A time-comparison circuit in the electric fish midbrain. II. Functional morphology

Abstract

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.

SK Channels Provide a Novel Mechanism for the Control of Frequency Tuning in Electrosensory Neurons

“…The ELL is subdivided into four segments containing topographic maps of the fish body (Heiligenberg and Dye, 1982;Carr et al, 1986). The most medial segment (MS) receives input from ampullary receptors and was not assessed in this study.…”

Evolution of Time-Coding Systems in Weakly Electric Fishes

“…The difference from Gymnarchus is that the time-locking afferents (T-type afferents) terminate only on relay neurons in the hindbrain (ELL), the spherical cells, which send time-coding action potentials via their axons to the torus semicircularis of the midbrain. The axons of spherical cells branch and terminate on giant cells and small cell in Lamina VI of the torus semicircularis (Carr et al, 1986b). The giant cells are also time locked and spread their axons within Lamina VI.…”

“…The input time-locked axons divide into direct and indirect paths to provide inputs to time comparators; the time-comparator neurons (the small cells in Eigenmannia and Brienomyrus and the ovoidal cells in Gymnarchus) receive inputs from the indirect and direct paths for time comparison. Other similar properties include (1) large-diameter and fast-conducting axons in the time pathways, (2) adendritic somata in time-locked neurons, and (3) the existence of mixed synapses (electrical and chemical), both time-conserving synapses that conserve spike time sequence and time-comparing synapses that drive timecomparator postsynaptic neurons (Carr et al, 1986b;Matsushita and Kawasaki, 2004). Fast conduction is believed to contribute to the accurate conduction of timelocked firing with minimal jitter.…”

Representation of Accurate Temporal Information in the Electrosensory System of the African Electric Fish,Gymnarchus niloticus

“…The brain structures for phase comparison, however, differ in these two species of electric fishes. The phase comparison circuit exists in a midbrain structure, the torus semicircularis, in Eigenmannia Heiligenberg, 1985a, 1986a,b;Carr et al, 1986b) but in a hindbrain structure, the ELL, in Gymnarchus (Kawasaki and Guo, 1996).…”