Timing is everything: Organization of timing circuits in auditory and electrical sensory systems

Auditory and electrosensory systems are specialized to encode incoming sensory information, often with microsecond precision (Trussell, 2002). This kind of accurate coding is metabolically costly (Laughlin, 2001), but precise encoding of temporal information has direct behavioral relevance for sound localization and communication and appears to be the subject of selection. It is certainly true that the kinds of physiological and morphological adaptations that could improve temporal coding are found in the auditory brainstem of both birds and mammals and in the electrosensory system (Carr and Soares, 2002). Why do the auditory and electrosensory systems go to so much expense to preserve temporal information? Most timing information is directed to the goal of accurately detecting time differences between two signals. Once the time difference is computed, the temporal code can be transformed into a new and less energetically expensive code of time or phase difference. Comparative studies of temporal coding in the auditory and electrosensory systems, including one from Matsushita and Kawasaki in this issue of the Journal, have identified circuits to detect time differences in all systems. All of these timing circuits share similar computational strategies and many morphological features. In the auditory system, the secure and precise transmission of the phase-locked discharges of the auditory nerve fibers to their postsynaptic targets is mediated by the giant end-bulb synapse, which ensures fast, reliable, high-frequency excitatory transmission. Similarly shaped caliciform synapses are also present in higher order auditory neurons of mammalian time coding pathways, including neurons of the medial nucleus of the trapezoid body (Forsythe, 1994) and the type II neurons of the ventral nucleus of the lateral lemniscus (Wu, 2000) and in the chick ciliary ganglion (Paysan et al., 2000). In this issue, Matsushita and Kawasaki describe a new giant synapse in the electrosensory system of the weakly electric fish, Gymnarchus. The synapse originates from an electrosensory giant cell, which forms a socket-like structure around the cell body of an ovoidal cell. This study has two novel results. First, their discovery of a new nonfenestrated giant synapse raises the question of how such a synapse might function. Second, they describe a new circuit for detection of temporal disparity, leading to fresh insights into the functional organization of time coding circuits in auditory and electrosensory circuits.