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

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.

The Lesioned Spinal Cord Is a “New” Spinal Cord: Evidence from Functional Changes after Spinal Injury in Lamprey

“…The highly regular activity sought and presented in fictive locomotion studies may thus reflect a pathological loss of complexity ( Pincus, 1994 ; Bienenstock and Lehmann, 1998 ; Berg et al, 2007 ). Consistent with this, fictive activity differs to intact activity in being less susceptible to modification by sensory or descending inputs in both lamprey and mammals (see Fagerstedt and Ullén, 2001 ; Musienko et al, 2012 ; Hsu et al, 2016 ). These effects could reflect the tonic application of glutamate receptor agonists that contrasts the normal spatial and temporal variability of glutamate release, or the removal of descending and sensory inputs [see Cohen et al, 1996 ; Wang and Jung, 2002 ; in the tadpole spinal cord brainstem input is needed for normal locomotor activity ( Li et al, 2009 )].…”

Increasing Viscosity Helps Explain Locomotor Control in Swimming Polypterus senegalus

“…2017 ). Both stretch receptors and proprioceptors input directly into local circuits (and stretch receptors also provide feedback directly to the reticulospinal neurons), facilitating rapid adjustment of locomotor movements to changes in environment ( Hsu et al. 2016 ).…”

Early midbrain sensorimotor pathway is involved in the timely initiation and direction of swimming in the hatchling Xenopus laevis tadpole

“…The spinal central pattern generator (CPG) circuits are responsible for the generation of the basic locomotor rhythm, by establishing the appropriate sequence of muscle activation combined with reciprocal muscle inhibition (Buchanan and Grillner, 1987;Kiehn, 2006;Goulding, 2009;Roberts et al, 2010;Kiehn, 2016). In order to meet everchanging behavioral demands, the activity of spinal CPG is modulated by descending inputs originating in highly distributed supraspinal neuronal circuits (Dubuc et al, 2008;Lemon, 2008;El Manira and Grillner, 2014;Bouvier et al, 2015;Daghfous et al, 2016;Hsu et al, 2017;Arber and Costa, 2018;Ferreira-Pinto et al, 2018;Ruder and Arber, 2019;Grillner and El Manira, 2020;Arber and Costa, 2022).…”