Functional properties of auditory-nerve fibers during postnatal development in the kitten

Physiological response properties of neurons in the ventral cochlear nucleus have a variety of features that are substantially different from the stereotypical auditory nerve responses that serve as the principal source of activation for these neurons. These emergent features are the result of the varying distribution of auditory nerve inputs on the soma and dendrites of the various cell types within the nucleus; the intrinsic membrane characteristics of the various cell types causing different responses to the same input in different cell types; and secondary excitatory and inhibitory inputs to different cell types. Well-isolated units were recorded with high-impedance glass microelectrodes, both intracellularly and extracellularly. Units were characterized by their temporal response to short tones, rate vs. intensity relation, and response areas. The principal response patterns were onset, chopper, and primary-like. Onset units are characterized by a well-timed first spike in response to tones at the characteristic frequency. For frequencies less than 1 kHz, onset units can entrain to the stimulus frequency with greater precision than their auditory nerve inputs. This implies that onset units receive converging inputs from a number of auditory nerve fibers. Onset units are divided into three subcategories, OC, OL, and OI. OC units have extraordinarily wide dynamic ranges and low-frequency selectivity. Some are capable of sustaining firing rates of 800 spikes/s at high intensities. They have the smallest standard deviation and coefficient of variation of the first spike latency of any cells in the cochlear nuclei. OC units are candidates for encoding intensity. OI and OL units differ from OC units in that they have dynamic ranges and frequency selectivity ranges much like those of auditory nerve fibers. They differ from one another in their steady-state firing rates; OI units fire mainly at the onset of a tone. OI units also differ from OL units in that they prefer frequency sweeps in the low to high direction. Primary-like-with-notch (PLN) units also respond to tones with a well-timed first spike. They differ from onset cells in that the onset peak is not always as precise as the spontaneous rate is higher. A comparison of spontaneous firing rate and saturation firing rate of PLN units with auditory nerve fibers suggest that PLN units receive one to four auditory nerve fiber inputs. Chopper units fire in a sustained regular manner when they are excited by sound.(ABSTRACT TRUNCATED AT 400 WORDS)

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Frequency Tuning and Spontaneous Activity in the Auditory Nerve and Cochlear Nucleus Magnocellularis of the Barn Owl Tyto alba

Journal of Neurophysiology ◽

10.1152/jn.1997.77.1.364 ◽

1997 ◽

Vol 77 (1) ◽

pp. 364-377 ◽

Cited By ~ 80

Author(s):

Christine Köppl

Keyword(s):

Response Latency ◽

Cochlear Nucleus ◽

Auditory Nerve ◽

Frequency Tuning ◽

Barn Owl ◽

Nerve Fibers ◽

Spontaneous Discharge ◽

Tyto Alba ◽

Nucleus Magnocellularis ◽

Auditory Nerve Fibers

Köppl, Christine. Frequency tuning and spontaneous activity in the auditory nerve and cochlear nucleus magnocellularis of the barn owl Tyto alba. J. Neurophysiol. 77: 364–377, 1997. Single-unit recordings were obtained from the brain stem of the barn owl at the level of entrance of the auditory nerve. Auditory nerve and nucleus magnocellularis units were distinguished by physiological criteria, with the use of the response latency to clicks, the spontaneous discharge rate, and the pattern of characteristic frequencies encountered along an electrode track. The response latency to click stimulation decreased in a logarithmic fashion with increasing characteristic frequency for both auditory nerve and nucleus magnocellularis units. The average difference between these populations was 0.4–0.55 ms. The most sensitive thresholds were ∼0 dB SPL and varied little between 0.5 and 9 kHz. Frequency-threshold curves showed the simple V shape that is typical for birds, with no indication of a low-frequency tail. Frequency selectivity increased in a gradual, power-law fashion with increasing characteristic frequency. There was no reflection of the unusual and greatly expanded mapping of higher frequencies on the basilar papilla of the owl. This observation is contrary to the equal-distance hypothesis that relates frequency selectivity to the spatial respresentation in the cochlea. On the basis of spontaneous rates and/or sensitivity there was no evidence for distinct subpopulations of auditory nerve fibers, such as the well-known type I afferent response classes in mammals. On the whole, barn owl auditory nerve physiology conformed entirely to the typical patterns seen in other bird species. The only exception was a remarkably small spread of thresholds at any one frequency, this being only 10–15 dB in individual owls. Average spontaneous rate was 72.2 spikes/s in the auditory nerve and 219.4 spikes/s for nucleus magnocellularis. This large difference, together with the known properties of endbulb-of-Held synapses, suggests a convergence of ∼2–4 auditory nerve fibers onto one nucleus magnocellularis neuron. Some auditory nerve fibers as well as nucleus magnocellularis units showed a quasiperiodic spontaneous discharge with preferred intervals in the time-interval histogram. This phenomenon was observed at frequencies as high as 4.7 kHz.

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