Preferred auditory temporal processing regimes and auditory-motor synchronization

Psychonomic Bulletin & Review, Jun 2021

Decoding the rich temporal dynamics of complex sounds such as speech is constrained by the underlying neuronal-processing mechanisms. Oscillatory theories suggest the existence of one optimal perceptual performance regime at auditory stimulation rates in the delta to theta range (< 10 Hz), but reduced performance in the alpha range (10–14 Hz) is controversial. Additionally, the widely discussed motor system contribution to timing remains unclear. We measured rate discrimination thresholds between 4 and 15 Hz, and auditory-motor coupling strength was estimated through a behavioral auditory-motor synchronization task. In a Bayesian model comparison, high auditory-motor synchronizers showed a larger range of constant optimal temporal judgments than low synchronizers, with performance decreasing in the alpha range. This evidence for optimal processing in the theta range is consistent with preferred oscillatory regimes in auditory cortex that compartmentalize stimulus encoding and processing. The findings suggest, remarkably, that increased auditory-motor synchronization might extend such an optimal range towards faster rates.

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Preferred auditory temporal processing regimes and auditory-motor synchronization

Psychonomic Bulletin & Review https://doi.org/10.3758/s13423-021-01933-w BRIEF REPORT Preferred auditory temporal processing regimes and auditory-motor synchronization Pius Kern 1 & M. Florencia Assaneo 2 & Dominik Endres 3 & David Poeppel 1,4,5 & Johanna M. Rimmele 1,5 Accepted: 7 April 2021 # The Author(s) 2021 Abstract Decoding the rich temporal dynamics of complex sounds such as speech is constrained by the underlying neuronal-processing mechanisms. Oscillatory theories suggest the existence of one optimal perceptual performance regime at auditory stimulation rates in the delta to theta range (< 10 Hz), but reduced performance in the alpha range (10–14 Hz) is controversial. Additionally, the widely discussed motor system contribution to timing remains unclear. We measured rate discrimination thresholds between 4 and 15 Hz, and auditory-motor coupling strength was estimated through a behavioral auditory-motor synchronization task. In a Bayesian model comparison, high auditory-motor synchronizers showed a larger range of constant optimal temporal judgments than low synchronizers, with performance decreasing in the alpha range. This evidence for optimal processing in the theta range is consistent with preferred oscillatory regimes in auditory cortex that compartmentalize stimulus encoding and processing. The findings suggest, remarkably, that increased auditory-motor synchronization might extend such an optimal range towards faster rates. Keywords Auditory . Perceptual constraints . Temporal sensitivity . Auditory-motor synchronization Introduction Natural sounds such as speech or music contain temporal structure at multiple time scales. Particularly slow acoustic modulations in the delta-theta range (2–9 Hz) are considered crucial for speech and music processing (Ding et al., 2017; Pellegrino et al., 2011; Singh & Theunissen, 2003). Such natural statistics are arguably not accidental and co-occur with * Johanna M. Rimmele 1 Department of Neuroscience, Max-Planck-Institute for Empirical Aesthetics, Grüneburgweg 14, 60322 Frankfurt/M, Germany 2 Instituto de Neurobiologia, Universidad Nacional Autónoma de México Juriquilla, Campus UNAM 3001, 76230 Juriquilla, Qro., Mexico 3 Department of Psychology, Philipps University Marburg, Gutenbergstraße 18, 35032 Marburg, Germany 4 Department of Psychology, New York University, 6 Washington Place, New York, NY 10003, USA 5 Max Planck NYU Center for Language, Music, and Emotion, Frankfurt/M, Germany, NY, USA potential neuronal coding principles in auditory cortex (Ravignani et al., 2019; Singh & Theunissen, 2003). Support for this proposal comes from electrophysiological studies that identified endogenous oscillations in auditory cortex in the delta-theta band (Giraud et al., 2007; Keitel & Gross, 2016; Lakatos et al., 2005; Lubinus et al., 2019). By entraining to acoustic signals at these time scales, neuronal oscillations in auditory cortex might contribute