Detection of synchrony in the activity of auditory nerve fibers by octopus cells of the mammalian cochlear nucleus

Abstract

The anatomical and biophysical specializations of octopus cells allow them to detect the coincident firing of groups of auditory nerve fibers and to convey the precise timing of that coincidence to their targets. Octopus cells occupy a sharply defined region of the most caudal and dorsal part of the mammalian ventral cochlear nucleus. The dendrites of octopus cells cross the bundle of auditory nerve fibers just proximal to where the fibers leave the ventral and enter the dorsal cochlear nucleus, each octopus cell spanning about one-third of the tonotopic array. Octopus cells are excited by auditory nerve fibers through the activation of rapid, calciumpermeable, ␣-amino-3-hydroxy-5-methyl-4-isoxazole-propionate receptors. Synaptic responses are shaped by the unusual biophysical characteristics of octopus cells. Octopus cells have very low input resistances (about 7 M⍀), and short time constants (about 200 sec) as a consequence of the activation at rest of a hyperpolarization-activated mixed-cation conductance and a lowthreshold, depolarization-activated potassium conductance. The low input resistance causes rapid synaptic currents to generate rapid and small synaptic potentials. Summation of small synaptic potentials from many fibers is required to bring an octopus cell to threshold. Not only does the low input resistance make individual excitatory postsynaptic potentials brief so that they must be generated within 1 msec to sum but also the voltage-sensitive conductances of octopus cells prevent firing if the activation of auditory nerve inputs is not sufficiently synchronous and depolarization is not sufficiently rapid. In vivo in cats, octopus cells can fire rapidly and respond with exceptionally well-timed action potentials to periodic, broadband sounds such as clicks. Thus both the anatomical specializations and the biophysical specializations make octopus cells detectors of the coincident firing of their auditory nerve fiber inputs.

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

“…Therefore, the deterministic discharge rate function is used as the timedependent AN input to the model, i.e., no individual spike trains for each AN fiber are computed. Such a convergent input agrees with observations from octopus cell recordings, although the actual number of AN fibers projecting onto an octopus cell has been difficult to estimate (e.g., Liberman, 1993;Oertel et al, 2000). In order to account for the wide across-frequency input that octopus cells receive (e.g., Oertel et al, 2000), the simulated AN activity is summed across a range of cochlear filters, such that each model unit receives equally weighted input from 11 cochlear filters spanning a frequency range of approximately one octave centered at the unit's CF.…”

“…Such a convergent input agrees with observations from octopus cell recordings, although the actual number of AN fibers projecting onto an octopus cell has been difficult to estimate (e.g., Liberman, 1993;Oertel et al, 2000). In order to account for the wide across-frequency input that octopus cells receive (e.g., Oertel et al, 2000), the simulated AN activity is summed across a range of cochlear filters, such that each model unit receives equally weighted input from 11 cochlear filters spanning a frequency range of approximately one octave centered at the unit's CF. In order to obtain the model input current from the output of the hair-cell model, it is multiplied by a constant synaptic conductance of 20 nS and convolved with an exponential function that decays with a time constant of 0.35 ms. With this choice of the synaptic conductance, a total synaptic input current of approx.…”

“…Kalluri and Delgutte (2003b) showed that their point-neuron coincidence-detector in combination with a spike-blocking mechanism accounts for temporal discharge patterns in response to individual tones in O I units, indicating that some of their responses can be understood from relatively simple principles. However, it will be shown in the present study that, due to its integrate-to-threshold dynamic and its fixed spike-blocking release threshold, the model does not account for O I -unit responses to tones covering a wide range of frequencies and sound pressure levels or for octopus cell responses to injected currents (e.g., Oertel et al, 2000;Ferragamo and Oertel, 2002).…”

“…The left panel of Fig. 6 shows recorded octopus cell data in response to increasing current steps, reprinted from Oertel et al (2000). When the cell is depolarized with a current pulse of 2 nA, it generates an action potential at the onset of the current pulse and remains at a low depolarization during the sustained portion of the current.…”

“…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). Kalluri and Delgutte (2003a) found that their point-neuron coincidence-detector model accounts for O L and O C responses, depending on the specific choice of particular model parameters, while O I unit responses cannot be accounted for.…”