Concurrent temporal channels for auditory processing: Oscillatory neural entrainment reveals segregation of function at different scales

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.

Dynamics of functional networks for syllable and word-level processing

“…At the neuronal level, temporal segmentation is argued to be realized through phasealignment of low-frequency (< 8 Hz; delta-theta) neuronal oscillations in auditory cortex to the slow (quasi-rhythmic) fluctuations of the speech signal at the syllabic scale ('speech tracking') (7)(8)(9)(10)(11)(12). This speech tracking possibly indicates the alignment of oscillatory excitability cycles of neuronal ensembles, which can result in perceptual constraints (13) such that speech perception is optimal at syllabic rates that fall within the range of intrinsic auditory cortex oscillations in the delta-theta range (2,14, 15 see also 16).…”

Theta and Gamma Bands Encode Acoustic Dynamics over Wide-ranging Timescales

“…Previous studies used various stimuli, such as 21 speech, music, and amplitude-or frequency-modulated sounds, and found robust neural 22 entrainment in auditory cortical areas below 10 Hz, suggesting a high temporal coding 23 capacity in the low frequency range (Luo and Poeppel, 2007 Gross et al, 2013). Previous experiments examined neural entrainment at the 32 low and high frequency ranges and demonstrated that both the neural theta and gamma 33 bands, but not the alpha band, robustly encode acoustic information (Luo and Poeppel,34 2012; Teng et al, 2017). However, two key mechanistic questions remain unresolved: 35 how are acoustic dynamics between the theta and gamma ranges encoded?…”

“…How does the human auditory system 3 encode acoustic information over wide-ranging timescales to achieve sound recognition? 4Previous work (Teng et al, 2017) demonstrated a temporal coding preference in the 5 auditory system for the theta (4 -7 Hz) and gamma (30 -45 Hz) ranges, but it remains 6 unclear how acoustic dynamics between these two ranges is encoded. Here we generated 7 artificial sounds with temporal structures over timescales from ~200 ms to ~30 ms and 8 investigated temporal coding on different timescales in the human auditory cortex.…”

“…One strategy would be to process acoustic information at every timescale equally and 9 derive the appropriate perceptual representations by integrating information across all 10 timescales without preferring any particular timescales. A different strategy would be to 11 selectively analyze slowly varying auditory attributes, carried over a longer timescale, to 12 guarantee sufficient information for perceptual analysis, and concurrently to extract fast 13 changing dynamics on a shorter timescale to preserve temporal resolution (Poeppel, 14 2003; Boemio et al, 2005;Giraud and Poeppel, 2012;Teng et al, 2017). To adjudicate 15 between these alternatives, we test how the auditory system is entrained by acoustic 16 dynamics over wide-ranging timescales.…”

“…Here, we test the temporal coding capacity of the human auditory cortex from 4 to 40 45 Hz by measuring neural entrainment. Building on earlier work (Teng et al, 2017), we 41 generated acoustic stimuli with modulation rates centered at theta (4 -7 Hz), alpha (8 -42 12 Hz), beta1 (13 -20 Hz), beta2 (21 -30 Hz) and low gamma bands (31 -45) and 43 conducted a match-to-sample task to evaluate listeners' discriminability of different 44 modulation rates. Classification and decoding analyses on the MEG data were performed 45 to test which neural frequency bands preserve high temporal coding capacity and 46 3 faithfully encode acoustic dynamics of different timescales.…”