Multiple electrosensory maps in the medulla of weakly electric gymnotiform fish. II. Anatomical differences

Abstract

Both wave- and pulse-type species of weakly electric gymnotiform fish have 3 topographic maps of electroreceptive information in the electrosensory lateral line lobe (ELL). These maps receive identical input from trifurcating axons of phase- and amplitude-coding primary afferents (Carr et al., 1982; Heiligenberg and Dye, 1982). Physiological experiments in the ELL of the wave-type fish Eigenmannia show that the amplitude-coding pyramidal cells differ among maps with respect to receptive field size, sensitivity, rate of adaptation, and temporal-frequency response (Shumway, 1989). This study investigated morphological correlates of the physiological differences among maps. Estimates of primary afferent convergence in Eigenmannia, based on map size, cell counts, and areas of terminal fields from intracellularly filled P-type primary afferents, suggest a 2-fold increase in convergence in the lateral map relative to the centromedial map. Similar differences in convergence between maps are found in the wave-type species Apteronotus leptorhynchus and the pulse-type fish Hypopomus occidentalis. The lateral and centrolateral maps in Hypopomus, however, show an even greater difference in convergence. Comparison of the efferent projections of pyramidal cells among the different maps of Eigenmannia indicates that cells from the 3 maps terminate in the same laminae of the torus semicircularis, but the maps differ in the strength of projection to particular laminae. In both wave-type species, the abundance of a class of interneurons which receives descending input and inhibits pyramidal cells (interneurons of the ventral molecular layer) differs among maps; the centromedial map has 10 times fewer neurons of this type than the other 2 maps. Cytochrome oxidase studies in all 3 species demonstrated increased levels of activity in the lateral map, within the region receiving descending input from the cerebellum. These results suggest that the primary anatomical bases of the physiological differences among maps are differences in the amount of primary afferent convergence, coupled with differences in descending input.