Nonlinear Spectrotemporal Sound Analysis by Neurons in the Auditory Midbrain

Abstract

The auditory system of humans and animals must process information from sounds that dynamically vary along multiple stimulus dimensions, including time, frequency, and intensity. Therefore, to understand neuronal mechanisms underlying acoustic processing in the central auditory pathway, it is essential to characterize how spectral and temporal acoustic dimensions are jointly processed by the brain. We use acoustic signals with a structurally rich time-varying spectrum to study linear and nonlinear spectrotemporal interactions in the central nucleus of the inferior colliculus (ICC). Our stimuli, the dynamic moving ripple (DMR) and ripple noise (RN), allow us to systematically characterize response attributes with the spectrotemporal receptive field (STRF) methods to a rich and dynamic stimulus ensemble. Theoretically, we expect that STRFs derived with DMR and RN would be identical for a linear integrating neuron, and we find that approximately 60% of ICC neurons meet this basic requirement. We find that the remaining neurons are distinctly nonlinear; these could either respond selectively to DMR or produce no STRFs despite selective activation to spectrotemporal acoustic attributes. Our findings delineate rules for spectrotemporal integration in the ICC that cannot be accounted for by conventional linear-energy integration models.

Hierarchical computation in the canonical auditory cortical circuit

“…Dynamic moving ripple noise stimuli were presented that contained temporal and spectral modulations known to drive cortical cells (15,17). Modulation parameters were randomly varied, and STRFs were calculated from the responses.…”

“…Laminar differences were also evident in the degree of feature selectivity, which expresses how similar a stimulus has to be to the averaged preevent ensemble to produce an action potential (17). Neurons were most feature selective in granular layers, i.e., deviations between stimulus and STA pattern are not well tolerated (Fig.…”

Stimulus-invariant processing and spectrotemporal reverse correlation in primary auditory cortex

“…Such processing is already under study in auditory neurophysiology (Kowalski et al, 1996a,b;Depireux et al, 2001;Miller et al, 2001Miller et al, , 2002Escabí and Schreiner, 2002) and psychoacoustics (Chi et al, 1999), and is also being investigated for various signal-processing tasks, including audio coding (Atlas and Shamma, 2003;Klein et al, 2003) and speech recognition (Hermmansky, 1999;Nadeu et al, 2001;Kleinschmidt and Gelbart, 2002;Kleinschmidt, 2002).…”

“…For example, Gaussian broad-band noise, the "ideal" stimulus for reverse-correlation, is often ineffective when applied to central auditory neurons (but see (Keller and Takahashi, 2000)). Meanwhile, a range of other stimuli and associated techniques have been auditioned, modulated broad-band noise (Miller et al, 2002;Escabí and Schreiner, 2002), random sequences of tones or chords (Aertsen and Johannesma, 1981a;Epping and Eggermont, 1985;Schafer et al, 1992;deCharms et al, 1998;Theunissen et al, 2000;Rutkowski et al, 2002), and natural stimuli (Aertsen and Johannesma, 1981a;Yeshurun et al, 1987;Schafer et al, 1992;Theunissen et al, 2000;Sen et al, 2001). While it is sometimes implied that the auditory system processes different stimuli differently, it has not been made clear, because of the lack of vocabulary, to what extent different stimulation methods should yield different results.…”

“…Each spectrotemporal modulation frequency is the conjunction of a spectral and a temporal modulation frequency; the higher the spectral modulation frequency, the sharper the spectral feature (e.g., sharp peaks or edges in the spectrum), and the higher the temporal modulation frequency, the more abruptly that feature changes in time. As a population, the strongest phase-locked response in central auditory neurons occurs over a select range of low spectral and temporal modulation frequencies (Rees and Moller, 1983;Shamma et al, 1995;Schreiner and Calhoun, 1995;Kowalski et al, 1996a;Depireux et al, 2001;Sen et al, 2001;Miller et al, 2002;Escabí and Schreiner, 2002). Not surprisingly, the most fruitful stimuli have had spectrotemporal modulation frequencies concentrated within this range.…”