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

Abstract

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.

Midbrain auditory selectivity to natural sounds

“…Possible sources of SC auditory selectivity are intrinsic and/or afferent inhibitory circuitry (25)(26)(27). In this study, neurons in dorsal SC showed greatest selectivity to FM stimuli, and previous research suggests that inhibitory interactions may underlie the sharpening of auditory responses to FM sweeps (28)(29)(30).…”

Rodent auditory perception: Critical band limitations and plasticity

“…Tones within the frequency range of a critical band are thought to activate the same location of the basilar membrane (Schreiner et al, 2000). Critical bands contribute to the ability to discriminate sounds (Ehret and Merzenich, 1988; Schreiner and Langner, 1997; Egorova et al, 2006; Egorova and Ehret, 2008) and to detect sounds in background noise (Watson, 1963). Critical band filtering and integration are basic components of mammalian sound perception (Plomp, 1968; Scharf, 1970; Plomp, 1971; Greenwood, 1991; Roederer, 2008) and are active for any sound composed of complex frequencies, which is almost every natural sound (Scharf, 1970).…”

“…The logarithmic scale of critical band frequency dependence implicated the cochlea in determining this feature, since cochlear maps are also logarithmic (Braun, 1997). Intensity independence and linearity are not present peripherally, however, and instead are thought to be represented more centrally, perhaps by midbrain structures (Ehret and Merzenich, 1985; 1988; Egorova and Ehret, 2008). …”

“…Strikingly, the spectral distance between frequency-band laminae corresponds to one critical band; frequencies spanned by a single lamina are also separated by one critical band (Schreiner and Langner, 1997). Thus in the cat, the anatomical and physiological characteristics of the central nucleus provide a spatial tonotopy organized in terms of critical bands (Egorova and Ehret, 2008). Furthermore, spectral bandwidths, inhibition and correlated firing within the central nucleus of the inferior colliculus are all on the order of one critical band (1/3 octave) in cat (Rodriguez et al, 2010; Chen et al, 2012).…”

Conserved mechanisms of vocalization coding in mammalian and songbird auditory midbrain

“…A common principle of the relationship between excitatory and inhibitory frequency tuning is that frequencies just above and/or below excitatory frequencies often suppress a neuron’s firing, both spontaneous and sound-evoked (Yang et al, 1992; Egorova et al, 2001; Egorova and Ehret, 2008; Mayko et al, 2012; Schneider and Woolley, 2011; Schumacher et al, 2011). This sideband inhibition is functionally similar to lateral inhibition in the visual system in that it sharpens tuning.…”