Frequency response areas of neurons in the mouse inferior colliculus. III. Time-domain responses: Constancy, dynamics, and precision in relation to spectral resolution, and perception in the time domain.

The auditory midbrain (central nucleus of inferior colliculus, ICC) receives multiple brainstem projections and recodes auditory information for perception in higher centers. Many neural response characteristics are represented in gradients (maps) in the three-dimensional ICC space. Map overlap suggests that neurons, depending on their ICC location, encode information in several domains simultaneously by different aspects of their responses. Thus, interdependence of coding, e.g. in spectral and temporal domains, seems to be a general ICC principle. Studies on covariation of response properties and possible impact on sound perception are, however, rare. Here, we evaluated tone-evoked single neuron activity from the mouse ICC and compared shapes of excitatory frequency-response areas (including strength and shape of inhibition within and around the excitatory area; classes I, II, III) with types of temporal response patterns and first-spike response latencies. Analyses showed covariation of sharpness of frequency tuning with constancy and precision of responding to tone onsets. Highest precision (first-spike latency jitter < 1 ms) and stable phasic responses throughout frequency-response areas were the quality mainly of class III neurons with broad frequency tuning, least influenced by inhibition. Class II neurons with narrow frequency tuning and dominating inhibitory influence were unsuitable for time domain coding with high precision. The ICC center seems specialized rather for high spectral resolution (class II presence), lateral parts for constantly precise responding to sound onsets (class III presence). Further, the variation of tone-response latencies in the frequency-response areas of individual neurons with phasic, tonic, phasic-tonic, or pauser responses gave rise to the definition of a core area, which represented a time window of about 20 ms from tone onset for tone-onset responding of the whole ICC. This time window corresponds to the roughly 20 ms shortest time interval that was found critical in several auditory perceptual tasks in humans and mice.

Tonotopy and inhibition in the midbrain inferior colliculus shape spectral resolution of sounds in neural critical bands.

Frequency resolution and spectral integration in acoustic perception is investigated psychacoustically by measuring critical bands (CBs) or equivalent quantities. In general, CB bandwidths increase with increasing sound frequency but remain constant over a large range of sound pressure levels (SPL; intensity independence). These CB properties have previously been found, on average, in responses of midbrain inferior colliculus neurons. Here, we use single-neuron recordings from the central nucleus of mouse inferior colliculus (ICC) to study neurons' excitatory and inhibitory frequency receptive fields together with neural critical bands (NCBs) measured in a narrowband noise-masking paradigm at SPLs up to 85 dB. We aim to clarify whether and how neurons with very different shapes of excitatory and inhibitory receptive fields express CB properties, whether and how inhibition contributes to set boundaries of NCBs, and where these boundaries are located in the excitatory-inhibitory receptive fields. The main results are: the above-mentioned general CB properties exist in neurons independent of the shapes of their receptive fields, that is, frequency filtering related to single tones (tuning curves) and frequency resolution related to complex sounds (NCBs) are different neuronal properties; NCB boundaries match the boundaries of an area devoid of inhibition around the characteristic frequencies in 67% of the neurons, that is, the inhibitory influence is adjusted to frequency resolution in part of the neurons; filter bandwidths of NCBs are, relative to their centre frequencies, about on average 1/3 octave wide, equaling the average frequency distance between frequency-band laminae as found in the cat ICC.

Spatial map of frequency tuning-curve shapes in the mouse inferior colliculus.

Neurons in the central nucleus of the auditory midbrain inferior colliculus divide into four classes according to the shapes of their receptive fields. Neurons of two of these classes - sharply tuned, inhibition-dominated neurons of class II, and broadly tuned neurons of class III - show systematic gradients in their abundance on isofrequency contours. Sharp tuning is most prevalent in the center, broad tuning in the periphery of the ICC. This new map of tuning-curve shape adds to the six previously described maps of neural response properties on isofrequency contours of the ICC and stresses the fact that very different sensitivities and selectivities to sound properties are combined in local clusters of collicular neurons.