Active sensing associated with spatial learning reveals memory-based attention in an electric fish

Active sensing behaviors reveal what an animal is attending to and how it changes with learning. Gymnotus sp., a gymnotiform weakly electric fish, generates an electric organ discharge (EOD) as discrete pulses to actively sense its surroundings. We monitored freely behaving gymnotid fish in a large dark “maze” and extracted their trajectories and EOD pulse pattern and rate while they learned to find food with electrically detectable landmarks as cues. After training, they more rapidly found food using shorter, more stereotyped trajectories and spent more time near the food location. We observed three forms of active sensing: sustained high EOD rates per unit distance (sampling density), transient large increases in EOD rate (E-scans) and stereotyped scanning movements (B-scans) were initially strong at landmarks and food, but, after learning, intensified only at the food location. During probe (no food) trials, after learning, the fish's search area and intense active sampling was still centered on the missing food location, but now also increased near landmarks. We hypothesize that active sensing is a behavioral manifestation of attention and essential for spatial learning; the fish use spatial memory of landmarks and path integration to reach the expected food location and confine their attention to this region.

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

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.

Sensitivity to novel feedback at different phases of a gymnotid electric organ discharge

SUMMARY Weakly electric fish communicate and electrolocate objects in the dark by discharging their electric organs (EOs) and monitoring the spatiotemporal pattern of current flow through their skin. In the South-American pulse-type gymnotid fish these organs often are intriguingly complex, comprising several hundreds of electrogenic cells (electrocytes) of various morphologies,innervation patterns and abilities to generate a spike, distributed over nearly the full length of the fish. An attractive idea is that different parts of the organ may serve distinct functions in electrocommunication and electrolocation. Recent studies support this notion and suggest that the currents produced during the final phase of the electric organ discharge (EOD)are used for communication. Here, we explore a method to directly assess the relevance of the various currents for electrolocation. In this new method, the pattern of current flow during a gymnotid EOD is changed selectively at distinct phases of the EOD so that currents generated by known electrocyte groups are affected. We have studied the roles played by the various currents for the detection of novel feedback at the trunk/tail region of the gymnotid fish Gymnotus carapo. An experimental animal rested in a cage and two electrodes were placed at a close distance to its trunk and tail. An electronic switch briefly connected these electrodes during a selected phase within an EOD and the shunting of EOD current that resulted from switch closure was directly monitored. G. carapo responded with an acceleration of its discharge rate to novelties in the EOD feedback that occurred only for a fraction of a single EOD. Controls in which the switch was closed during the silent intervals between successive EODs showed that the fish responded to the changes in EOD feedback and not to unrelated artefacts of the brief switch closure. Fish responded to shunting of current during all phases; the sensitivity was highest during the final headnegative phase but the magnitude of shunted current was largest in the preceeding phase. The current produced during the final part of the EOD is thus not reserved for communication as previously suggested but plays a predominant role in electrolocation at the trunk and tail region of G. carapo.