Pre-receptor profile of sensory images and primary afferent neuronal representation in the mormyrid electrosensory system

SUMMARY Afferent responses to the fish's own electric organ discharge were explored in the electrosensory lobe of the mormyrid fish Gnathonemus petersii. In order to understand the neural encoding of natural sensory images, responses were examined while objects of different conductivities were placed at different positions along the skin of the fish, i.e. at different points within, and also outside, peripheral receptive fields. The presence of an object in the fish's self-generated electric field produces local modulation of transcutaneous current density. Measurement of the local electric organ discharge shows that object images formed at the electroreceptive sensory surface have an opposing center-surround, `Mexican hat' profile. This is a pre-receptor phenomenon intrinsic to the physical nature of the sensory stimulus that takes place prior to neural lateral inhibition and is independent of such central inhibition. Stimulus intensity is encoded in the latency and number of action potentials in the response of primary afferent fibers. It is also reflected in changes in the amplitude and area of extracellular field potentials recorded in the deep granular layer of the electrosensory lobe. Since the object image consists of a redistribution of current density over the receptive surface, its presence is coded by change in the activity of receptors over an area much larger than the skin surface facing the object. We conclude that each receptor encodes information coming from the whole scene in a manner that may seem ambiguous when seen from a single point and that, in order to extract specific object features, the brain must process the electric image represented over the whole sensory surface.