Gating of steering signals through phasic modulation of reticulospinal neurons during locomotion

Abstract

The neural control of movements in vertebrates is based on a set of modules, like the central pattern generator networks (CPGs) in the spinal cord coordinating locomotion. Sensory feedback is not required for the CPGs to generate the appropriate motor pattern and neither a detailed control from higher brain centers. Reticulospinal neurons in the brainstem activate the locomotor network, and the same neurons also convey signals from higher brain regions, such as turning/steering commands from the optic tectum (superior colliculus). A tonic increase in the background excitatory drive of the reticulospinal neurons would be sufficient to produce coordinated locomotor activity. However, in both vertebrates and invertebrates, descending systems are in addition phasically modulated because of feedback from the ongoing CPG activity. We use the lamprey as a model for investigating the role of this phasic modulation of the reticulospinal activity, because the brainstem-spinal cord networks are known down to the cellular level in this phylogenetically oldest extant vertebrate. We describe how the phasic modulation of reticulospinal activity from the spinal CPG ensures reliable steering/turning commands without the need for a very precise timing of on-or offset, by using a biophysically detailed large-scale (19,600 model neurons and 646,800 synapses) computational model of the lamprey brainstem-spinal cord network. To verify that the simulated neural network can control body movements, including turning, the spinal activity is fed to a mechanical model of lamprey swimming. The simulations also predict that, in contrast to reticulospinal neurons, tectal steering/ turning command neurons should have minimal frequency adaptive properties, which has been confirmed experimentally.large-scale modeling | compartmental modelling | full-scale model | MLR

Referent control of action and perception

“…rhythmical opening and closing of afferent feedback to α-MNs or neurons of descending pathways (e.g. Duysens et al 1990 ;Kozlov et al 2014). In the framework of referent control, these modulations are indicative of central shifts in the spatial boundaries in which refl exes can function, rather than of opening and closing of refl exes at specifi c phases of motion.…”

“…It is also assumed that refl ex gain is modulated in time depending on the phase of movements. These fi ndings have motivated the concept of refl ex gating defi ned as the closing and opening of refl ex pathways produced by a CPG at different phases of movement ( Duysens et al 1990 ;Kozlov et al 2014 ).…”

Spatial distribution of intermingling pools of projection neurons with distinct targets: A 3D analysis of the commissural ganglia in Cancer borealis

“…This is particularly true for areas of the nervous system with apparent unstructured or variable organization. Relatively little is known about the functional and anatomical organization of descending neurons in motor control (but see Hsu & Bhandawat, 2016), despite their importance for motor pattern selection and modulation (Berkowitz, Roberts, & Soffe, 2010;Card, 2012;Deliagina, Beloozerova, Zelenin, & Orlovsky, 2008;Dubuc & Grillner, 1989;Herberholz & Marquart, 2012;Kozlov, Kardamakis, Hellgren Kotaleski, & Grillner, 2014;Le Ray, Juvin, Ryczko, & Dubuc, 2011;Nusbaum, 2009;Schuster, 2012;Stein, 2009). This is in part because of a dichotomy between functional and anatomical studies: functional studies are often concerned with one type or a particular group of neurons, while anatomical studies may not or only superficially address neuronal function.…”

Supraspinal control of spinal reflex responses to body bending during different behaviours in lampreys

“…; Kozlov et al . ). Second, the spinal networks, activated by spinal cord stimulation and by MLR stimulation, differ to some extent.…”

“…A similar result was obtained in the isolated spinal cord (Hsu et al 2013a). This finding suggests that, first, networks underlying concave responses to bending in the rostral segments could be selectively activated and thus contribute to the behaviours like steering during FFS that require large amplitude bending in the rostral part of the body Saitoh et al 2007;Kozlov et al 2014). Second, the spinal networks, activated by spinal cord stimulation and by MLR stimulation, differ to some extent.…”