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

Abstract

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.

The role of single spiking spherical neurons in a fast sensory pathway

“…Finally, the spherical cells of pulse fish have much in common with auditory cells of birds and mammals (Carr, 2004). The combination of conductances described is similar to that exhibited by bushy and octopus cells in mammalian ventral cochlear nucleus (Golding et al, 1999;Manis and Marx, 1991;Wu and Oertel, 1984;Brew and Forsythe, 1995;Oertel et al, 2000), and avian angularis, magnocellularis and lemniscal nucleus, which share with spherical cells the accurate transmission of information using a latency code (Trussell, 1999;Rathouz and Trussell, 1998;Reyes et al, 1994;Soares et al, 2002).…”

“…These comparative data suggest that single spiking cells and their intrinsic properties are a convergent solution in the evolution of sensory systems (Carr, 2004;Carr et al, 2005). However, species variations may adapt cell structure and specific functions reciprocally.…”

Perceptual Consequences of Disrupted Auditory Nerve Activity

“…Temporal dispersion in AN subjects is likely Ͼ1 ms as evidenced by the absence or significant delays (1-3 ms) of wave V in the auditory brain stem responses in AN subjects (Starr et al 2001(Starr et al , 2003. The desynchronized auditory nerve activity is likely to produce abnormal response in brain stem neurons that detect coincident firing of auditory nerve fibers (Carney 1990;Carr 2004;Golding et al 1995;Joris 1996;Joris et al 1998;Oertel et al 2000). These physiological mechanisms may underlie the observed perceptual changes in AN subjects.…”

Reciprocal Regulation of Presynaptic and Postsynaptic Proteins in Bipolar Spiral Ganglion Neurons by Neurotrophins

“…Spiral ganglion neurons, which are responsible for conveying auditory signals into the brain, must do so with remarkable precision to retain the timing and intensity information necessary to represent accurately features of the stimulus and its location (Carr, 2004). In addition to myriad specializations that typify the complex cochlear end organ (Rubel and Fritzsch, 2002;Raphael and Altschuler, 2003), previous studies from our laboratory established that the speed with which neurons are capable of responding to stimuli, along with their level of accommodation, vary systematically along the cochlear frequency map (Adamson et al, 2002b).…”