Corollary discharge enables proprioception from lateral line sensory feedback

Abstract

Animals modulate sensory processing in concert with motor actions. Parallel copies of motor signals, called corollary discharge (CD), prepare the nervous system to process the mixture of externally and self-generated (reafferent) feedback that arises during locomotion. Commonly, CD in the peripheral nervous system cancels reafference to protect sensors and the central nervous system from being fatigued and overwhelmed by self-generated feedback. However, cancellation also limits the feedback that contributes to an animal’s awareness of its body position and motion within the environment, the sense of proprioception. We propose that, rather than cancellation, CD to the fish lateral line organ restructures reafference to maximize proprioceptive information content. Fishes’ undulatory body motions induce reafferent feedback that can encode the body’s instantaneous configuration with respect to fluid flows. We combined experimental and computational analyses of swimming biomechanics and hair cell physiology to develop a neuromechanical model of how fish can track peak body curvature, a key signature of axial undulatory locomotion. Without CD, this computation would be challenged by sensory adaptation, typified by decaying sensitivity and phase distortions with respect to an input stimulus. We find that CD interacts synergistically with sensor polarization to sharpen sensitivity along sensors’ preferred axes. The sharpening of sensitivity regulates spiking to a narrow interval coinciding with peak reafferent stimulation, which prevents adaptation and homogenizes the otherwise variable sensor output. Our integrative model reveals a vital role of CD for ensuring precise proprioceptive feedback during undulatory locomotion, which we term external proprioception.

Hatchling fish disperse using an efficient multisensory strategy

“…One possible explanation for swimming adaptation following loss of flow sensing and vision is that hatchlings combine sensory information from both modalities to evaluate motion levels. The lateral line conveys signals not only about external flow but also motion generated by swimming [54], providing a gross readout of transport. Given that zebrafish can intensify swimming under restraint in virtual reality [55], we next tested the hypothesis hatchlings swim more vigorously without lateral line or visual sensation.…”

Multisensory strategies for postural compensation after lateral line loss

“…The lateral line, the swim bladder, and buoyancy Classical work has defined the role of the lateral line 3 , while recent studies have expanded our understanding of this remarkable organ. Functional investigation of the lateral line has demonstrated sophisticated comparisons of expected and observed patterns of flow during swimming [23][24][25][26][27] . Studies of lateral line neuromasts have revealed foundational principles of patterning 28,29 , organogenesis 30,31 , molecular and functional descriptions of hair cells [32][33][34] , and sensitivity to ototoxic compounds 35,36 .…”

Sensorimotor control of swimming Polypterus senegalus is preserved during sensory deprivation conditions across altered environments

“…The lateral line system appears to provide feedback about the fish's own movement ( Ayali et al, 2009 ). Furthermore, feedback between sequential lateral line neuromasts has been theorized to allow the calculation of body wave parameters such as wave frequency ( Skandalis et al, 2021 ). The body wave parameters encoded by sequential neuromasts could be altered or missing when the lateral line is blocked, resulting in changes in wave frequency as the fish is unable to determine its own movement.…”