Streaming of Repeated Noise in Primary and Secondary Fields of Auditory Cortex

Abstract

Statistical regularities in natural sounds facilitate the perceptual segregation of auditory sources, or streams. Repetition is one cue that drives stream segregation in humans, but the neural basis of this perceptual phenomenon remains unknown. We demonstrated a similar perceptual ability in animals by training ferrets of both sexes to detect a stream of repeating noise samples (foreground) embedded in a stream of random samples (background). During passive listening, we recorded neural activity in primary auditory cortex (A1) and secondary auditory cortex (posterior ectosylvian gyrus, PEG). We used two context-dependent encoding models to test for evidence of streaming of the repeating stimulus. The first was based on average evoked activity per noise sample and the second on the spectro-temporal receptive field. Both approaches tested whether differences in neural responses to repeating versus random stimuli were better modeled by scaling the response to both streams equally (global gain) or by separately scaling the response to the foreground versus background stream (stream-specific gain). Consistent with previous observations of adaptation, we found an overall reduction in global gain when the stimulus began to repeat. However, when we measured stream-specific changes in gain, responses to the foreground were enhanced relative to the background. This enhancement was stronger in PEG than A1. In A1, enhancement was strongest in units with low sparseness (i.e., broad sensory tuning) and with tuning selective for the repeated sample. Enhancement of responses to the foreground relative to the background provides evidence for stream segregation that emerges in A1 and is refined in PEG.

Neuronal figure-ground responses in primate primary auditory cortex

“…A1 sites detected temporally coherent frequency elements that had no simple mathematical relationship to each other (Figures 3C-3E, 4A, and 4E), unlike previous work that identified A1 responses to harmonically related elements (Feng and Wang, 2017). These results accord with recent findings showing that perceptual organization depends on the primary auditory cortex for the segregation of repeated noise stimuli (Saderi et al, 2020) and synchronous tone sequences (Lu et al, 2017). In addition, dynamic causal modeling has demonstrated disinhibition of the primary core during the presentation of auditory figures .…”

Corticothalamic projections deliver enhanced responses to medial geniculate body as a function of the temporal reliability of the stimulus

“…2019 a , b ; Saderi et al . 2020). Electrophysiological and fMRI studies suggest a role for repetition suppression/adaptation to repeating stimuli in support of image sharpening and perceptual priming (Gross et al .…”

“…Prediction error is a mechanism to strengthen the internal representation of less temporally distinct/ambiguous stimuli which may lead to generation of a better prediction upon the next repetition (Rao & Ballard, 1999). Studies have suggested increased use of predictive coding in order to cope with less distinct stimuli or ageing accompanied by a less temporally distinct/lower signal-to-noise ratio (Heinemann et al 2011;Peelle & Wingfield, 2016;Presacco et al 2019;Price et al 2019;Bidelman et al 2019a,b;Saderi et al 2020). Electrophysiological and fMRI studies suggest a role for repetition suppression/adaptation to repeating stimuli in support of image sharpening and perceptual priming (Gross et al 1967;Dolan et al 1997;James et al 2000;Grill-Spector et al 2006;Näätänen et al 2007).…”

Hearing in Complex Environments: Auditory Gain Control, Attention, and Hearing Loss

“…Indeed, neurons in non-primary ACx exhibit greater invariance in encoding acoustically distorted communicative signals compared to neurons in primary ACx ( Carruthers et al, 2013 , 2015 ). Similarly, dual recordings from primary and secondary ACx in ferrets trained to detect streams of repeated noise samples embedded in a stream of random background samples found that stream-specific gain enhancement was stronger in secondary cortical areas compared to primary ACx ( Saderi et al, 2020 ). Importantly, categorical sound representations in higher-order cortical regions are often behaviorally-gated, adaptively assuming different states or filter properties depending upon the demands of the ongoing task.…”