Sensitivity to time disparities requires convergence of phase-locked signals from two different sources onto a time comparator. The existence of such a circuit was predicted for Gymnarchus
(Kawasaki and Guo, 1996
) and is described here by Matsushita and Kawasaki. The ovoidal cell in the electrosensory lateral line lobe receives phase-locked synaptic input from a giant cell onto its cell body and phase-locked synaptic input from a single S-afferent onto its dendrite. This convergence of temporal information satisfies the requirement for a comparator circuit and predicts that the ovoidal cell will be sensitive to phase differences between different parts of the body surface.
This circuit in Gymnarchus
resembles a similar circuit in the unrelated South American weakly electric fish, Eigenmannia
). Both groups of weakly electric fish compare timing on the order of microseconds of sensory feedback from electric organ discharges received at different parts of its body surfaces. This capability is essential for and demonstrated by the jamming avoidance response (JAR). Gymnarchus
exhibit a nearly identical JAR and share a rather complex but identical set of computational algorithms for computing the appropriate JAR (Kawasaki, 1997
). Despite the algorithmic identity, Kawasaki and Guo (1996)
showed that one of the computational steps, the timing comparison between body surfaces, occurs in the hindbrain in Gymnarchus
, not in the midbrain as in Eigenmannia
. Thus, similar systems with a similar overall function evolved differently in different genera by assigning the same task to different brain regions.
The phase difference detectors may be located in the midbrain in Eigenmannia and in the lateral line lobe in Gymnarchus, but the organization of the circuit is remarkably similar in both. In Gymnarchus, timing of the electric organ discharge on a small part of the body surface is encoded by phase locked action potentials in the S-type primary afferent fibers. Each afferent projects onto the dorsal dendrite of the ovoidal cell. The giant cells receive inputs from multiple S-afferents so are able provide global timing information for a large part of the body surface. Because giant cells form large end-bulb–like synapses on the cell body of ovoidal cells, the ovoidal cells can act as the time comparators to compare arrival times of action potentials from one giant cell terminal with input from one S-afferent terminal.
, the equivalent of the S-type afferents encode the timing of the electric organ discharge on a small part of the body surface. Each projects to a relay neuron that sends a projection to a dendrite of phase comparator cell (Carr, 1993
). They also project to giant cells that form a large synapse on the cell body of the time comparator. Thus, the unrelated African and South American electric fish appear to have independently converged not only upon identical algorithms for encoding the timing of the stimulus, but also almost identical circuits for detecting timing differences between different parts of the body surface. In both cases, the fish receives a relayed timing signal onto its cell body and a direct timing signal onto its dendrite.
There is more to the story. The ovoidal cells contact the dendrite of pyramidal cells, which also receive S-afferent input. Pyramidal cells are also sensitive to phase differ-ences and project to the midbrain. The details of the ovoidal cell to pyramidal cell circuit remain to be determined, but it seems likely that ovoidal cells detect phase differences and pass that sensitivity onto the pyramidal cells by means of a dendrodendritic gap junction connection.
Although both auditory and electrosensory systems encode timing information and detect differences in the microsecond range, the time difference detector works differently in each system. Timing difference detectors in birds and mammals are bitufted neurons with inputs from each ear segregated onto two sets of dendrites (Carr et al., 2001
). The neurons act as coincidence detectors and fire maximally when inputs from the ears coincide (or almost coincide). Why are timing difference detector neurons assembled differently in the auditory and electrosensory systems? It seems unlikely that the similarity comes from a similar structure in common ancestors, because the two groups of weakly electric fish independently derived their electric sense, and birds and mammals independently evolved the ability to hear airborne sound. It seems more likely that computational constraints instead directed selection. Perhaps electric fish need to compare a global electrical signal with a local one, while the auditory system compares two equal signals, one from each ear.
Matsushita and Kawasaki’s study of a temporal difference detection circuit in the electrosensory system identifies computational strategies shared both with unrelated groups of electric fish, and with the auditory system of birds and mammals. The existence of parallel circuits allows us to identify shared algorithms and propose that these are suited to extracting the stimulus variables relevant for temporal coding.