Two separate inhibitory mechanisms shape the responses of dorsal cochlear nucleus type IV units to narrowband and wideband stimuli

I. Nelken, E. D. Young

Research output: Contribution to journalArticle

Abstract

1. The principal cells of the dorsal cochlear nucleus (DCN) are mostly inhibited by best frequency (BF) tones but are mostly excited by broadband noise (BBN), producing the so-called type IV response characteristic. The narrowband inhibitory responses can be explained by the inhibitory influence of interneurons with type II response characteristics. However, it is not clear that all the details of the type IV responses can be accounted for by this neural circuit. In particular, many type IV units are inhibited by band- reject noise (notch noise); type II units tend to be only weakly excited by these stimuli, if at all. In this paper we study the relationships between the narrowband, inhibitory and the wideband, excitatory regimes of the type IV responses and present the case for the existence of a second inhibitory source in DCN, called the wideband inhibitor (WBI) below. 2. Type IV units were studied using pure tones, noise bands arithmetically centered on BF, notch noise centered on BF, and BBN. We measured the rate-level function (response rate as function of stimulus level) for each stimulus. This paper is based on the responses of 28 type IV units. 3. Evidence for low-threshold inhibitory input to type IV units is derived from analysis of rate-level functions at sound levels just above threshold. Notch noise stimuli of the appropriate notch width produce inhibition at threshold in this regime. When BBN is presented, this inhibition appears to summate with excitation produced by energy in the band of noise centered on BF, resulting in BBN rate-level functions with decreased slope and maximum firing rate. A range of slopes and maximal firing rates is observed, but these variables are strongly correlated and they are negatively correlated with the strength of the inhibition produced by notch noise; this result supports the conclusion that a single inhibitory source is responsible for these effects. 4. By contrast, there is a weak (nonsignificant) positive correlation between the strength of the inhibitory effect of notch noise and the slope/maximal firing rate in response to narrowband stimuli, including BF tones. The contrast between this positive nonsignificant correlation and the significant negative correlation mentioned above suggests that more than one inhibitory effect operates; specifically, the type II input is responsible for inhibition by narrowband stimuli and a different inhibitory source, the WBI, produces inhibition by notch stimuli. 5. Several lines of evidence are given to show that type II units cannot produce the inhibition seen with notch noise stimuli. First, inhibitory effects are seen at notch widths well beyond estimates of the bandwidth of type II inhibitory inputs; second, the threshold of inhibition produced by notch noise stimuli is usually well below that of type II units for noise; and third, the firing rate of type II units decreases monotonically as the bandwidth of a narrow noise band is widened, whereas the peak response rate of type IV units can increase, decrease, or vary nonmonotonically under the same conditions. 6. Type IV units can be classified along two continua, according to their responses to narrowband stimuli on the one hand and to wideband stimuli on the other. Units differ along each continuum in the strength of inhibitory effects for narrowband or wideband stimuli, respectively. There may be an inverse relationship between the two continua, although the relationship is not statistically significant in the data of this paper. 7. A qualitative model for DCN is given that is capable of explaining the known results. In the model, type IV units receive strong inhibitory inputs from type II units that dominate for narrowband stimuli and weak inhibitory inputs from the WBI that dominate only when the excitatory input to type IV units is weakened by a noise notch. For either narrow peaks or narrow notches, type IV units give inhibitory responses. We therefore hypothesize that type IV units are detectors of sharp spectral features in acoustic stimuli. In this way they may direct the attention of higher auditory centers to those parts of the spectrum that carry interesting information about natural sounds.

Original languageEnglish (US)
Pages (from-to)2446-2462
Number of pages17
JournalJournal of neurophysiology
Volume71
Issue number6
DOIs
StatePublished - Jan 1 1994

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ASJC Scopus subject areas

  • Neuroscience(all)
  • Physiology

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