Characterization of the encoding properties of intraspinal mechanosensory neurons in the lamprey

Abstract

Proprioceptive sensory inputs are an integral part of the closed-loop system of locomotion. In the lamprey, a model organism for vertebrate locomotion, such sensory inputs come from intraspinal mechanosensory cells called "edge cells". These edge cells synapse directly onto interneurons in the spinal central pattern generator (CPG) circuit and allow the CPG to adjust the motor output according to how the body is bending. However, the encoding properties of the edge cells have never been fully characterized. To identify these properties and better understand edge cells' role in locomotion, we isolated spinal cords of silver lampreys (Ichthyomyzon unicuspis) and recorded extracellularly from the lateral tracts where edge cell axons are located. We identified cells that responded to mechanical stimuli and used standard spike sorting algorithms to identify separate units, then examined how the cells respond to bending rate and bending angle. Although some cells respond to the bending angle, as was previously known, the strongest and most common responses were to bending velocity. These encoding properties will help us better understand how lampreys and other basal vertebrates adapt their locomotor rhythms to different water flow patterns, perturbations, or other unexpected changes in their environments.

The role of curvature feedback in the energetics and dynamics of lamprey swimming: A closed-loop model

“…In the lamprey, proprioceptive feedback is mediated by mechanoreceptive cells in the spinal cord called edge cells [ 5 ]. When the spinal cord bends, one side is stretched, which activates edge cells on that side [ 5 , 13 ]. The greater the curvature, the stronger the activation [ 13 ].…”

“…When the spinal cord bends, one side is stretched, which activates edge cells on that side [ 5 , 13 ]. The greater the curvature, the stronger the activation [ 13 ]. The activated edge cells then inhibit activity on the opposite side and excite activity on the same side [ 7 ].…”

“…In these experiments, researchers record the response to different types of mechanical stimuli ( e.g. , [ 10 , 13 ]) or they record the effect of edge cells on the CPG due to mechanical inputs ( e.g. , [ 8 , 9 , 11 , 14 ]).…”

“…Although edge cells have been studied for a long time and their electrical activity is known to be affected by bending, their response properties are only beginning to be characterized. Current experiments indicate that they respond to both the magnitude of bending and the bending rate [ 13 ], but their effects on the CPG are not well understood, particularly in a closed-loop system with relatively small deviations from a steady sinusoidal oscillation. Here, we simulate different functional forms of mechanosensory feedback, and investigate how the choice of the feedback model affects swimming performance in the closed-loop neuromechanical system.…”

Body stiffness and damping depend sensitively on the timing of muscle activation in lampreys

“…Lampreys are a well-established model system for understanding the neural control of locomotion (Grillner 2003;Tytell et al 2011). In particular, they are the only vertebrate for which we know the cells and their connectivity that make up the central pattern generator, the neural circuit that generates locomotion (Grillner et al 1991;Parker 2006), and the only non-tetrapod vertebrate for which we know the proprioceptive sensory cells that allow the animal to sense its own movement (Grillner et al 1984;Massarelli et al 2017). Adult lampreys are active migratory fishes, capable of high speed swimming (Mesa et al 2003;Dauble et al 2006), though they are not quite as athletic as some teleost fishes (Quintella et al 2004).…”