Neural mechanisms for the control of posture, locomotion and steering : a behavioral, electrophysiological and modeling study in lamprey

When animals move around interacting with the environment, the nervous system has to solve several tasks simultaneously in order to produce and control the movements - notably propulsion, posture, balance, and associated movements. Basic motor tasks are controlled by neuronal networks organized into central pattern generators (CPGs) and reflexes, located in the spinal cord and brainstem. The overall aim of this work has been to study how supraspinal descending control systems for locomotion, including control of movement direction, and postural control interact with each other, and with the spinal locomotor CPG in order to produce purposeful and economic movements.

Locomotion and postural corrections were studied in the lamprey, a lower vertebrate, in which the reticulospinal (RS) system is responsible for sensori-motor integration and descending control. Different aspects of locomotor activity - initiation, termination, and regulation of the intensity of locomotion, as well as steering and maintenance of a proper posture - were reflected in the activity of RS neurons in intact, freely swimming lampreys. In vitro studies have shown that groups of RS neurons in the middle and posterior rhombencephalic reticular nuclei are activated by vestibular and visual stimuli. Here, the activity of these neurons was correlated to the direction of fictive turns in a novel in vitro preparation. Commands for lateral turns can be initiated in rhombencephalon and are mediated by ipsilateral descending spinal pathways. Asymmetric descending command signals, such as the commands for turning and postural corrections, are amplified by a system of crossed reciprocal inhibition in the spinal cord and phasically modulated by the locomotor activity.

The alternating locomotor pattern is also dependent on crossed reciprocal inhibition between the two sides of the spinal cord. Crossing inhibitory neurons are subject to inhibition from a class of propriospinal neurons, the lateral interneurons (LINs), which have been considered as a possible burst terminating factor in the locomotor CPG. The LIN activity, however, is only weakly correlated to the output of the locomotor network. LINs receive input from RS neurons and may mediate descending commands related to motor function instead. Inhibitory mechanisms were also investigated in a light and electron microscopic study. A proportion of synaptic terminals in the lamprey spinal cord display immunoreactivity against two co-localized inhibitory neurotransmitters: glycine and GABA. Computer modeling of the neural mechanisms of lateral turns showed that locomotor models depending on LINs for burst termination did not generate turn-like patterns when LINs were activated. A strong activation of crossing inhibitory neurons by the descending turn command was necessary to generate turns in models of the locomotor network in which bursts are terminated by intrinsic properties of the crossing inhibitory neurons.

In many species of fish, the paired pectoral and pelvic fins are the main effector organs for stabilizing and changing the body orientation in the roll and pitch planes. Lampreys lack paired fins but the dorsal fin may provide better stability in the roll plane. Primary afferents from the fin appear to take part in a local monosynaptic resistance reflex that activates fin motoneurons.

List of scientific papers

I. Deliagina TG, Zelenin PV, Fagerstedt P, Grillner S, Orlovsky GN (2000). "Activity of reticulospinal neurons during locomotion in the freely behaving lamprey" J Neurophysiol 83(2): 853-863
https://pubmed.ncbi.nlm.nih.gov/20134657

II. Deliagina TG, Fagerstedt P (2000). "Responses of reticulospinal neurons in intact lamprey to vestibular and visual inputs" J Neurophysiol 83(2): 864-878
https://pubmed.ncbi.nlm.nih.gov/20134658

III. Fagerstedt P, Ullén F (2000). "Lateral turns in the lamprey. I: Pathway and phase dependence of lateral turns in the lamprey" J Neurophysiol (Accepted)

IV. Fagerstedt P, Orlovsky GN, Deliagina TG, Grillner S, Ullén F (2000). "Lateral turns in the lamprey. II: Reticulospinal commands during the generation of fictive turns" J Neurophysiol (Accepted)

V. Fagerstedt P, Zelenin PV, Deliagina TG, Orlovsky GN, Grillner S (2000). "Crossed reciprocal inhibition evoked by electrical stimulation of the lamprey spinal cord" Exp Brain Res (In Print)

VI. Fagerstedt P, Wallén P, Grillner S (2000). "Activity of lateral interneurons during fictive locomotion in the lamprey" (Submitted)

VII. Shupliakov O, Fagerstedt P, Ottersen OP, Storm-Mathiesen J, Grillner S, Brodin L (1996). "Immunocytochemical localization of glycine in the lamprey spinal cord with reference to GABAergic and glutamatergic synapses: a light and electron microscopic study" Acta Biol Hung 47(1-4): 393-410
https://pubmed.ncbi.nlm.nih.gov/97146809

VIII. El Manira A, Shupliakov O, Fagerstedt P, Grillner S (1996). "Monosynaptic input from cutaneous sensory afferents to fin motoneurons in lamprey" J Comp Neurol 369(4): 533-542
https://pubmed.ncbi.nlm.nih.gov/96354219

IX. Kozlov A, Ullén F, Fagerstedt P, Aurell E, Lansner A, Grillner S (2000). "Turning behaviour in lamprey in response to descending unilateral commands" (Submitted)