to the processing of temporal information in sound (Ghitza, 2012; Giraud & Poeppel, 2012; Gross et al., 2013; McAuley & Jones, 2003; Miller & McAuley, 2005; Rimmele, Gross, et al., 2018). The optimal processing range of neuronal populations should, therefore, constrain auditory perception by facilitating auditory temporal processing within this range (Haegens & Zion Golumbic, 2018; Rimmele, Morillon, et al., 2018). Perceptual constraints, such as decreased neuronal tracking of speech and reduced speech comprehension at fast rates outside of the presumably optimal range, have been shown previously (Ahissar et al., 2001; Brungart et al., 2007; Doelling et al., 2014; Ghitza & Greenberg, 2009). Similarly, for amplitude-modulated sounds and isochronous tone sequences, reduced neuronal tracking (Teng et al., 2017; Teng & Poeppel, 2020) and reduced temporal sensitivity have been observed at stimulus rates associated with the higher alpha Psychon Bull Rev range compared to lower rates (Drake & Botte, 1993; Friberg & Sundberg, 1995; Teng et al., 2017; Viemeister, 1979). Overall, there is considerable evidence from studies on rate perception for “constant” optimal auditory temporal processing in the theta range (4–8 Hz, including lower rates in the delta range 2–4 Hz). This has typically been assessed through relative difference thresholds for rate discrimination, that is, the minimal difference between two stimulation rates necessary for discrimination normalized by the standard rate. Relative difference thresholds have been shown to be lowest and constant in the theta range, which is commonly interpreted as a zone of optimal temporal processing, referring to Weber’s law (Drake & Botte, 1993; Friberg & Sundberg, 1995; Viemeister, 1979). According to Weber’s law, the ability to distinguish stimulation rates is proportional to the frequency of the presentation rate. The absolute rate difference necessary for discrimination, thus, scales with the stimulation rate, resulting in a constant relative difference threshold. Although the temporal sensitivity has been shown to be constant at low stimulation rates (corresponding roughly to the delta-theta band, in neural terms), the onset of the decrease in temporal sensitivity is controversial. While some studies already find higher relative thresholds for rates around 8 Hz (Drake & Botte, 1993; Friberg & Sundberg, 1995; ten Hoopen et al., 1994; ten Hoopen et al., 2011), others report a threshold increase at 10 Hz (McAuley & Kidd, 1998; Michon, 1964), 12 Hz (Ehrlé & Samson, 2005; Elliott & Theunissen, 2009), 16 Hz (Nordmark, 1968; Viemeister, 1979), or even 40 Hz (Dau et al., 1997; Sheft & Yost, 1990). In these studies, typically only a coarse range of standard (modulation) rates in the upper theta and alpha range was tested. Here, we investigate whether interindividual differences in auditory-motor coupling strength might contribute to the controversial or mixed findings regarding the (onset of) sensitivity changes, using a behavioral paradigm. “Temporal predictions” from motor cortex have been shown to modulate auditory processing in studies presenting periodic tone sequences (Arnal et al., 2015; Morillon et al., 2014; Morillon & Baillet, 2017) or continuous speech (Keitel et al., 2018; Park et al., 2015), even during passive listening (Chen et al., 2008; Grahn & Rowe, 2013). Top-down effects from motor cortex seem to particularly affect auditory processing and facilitate behavior during demanding listening situations (Stokes et al., 2019; Wu et al., 2014). Interestingly, it has been proposed based on MEG findings that the right hemispheric lateralization of speech processing is reduced at more challenging fast stimulation rates (Assaneo, Rimmele, et al., 2019), whereas such lateralization might be linked to motor top-down predictions (Tang et al., 2020). Recently, Assaneo et al. (2019) developed a simple behavioral protocol to measure spontaneous auditory-motor synchronization. The synchronization of one’s own speech produ (...truncated)


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Pius Kern, M. Florencia Assaneo, Dominik Endres, David Poeppel, Johanna M. Rimmele. Preferred auditory temporal processing regimes and auditory-motor synchronization, Psychonomic Bulletin & Review, 2021, pp. 1-14, DOI: 10.3758/s13423-021-01933-w