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Journal of Neuroscience, Vol 9, 4400-4415, Copyright © 1989 by Society for Neuroscience
Multiple electrosensory maps in the medulla of weakly electric gymnotiform fish. II. Anatomical differences
CA Shumway
Neurobiology Unit, Scripps Institution of Oceanography, UCSD, La Jolla, California 92093.
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.
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