Neural Substrate of an Increase in Sensory Sampling Triggered by a Motor Command in a Gymnotid Fish

Abstract

Despite recent advances that have elucidated the effects of collateral of motor commands on sensory processing structures, the neural mechanisms underlying the modulation of active sensory systems by internal motor-derived signals remains poorly understood. This study deals with the neural basis of the modulation of the motor component of an active sensory system triggered by a central motor command in a gymnotid fish. In Gymnotus omarorum, activation of Mauthner cells, a pair of reticulospinal neurons responsible for the initiation of escape responses in most teleosts, evokes an abrupt and prolonged increase in the rate of the electric organ discharge (EOD), the output signal of the electrogenic component of the active electrosensory system. We show here that prepacemaker neural structures (PPs) that control the discharge of the command nucleus for EODs are key elements of this modulation. Retrograde labeling combined with injections of glutamate at structures that contain labeled neurons showed that PPs are composed of a bilateral group of dispersed brain stem neurons that extend from the diencephalon to the caudal medulla. Blockade of discrete PPs regions during the Mauthner cell-initiated electrosensory modulation indicate that the long duration of this modulation relied on activation of diencephalic PPs, whereas its peak amplitude depended on the recruitment of medullary PPs. Temporal correlation of motor and sensory consequences of Mauthner cell activation suggests that the Mauthner cell-initiated enhancement of electrosensory sampling is involved in the selection of escape trajectory.