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.

Adaptation and spectral enhancement at auditory temporal perceptual boundaries - Measurements via temporal precision of auditory brainstem responses.

In human and animal auditory perception the perceived quality of sound streams changes depending on the duration of inter-sound intervals (ISIs). Here, we studied whether adaptation and the precision of temporal coding in the auditory periphery reproduce general perceptual boundaries in the time domain near 20, 100, and 400 ms ISIs, the physiological origin of which are unknown. In four experiments, we recorded auditory brainstem responses with five wave peaks (P1 -P5) in response to acoustic models of communication calls of house mice, who perceived these calls with the mentioned boundaries. The newly introduced measure of average standard deviations of wave latencies of individual animals indicate the waves' temporal precision (latency jitter) mostly in the range of 30-100 µs, very similar to latency jitter of single neurons. Adaptation effects of response latencies and latency jitter were measured for ISIs of 10-1000 ms. Adaptation decreased with increasing ISI duration following exponential or linear (on a logarithmic scale) functions in the range of up to about 200 ms ISIs. Adaptation effects were specific for each processing level in the auditory system. The perceptual boundaries near 20-30 and 100 ms ISIs were reflected in significant adaptation of latencies together with increases of latency jitter at P2-P5 for ISIs < ~30 ms and at P5 for ISIs < ~100 ms, respectively. Adaptation effects occurred when frequencies in a sound stream were within the same critical band. Ongoing low-frequency components/formants in a sound enhanced (decrease of latencies) coding of high-frequency components/formants when the frequencies concerned different critical bands. The results are discussed in the context of coding multi-harmonic sounds and stop-consonants-vowel pairs in the auditory brainstem. Furthermore, latency data at P1 (cochlea level) offer a reasonable value for the base-to-apex cochlear travel time in the mouse (0.342 ms) that has not been determined experimentally.

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.

Corticofugal shaping of frequency tuning curves in the central nucleus of the inferior colliculus of mice.

Plasticity of the auditory cortex can be induced by conditioning or focal cortical stimulation. The latter was used here to measure how stimulation in the tonotopy of the mouse primary auditory cortex influences frequency tuning in the midbrain central nucleus of the inferior colliculus (ICC). Shapes of collicular frequency tuning curves (FTCs) were quantified before and after cortical activation by measuring best frequencies, FTC bandwidths at various sound levels, level tolerance, Q-values, steepness of low- and high-frequency slopes, and asymmetries. We show here that all of these measures were significantly changed by focal cortical activation. The changes were dependent not only on the relationship of physiological properties between the stimulated cortical neurons and recorded collicular neurons but also on the tuning curve class of the collicular neuron. Cortical activation assimilated collicular FTC shapes; sharp and broad FTCs were changed to the shapes comparable to those of auditory nerve fibers. Plasticity in the ICC was organized in a center (excitatory)-surround (inhibitory) way with regard to the stimulated location (i.e., the frequency) of cortical tonotopy. This ensures, together with the spatial gradients of distribution of collicular FTC shapes, a sharp spectral filtering at the core of collicular frequency-band laminae and an increase in frequency selectivity at the periphery of the laminae. Mechanisms of FTC plasticity were suggested to comprise both corticofugal and local ICC components of excitatory and inhibitory modulation leading to a temporary change of the balance between excitation and inhibition in the ICC.

Mapping responses to frequency sweeps and tones in the inferior colliculus of house mice.

In auditory maps of the primary auditory cortex, neural response properties are arranged in a systematic way over the cortical surface. As in the visual system, such maps may play a critical role in the representation of sounds for perception and cognition. By recording from single neurons in the central nucleus of the inferior colliculus (ICC) of the mouse, we present the first evidence for spatial organizations of parameters of frequency sweeps (sweep speed, upward/downward sweep direction) and of whole-field tone response patterns together with a map of frequency tuning curve shape. The maps of sweep speed, tone response patterns and tuning curve shape are concentrically arranged on frequency band laminae of the ICC with the representation of slow speeds, build up response types and sharp tuning mainly in the centre of a lamina, and all (including high) speeds, phasic response types and broad tuning mainly in the periphery. Representation of sweep direction shows preferences for upward sweeps medially and laterally and downward sweeps mainly centrally in the ICC (either striped or concentric map). These maps are compatible with the idea of a gradient of decreasing inhibition from the centre to the periphery of the ICC and by gradients of intrinsic neuronal properties (onset or sustained responding). The maps in the inferior colliculus compare favourably with corresponding maps in the primary auditory cortex, and we show how the maps of sweep speed and direction selectivity of the primary auditory cortex could be derived from the here-found maps of the inferior colliculus.

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.