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Journal of Neuroscience, Vol 6, 1372-1383, Copyright © 1986 by Society for Neuroscience
A time-comparison circuit in the electric fish midbrain. II. Functional morphology
CE Carr, L Maler and B Taylor
The weakly electric fish Eigenmannia is able to detect temporal disparities
as small as 400 nsec between two signals from different parts of the body
surface (Carr et al., 1986). The elements of this time-comparison circuit
have been identified by EM reconstruction of its component cells.
Information about the timing of the zero-crossing of signals on each area
of the body surface is coded in phase-coder receptors, a subset of tuberous
electroreceptors. Electroreceptors on the body surface are innervated by
primary afferents with their central termination on the spherical cells of
the medullary electrosensory lateral line lobe. These cells project to
lamina VI of the midbrain torus, a structure similar to the inferior
colliculus. Afferents entering lamina VI form a very restricted terminal
arbor in which they synapse on the three cell types of this lamina. Each
afferent makes gap- junction synapses on one or two giant cell somata and
morphologically mixed synapses on the distal dendrites of two types of
small cell. The afferent terminals thus encode the timing of the electric
signal on a local patch of the body surface, forming a somatotopic map of
the body surface in lamina VI. The giant cells are adendritic and their
axonal arbor is such as to distribute timing information originating from
one part of the body surface throughout lamina VI, so that each region of
lamina VI receives information about the timing of zero-crossings from the
entire body surface from giant cells, as well as information from a local
portion of the body surface from the afferent terminals. The giant cells
terminate exclusively on the cell bodies of the small cells of lamina VI,
shown to be sensitive to small temporal disparities by Heiligenberg and
Rose (1985). Thus, each small cell receives a single synapse on its soma
from a giant cell that conveys phase-coding information from some portion
of the body surface and receives local phase-coding input onto its
dendrites from spherical cell afferents. The sensitivity of the small cells
to temporal disparities appears to be conferred by their segregation of
inputs from two different parts of the body surface onto dendrites and
soma, respectively. We propose that the dendritic input acts as a delay
line, and the small cell fires maximally when the inputs from the dendrites
and the giant cell input onto the soma coincide.
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