Behavioral evidence for post-pause reduced responsiveness in the electrosensory system of Gymnotus carapo

Gymnotiform weakly electric fish find their way in the dark using a continuously operating active sensory system. An electric organ generates a continuous train of discharges (electric organ discharges, EODs), and tuberous high-frequency electroreceptors monitor the pattern of transcutaneous current flow associated with each EOD. Here, I report that a prior interruption to the continuous train of EODs dramatically affects a response shown by many pulse-type gymnotids. In this so-called novelty response, fish normally raise their electrosensory sampling rate in response to novel sensory stimuli. The gymnotid Gymnotus carapo was induced to pause its EODs briefly, and the novelty response to sensory stimuli given post-pause was analyzed. Mechanosensory stimuli given as early as 20 EODs after a pause elicited clear novelty responses, but strong high-frequency electrical stimuli were ineffective at this time. Moreover, high-frequency electrical stimuli remained less efficient in eliciting normal-sized responses until approximately 2000 EODs, or 40s, after a pause. The post-pause inefficiency of high-frequency stimuli was not due to an inappropriate choice of intensity or their temporal patterning and did not result from the stimulation that caused the pausing. Low-frequency stimuli that also recruited ampullary electroreceptors were more efficient than high-frequency stimuli in eliciting post-pause responses. These findings show that continuous activity is required either to maintain sensitivity to high-frequency electrical stimuli or to ensure that such stimuli are able to modulate efficiently the pacemaker that sets the discharge frequency.