Spectral-temporal processing of naturalistic sounds in monkeys and humans

Abstract

Human speech and vocalizations in animals are rich in joint spectrotemporal (S-T) modulations, wherein acoustic changes in both frequency and time are functionally related. In principle, the primate auditory system could process these complex dynamic sounds based on either an inseparable representation of S-T features, or alternatively, a separable representation. The separability hypothesis implies an independent processing of spectral and temporal modulations. We collected comparative data on the S-T hearing sensitivity in humans and macaque monkeys to a wide range of broadband dynamic spectrotemporal ripple stimuli employing a yes-no signal-detection task. Ripples were systematically varied-as a function of density (spectral modulation-frequency), velocity (temporal modulation-frequency), or modulation depth-to cover a listener's full S-T modulation sensitivity; derived from a total of 87 psychometric ripple detection curves. Audiograms were measured to control for normal hearing. Determined were hearing thresholds, reaction time distributions, and S-T modulation transfer functions (MTFs); both at the ripple detection thresholds, and at supra-threshold modulation depths. Our psychophysically derived MTFs are consistent with the hypothesis that both monkeys and humans employ analogous perceptual strategies: S-T acoustic information is primarily processed separable. Singular-value decomposition (SVD), however, revealed a small but consistent, inseparable spectral-temporal interaction. Finally, SVD analysis of the known visual spatiotemporal contrast-sensitivity function (CSF) highlights that human vision is space-time inseparable to a much larger extent than is the case for S-T sensitivity in hearing. Thus, the specificity with which the primate brain encodes natural sounds appears to be less strict than is required to adequately deal with natural images.

Spectro-temporal acoustical markers differentiate speech from song across cultures

“…Thus, neural responses are well-matched to the statistical properties of the most important aspects of both the visual 58 and auditory worlds 59 of a given species. Second, in auditory neuroscience, the STM framework has proven successful in accounting for the processing of complex environmental sounds, including vocalizations 24–28 , in several species, which fits well with our conclusions. Third, it supports the hypothesis that music and speech tend to have distinct functional roles 2,39,40 in human evolution.…”

“…Neurons in auditory regions across various species can be described in terms of their spectro-temporal receptive fields, which have been shown to constitute an efficient coding scheme for complex acoustical patterns 25–27 . Spectral and temporal modulation dimensions are largely separable in both humans and monkeys 28 . Moreover, neuronal spectro-temporal tuning functions correspond well to the most relevant acoustical features that characterize different animals’ communicative signals, including birdsong 27 , cat meows 29 , and monkey calls 30 , indicating a match between the acoustics of important sounds in the environment and the neural hardware needed to process them.…”