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Single steps in different directions are often used for postural corrections. However, our knowledge about the neural mechanisms underlying their generation is scarce. This study was aimed to characterize the corrective steps generated in response to disturbances of the basic body configuration caused by forward, backward or outward displacement of the hindlimb, as well as to reveal location in the CNS of the corrective step generating mechanisms. Video recording of the motor response to translation of the supporting surface under the hindlimb along with contact forces and activity of back and limb muscles was performed in freely standing intact and in fixed postmammillary rabbits. In intact rabbits, displacement of the hindlimb in any direction caused a lateral trunk movement towards the contralateral hindlimb, and then a corrective step in the direction opposite to the initial displacement. The time difference between onsets of these two events varied considerably. The EMG pattern in the supporting hindlimb was similar for all directions of corrective steps. It caused the increase in the limb stiffness. EMG pattern in the stepping limb differed in steps with different directions. In postmammillary rabbits the corrective stepping movements, as well as EMG patterns in both stepping and standing hindlimbs were similar to those observed in intact rabbits. This study demonstrates that the corrective trunk and limb movements are generated by separate mechanisms activated by sensory signals from the deviated limb. The neuronal networks generating postural corrective steps reside in the brainstem, cerebellum, and spinal cord.

KEY POINTS Spinal reflexes are substantial components of the motor control system in all vertebrates and centrally driven reflex modifications are essential to many behaviours, but little is known about the neuronal mechanisms underlying these modifications. To study this issue, we took advantage of an in vitro brainstem-spinal cord preparation of the lamprey (a lower vertebrate), in which spinal reflex responses to spinal cord bending (caused by signals from spinal stretch receptor neurons) can be evoked during different types of fictive behaviour. Our results demonstrate that reflexes observed during fast forward swimming are reversed during escape behaviours, with the reflex reversal presumably caused by supraspinal commands transmitted by a population of reticulospinal neurons. NMDA receptors are involved in the formation of these commands, which are addressed primarily to the ipsilateral spinal networks. In the present study the neuronal mechanisms underlying reflex reversal have been characterized for the first time. ABSTRACT Spinal reflexes can be modified during different motor behaviours. However, our knowledge about the neuronal mechanisms underlying these modifications in vertebrates is scarce. In the lamprey, a lower vertebrate, body bending causes activation of intraspinal stretch receptor neurons (SRNs) resulting in spinal reflexes: activation of motoneurons (MNs) with bending towards either the contralateral or ipsilateral side (a convex or concave response, respectively). The present study had two main aims: (i) to investigate how these spinal reflexes are modified during different motor behaviours, and (ii) to reveal reticulospinal neurons (RSNs) transmitting commands for the reflex modification. For this purpose in in vitro brainstem-spinal cord preparation, RSNs and reflex responses to bending were recorded during different fictive behaviours evoked by supraspinal commands. We found that during fast forward swimming MNs exhibited convex responses. By contrast, during escape behaviours, MNs exhibited concave responses. We found RSNs that were activated during both stimulation causing reflex reversal without initiation of any specific behaviour, and stimulation causing reflex reversal during escape behaviour. We suggest that these RSNs transmit commands for the reflex modification. Application of the NMDA antagonist (AP-5) to the brainstem significantly decreased the reversed reflex, suggesting involvement of NMDA receptors in the formation of these commands. Longitudinal split of the spinal cord did not abolish the reflex reversal caused by supraspinal commands, suggesting an important role for ipsilateral networks in determining this type of motor response. This is the first study to reveal the neuronal mechanisms underlying supraspinal control of reflex reversal.

Central pattern generators consist of sets of interconnected neurons able to generate a basic motor output pattern underlying automatic movements (respiration, locomotion, chewing, swallowing, etc.) without any afferent signals from the executive motor apparatus. They are divided into constitutive pattern generators, which are active throughout life (the respiratory generator), and conditional pattern generators, which control episodic movements (locomotion, chewing, swallowing, etc.). As the motor output of a pattern generator is defined by its internal organization, the activity of conditional pattern generators is initiated by a simple command arriving from the higher centers. The structural-functional organization of the locomotor pattern generators in the marine mollusk Clione, the lamprey, the frog embryo, and laboratory mammals (cats, mice, and rats) are described, along with pattern generators controlling respiratory and swallowing movements in mammals and pattern generators for discharges of the electric organs of gymnotiform fish. Generation of the rhythmic motor output is shown in all cases to be based on the endogenous (pacemaker) activity of specific groups of interneurons and interneural interactions. These two interacting mechanisms supplement each other, ensuring the reliable operation of pattern generators. The question of whether experience gained from studies of central pattern generators can be used for understanding the mechanisms of more complex brain functions, including cognitive functions, is discussed.

