From retina to motoneurons: A substrate for visuomotor transformation in salamanders

Abstract

The transformation of visual input into motor output is essential to approach a target or avoid a predator. In salamanders, visually guided orientation behaviors have been extensively studied during prey capture. However, the neural circuitry involved is not resolved. Using salamander brain preparations, calcium imaging and tracing experiments, we describe a neural substrate through which retinal input is transformed into spinal motor output. We found that retina stimulation evoked responses in reticulospinal neurons of the middle reticular nucleus, known to control steering movements in salamanders. Microinjection of glutamatergic antagonists in the optic tectum (superior colliculus in mammals) decreased the reticulospinal responses. Using tracing, we found that retina projected to the dorsal layers of the contralateral tectum, where the dendrites of neurons projecting to the middle reticular nucleus were located.In slices, stimulation of the tectal dorsal layers evoked glutamatergic responses in deep tectal neurons retrogradely labeled from the middle reticular nucleus. We then examined how tectum activation translated into spinal motor output. Tectum stimulation evoked motoneuronal responses, which were decreased by microinjections of glutamatergic antagonists in the contralateral middle reticular nucleus. Reticulospinal fibers anterogradely labeled from tracer injection in the middle reticular nucleus were preferentially distributed in proximity with the dendrites of ipsilateral motoneurons. Our work establishes a neural substrate linking visual and motor centers in salamanders. This retino-tecto-reticulo-spinal circuitry is well positioned to control orienting behaviors. Our study bridges the gap between the behavioral studies and the neural mechanisms involved in the transformation of visual input into motor output in salamanders.

Adeno-Associated Viral Tools to Trace Neural Development and Connectivity Across Amphibians

“…The study of the amphibian nervous system has enhanced our knowledge of the development and evolution of neural cell types. Historically, amphibians were instrumental in the discovery of the Spemann-Mangold embryonic organizer (reviewed in 1 ) and of fundamental mechanisms of synaptic transmission 2 More recent work on neuronal cell type determination, sensory processing, motor pattern generation, circuit formation, regeneration and plasticity [3][4][5][6][7][8][9][10][11][12][13] , as well as human neurodevelopmental disorders 14,15 has benefited greatly from the use of amphibian models. Finally, the amphibian's position in vertebrate evolution also enables inferences about nervous system adaptations across the evolutionary transition from aquatic to terrestrial environments 8,[16][17][18] .…”