Motion processing across multiple topographic maps in the electrosensory system

• Published in: Physiological reports 2014-03, Vol.2 (3), p.e00253-n/a
• Main Authors: Khosravi‐Hashemi, Navid, Chacron, Maurice J.
• Format: Article
• Language: English
• Subjects: Behavior; Electrosensory system; Feedback; Information processing; Mathematical models; Motion detection; Neural coding; Original Research; Physiology; Pyramidal cells; pyramidal neuron; Receptive field; Sensory integration; Sensory properties; Sensory stimuli; Skin; Studies; Topography; Velocity; velocity tuning; weakly electric fish
• ISSN: 2051-817X; 2051-817X
• DOI: 10.1002/phy2.253

Animals can efficiently process sensory stimuli whose attributes vary over orders of magnitude by devoting specific neural pathways to process specific features in parallel. Weakly electric fish offer an attractive model system as electrosensory pyramidal neurons responding to amplitude modulations of their self‐generated electric field are organized into three parallel maps of the body surface. While previous studies have shown that these fish use parallel pathways to process stationary stimuli, whether a similar strategy is used to process motion stimuli remains unknown to this day. We recorded from electrosensory pyramidal neurons in the weakly electric fish Apteronotus leptorhynchus across parallel maps of the body surface (centromedial, centrolateral, and lateral) in response to objects moving at velocities spanning the natural range. Contrary to previous observations made with stationary stimuli, we found that all cells responded in a similar fashion to moving objects. Indeed, all cells showed a stronger directionally nonselective response when the object moved at a larger velocity. In order to explain these results, we built a mathematical model incorporating the known antagonistic center–surround receptive field organization of these neurons. We found that this simple model could quantitatively account for our experimentally observed differences seen across E and I‐type cells across all three maps. Our results thus provide strong evidence against the hypothesis that weakly electric fish use parallel neural pathways to process motion stimuli and we discuss their implications for sensory processing in general. e00253 It is widely believed that the brain uses parallel processing in order to process natural stimuli whose attributes can vary over several orders of magnitude. In weakly electric fish, previous studies have shown that parallel processing of stationary stimuli is achieved by three parallel maps of the body surface. Surprisingly, we found that this did not apply to the processing of motion stimuli. Thus, our results show that the coding strategies used for motion stimuli strongly differ from those used for stationary stimuli.