences were located in the intermediate zone and ventral horn. The population of PLRrelated neurons presumably responsible for disappearance of muscle tone and PLRs after spinalization was revealed.

The effects of manipulation with the tonic supraspinal drive (by means of binaural galvanic vestibular stimulation, GVS) on the postural system were studied. GVS creates asymmetry in tonic supraspinal drive, resulting in a lateral body sway towards the anode. This new body orientation is actively stabilized. To reveal the underlying mechanisms, spinal neurons were recorded during PLRs with and without GVS. It was found that GVS enhanced PLRs on the cathode side and reduced them on the anode side. It was suggested that GVS changes the set-point of the postural system through the change of the gain in antagonistic PLRs. Two sub-groups of PLR-related neurons presumably mediating the effect of GVS on PLRs were found.

An artificial feedback system was formed in which GVS-caused body sway was used to counteract the lateral body sway resulting from a mechanical perturbation of posture. It was demonstrated that the GVS-based artificial feedback was able to restore the postural function in rabbits with postural deficit. We suggested that such a control system could compensate for the loss of lateral stability of different etiology. Neuronal mechanisms underlying control of body configuration were analyzed in lampreys. The lamprey is capable of different forms of motor behavior: fast forward swimming (FFS), slow forward swimming (SFS), backward swimming (BS), forward and backward crawling, and lateral turns (LT). The amplitude of the body flexion (characterizing the body configuration) differs in different forms of motor behavior. In the lamprey, signals about the body configuration are provided by intraspinal stretch receptor neurons (SRNs). To clarify whether the networks generating different forms of motor behavior are located in the spinal cord, in chronic spinal lampreys, electrical stimulation of the spinal cord was performed. It was demonstrated that all forms of motor behavior are generated by the spinal networks.

To study SRN-mediated reflexes and their contribution to the control of body configuration in different motor behaviors, in the in vitro preparation we recorded responses of reticulospinal (RS) neurons and motoneurons (MNs) to bending of the spinal cord in different planes and at different rostro-caudal levels during different forms of fictive motor behavior Bending in the pitch plane during FFS caused SRN-mediated reflexes. MNs on the convex side were activated by pitch bending in the mid-body region. These reflexes will reduce the bend, thus contributing to maintenance of rectilinear body axis in the pitch plane during FFS.

It was found that bending in the yaw plane activated MNs on the convex side during FFS, but on the concave side during different forms of escape behavior (SFS, BS, LT). It was demonstrated that a reversal of reflex responses was due to ipsilateral supraspinal commands causing modifications of the spinal network located in the ipsi-hemicord. A population of RS neurons (residing in the middle rhombencephalic reticular nuclei) presumably transmitting these commands has been revealed. We suggest that modifications of SRN-mediated reflex responses will result in the decrease and increase of the lateral bending amplitude during FFS and escape behaviors, respectively, thus reinforcing movements generated in each specific behavior. Thus in the present study, for the first time, some neuronal mechanisms underlying reflex reversal in vertebrate animals have been revealed.