Recordings from slices indicate that octopus cells of the cochlear nucleus detect coincident firing of auditory nerve fibers with temporal precision

Abstract

Acoustic information in auditory nerve discharges is integrated in the cochlear nuclei, and ascends through several parallel pathways to higher centers. Octopus cells of the posteroventral cochlear nucleus form a pathway known to carry information in the timing of action potentials. Octopus cells have dendrites oriented to receive converging input from many auditory nerve fibers. In all 34 intracellular recordings from anatomically identified octopus cells in slices, shocks to the auditory nerve evoked brief, consistent, graded EPSPs. EPSPs were about 1 msec in duration. At all but the lowest shock strengths, the delays between shocks and the peaks of resultant EPSPs had SDs of 0.02 msec. Polysynaptic excitation, perhaps arising from the axon collaterals of octopus cells, was observed. No detectable glycinergic or GABAergic inhibition was evoked with shocks. The input resistances were low, around 10 M omega, voltage changes were rapid, with time constants of about 1 msec, and action potentials were small. The low input resistance resulted in part from a Cs(+)-sensitive conductance. In the presence of 10 or 15 mM extracellular Cs+ the time constants increased 20-fold in the hyperpolarizing voltage range. As several subthreshold inputs were required to produce suprathreshold responses, octopus cells detect the coincident firing of auditory nerve fibers. Under physiological conditions the low input resistance and resulting short time constant limit the time over which temporal summation of excitation from auditory nerve fibers can occur and thus provide temporal precision to electrical signaling.

Coding interaural time differences at low best frequencies in the barn owl

“…These neurons require the summation of many synaptic inputs within a period of 1 ms to fire and thus detect coincident firing among their inputs [37]. In requiring the summation of many small inputs to produce a brief but robust synaptic response, the temporal jitter in the timing of individual auditory nerve inputs is lost in the firing of octopus cells.…”

Postsynaptic Targets of Type II Auditory Nerve Fibers in the Cochlear Nucleus.

“…1) and terminate in the cochlear nucleus (Lorente de No 1933;Fekete et al 1984;Brown et al 1988a). Type I fibers have an excitatory influence on their postsynaptic targets, leading to discharge of cochlear-nucleus neurons (Pfeiffer 1966;Golding et al 1995;Kopp-Scheinpflug et al 2002). Type I targets in the cochlear nucleus are a variety of types of neurons (Brawer and Morest 1975;Rouiller et al 1986), which have been classified by their morphology using different stains (Osen 1969;Brawer et al 1974).…”

A Functional Point-Neuron Model Simulating Cochlear Nucleus Ideal Onset Responses

“…Octopus cells have been assumed to act as coincidence detectors (e.g., Oertel et al, 2000) due to the large number of high-spontaneous rate AN fibers (Liberman, 1993) providing across-frequency excitatory AN input and due to their rapid membrane time constant (<200 µs) (Golding et al 1995(Golding et al , 1999. However, as was already shown by Kalluri and Delgutte (2003a), coincidence detection itself is not sufficient to simulate the ideal onset responses to pure tones observed in octopus cells.…”

“…The general ability of these cells to entrain to periodic stimuli has led to the assumption that octopus cells may play an important role in the processing of amplitude modulation and pitch information (Golding et al, 1995;Cai et al, 2001). Moreover, since octopus cells emphasize transient stimulus features like gaps and onsets, known to be important in speech processing (e.g., Stevens, 1995) as well as in auditory binding (e.g., Bregman, 1990), it has been suggested that they are also involved in these auditory tasks.…”

“…Their model essentially represents a coincidence detector as it is based on a short membrane time constant, τ m , and a large number of weak synaptic AN inputs. Viewing octopus cells as coincidence detectors across their AN input fibers became popular (i) due to the large number of high-spontaneous rate AN fibers (Liberman, 1993) providing across-frequency excitatory AN input and (ii) due to their rapid membrane time constant (<200 µs) (Golding et al, 1995(Golding et al, , 1999. Moreover, it has been found that an octopus cell is activated only if a sufficient number of AN fibers, causing small and rapid excitatory postsynaptic potentials, are activated within a small time window of approximately 1 ms (Oertel et al, 2000).…”