The pelagic marine mollusk Clione limacina (class Gastropoda, subclass Opisthobranchaea, order Pteropoda), 3–5 cm in length, swims by rhythmically moving (1–2-Hz) two winglike appendages. Each swim cycle consists of two phases—the dorsal (D) and ventral (V) wing flexions. The nervous system of Clione consists of five pairs of ganglia. The wing movements are controlled by the pedal ganglia giving rise to the wing nerves. The neuronal circuit of the swim central pattern generator (CPG) is located in the pedal ganglia, which is able to generate the basic pattern of rhythmic activity after isolation from the organism (fictive swimming). Approximately 120 pedal neurons exhibit rhythmic activity during fictive swimming. According to their morphology, rhythmic neurons are divided into motoneurons (MNs), with axons exiting via the wing nerves to wing muscles, and interneurons (INs), with axons projecting to the contralateral ganglion.

The lamprey has two principal behavioral states—a quiescent state, when it is attached to the substrate with its sucker mouth; and an active state, when it locomotes. It is capable of several forms of locomotion, but it actively stabilizes its body orientation in space only during the main form, fast forward swimming. During fast forward swimming, orientation of the lamprey in the sagittal (pitch) and transversal (roll) planes is stabilized in relation to the gravity vector by means of the postural control systems driven by vestibular input. Any deviations from the stabilized orientation are reflected in vestibular signals, which cause corrective motor responses. In the pitch and yaw planes, the corrections occur due to the body bending in the corresponding plane. In the roll plane, the corrections occur due to a change in the direction of locomotor body undulations, from lateral to oblique.

In quadrupeds, acute lateral hemisection of the spinal cord (LHS) severely impairs postural functions, which recover over time. Postural limb reflexes (PLRs) represent a substantial component of postural corrections in intact animals. The aim of the present study was to characterize the effects of acute LHS on two populations of spinal neurons (F and E) mediating PLRs. For this purpose, in decerebrate rabbits, responses of individual neurons from L5 to stimulation causing PLRs were recorded before and during reversible LHS (caused by temporal cold block of signal transmission in lateral spinal pathways at L1), as well as after acute surgical LHS at L1. Results obtained after Sur-LHS were compared to control data obtained in our previous study. We found that acute LHS caused disappearance of PLRs on the affected side. It also changed a proportion of different types of neurons on that side. A significant decrease and increase in the proportion of F- and non-modulated neurons, respectively, was found. LHS caused a significant decrease in most parameters of activity in F-neurons located in the ventral horn on the lesioned side and in E-neurons of the dorsal horn on both sides. These changes were caused by a significant decrease in the efficacy of posture-related sensory input from the ipsilateral limb to F-neurons, and from the contralateral limb to both F- and E-neurons. These distortions in operation of postural networks underlie the impairment of postural control after acute LHS, and represent a starting point for the subsequent recovery of postural functions.

Postural limb reflexes (PLRs) represent a substantial component of postural corrections. Spinalization results in loss of postural functions, including disappearance of PLRs. The aim of the present study was to characterize the effects of acute spinalization on two populations of spinal neurons (F and E) mediating PLRs, which we characterized previously. For this purpose, in decerebrate rabbits spinalized at T12, responses of interneurons from L5 to stimulation causing PLRs before spinalization, were recorded. The results were compared to control data obtained in our previous study. We found that spinalization affected the distribution of F- and E-neurons across the spinal grey matter, caused a significant decrease in their activity, as well as disturbances in processing of posture-related sensory inputs. A two-fold decrease in the proportion of F-neurons in the intermediate grey matter was observed. Location of populations of F- and E-neurons exhibiting significant decrease in their activity was determined. A dramatic decrease of the efficacy of sensory input from the ipsilateral limb to F-neurons and from the contralateral limb to E-neurons was found. These changes in operation of postural networks underlie the loss of postural control after spinalization and represent a starting point for the development of spasticity.