Abstract
Natural sounds convey perceptually relevant information over multiple timescales, and the necessary extraction of multi-timescale information requires the auditory system to work over distinct ranges. The simplest hypothesis suggests that temporal modulations are encoded in an equivalent manner within a reasonable intermediate range. We show that the human auditory system selectively and preferentially tracks acoustic dynamics concurrently at 2 timescales corresponding to the neurophysiological theta band (4–7 Hz) and gamma band ranges (31–45 Hz) but, contrary to expectation, not at the timescale corresponding to alpha (8–12 Hz), which has also been found to be related to auditory perception. Listeners heard synthetic acoustic stimuli with temporally modulated structures at 3 timescales (approximately 190-, approximately 100-, and approximately 30-ms modulation periods) and identified the stimuli while undergoing magnetoencephalography recording. There was strong intertrial phase coherence in the theta band for stimuli of all modulation rates and in the gamma band for stimuli with corresponding modulation rates. The alpha band did not respond in a similar manner. Classification analyses also revealed that oscillatory phase reliably tracked temporal dynamics but not equivalently across rates. Finally, mutual information analyses quantifying the relation between phase and cochlear-scaled correlations also showed preferential processing in 2 distinct regimes, with the alpha range again yielding different patterns. The results support the hypothesis that the human auditory system employs (at least) a 2-timescale processing mode, in which lower and higher perceptual sampling scales are segregated by an intermediate temporal regime in the alpha band that likely reflects different underlying computations.
Highlights
Speech, music, and many natural sounds have a rich temporal structure over multiple timescales [1,2,3,4,5]; such sounds contain perceptually critical information that is encoded over short periods and, concurrently, information encoded over longer periods
That the human auditory system does not treat all rates but predominantly uses 2 nonoverlapping timescales, the slower and faster bands, to track acoustic dynamics, while the timescale corresponding to an intermediate timescale is likely reserved for other cortical operations, perhaps relating to attention and functional inhibition
Studies using amplitude-modulated sounds or click trains have shown a low-pass modulation transfer function (MTF) with a rebound above 30 Hz [40,41,42,43,44,45]. These findings demonstrate dominant auditory responses in the low frequency range and the gamma band, the cortical oscillations entrained by stimuli of corresponding frequencies of the regular modulation are not sufficient to demonstrate the importance of theta, alpha, and gamma bands in auditory processing, because the entrainment could reflect a modulation-frequency following response which may have little to do with the auditory system actively processing acoustic information in the theta and gamma bands
Summary
Music, and many natural sounds have a rich temporal structure over multiple timescales [1,2,3,4,5]; such sounds contain perceptually critical information that is encoded over short periods (e.g., the identity and exact sequence of phonemes in a spoken word) and, concurrently, information encoded over longer periods (e.g., the intonation change over a word that signals intent or affect). Successful perceptual analysis of these signals requires the auditory system to extract acoustic information at multiple scales. This presents a specific problem: how does the auditory system process different, co-occurring rates of information across multiple timescales? To derive the appropriate perceptual representations, the auditory system must extract rapidly varying information on a scale of milliseconds (approximately 10–50 ms), operating with high temporal resolution, and concurrently analyze more slowly varying signal attributes on a scale of hundreds of milliseconds (about 150–300 ms), enabling sufficient spectral resolution [6]. Previous models of temporal integration typically assuming leaky integration demonstrate timescales above 150 ms, such as loudness summation [19,20], signal detection in noise [21,22], and temporal integration at threshold [14,23,24,25,26]
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