Stream segregation in the anesthetized auditory cortex

Abstract

Auditory stream segregation describes the way that sounds are perceptually segregated into groups or streams on the basis of perceptual attributes such as pitch or spectral content. For sequences of pure tones, segregation depends on the tones' proximity in frequency and time. In the auditory cortex (and elsewhere) responses to sequences of tones are dependent on stimulus conditions in a similar way to the perception of these stimuli. However, although highly dependent on stimulus conditions, perception is also clearly influenced by factors unrelated to the stimulus, such as attention. Exactly how ‘bottom-up’ sensory processes and non-sensory ‘top-down’ influences interact is still not clear.Here, we recorded responses to alternating tones (ABAB …) of varying frequency difference (FD) and rate of presentation (PR) in the auditory cortex of anesthetized guinea-pigs. These data complement previous studies, in that top-down processing resulting from conscious perception should be absent or at least considerably attenuated.Under anesthesia, the responses of cortical neurons to the tone sequences adapted rapidly, in a manner sensitive to both the FD and PR of the sequences. While the responses to tones at frequencies more distant from neuron best frequencies (BFs) decreased as the FD increased, the responses to tones near to BF increased, consistent with a release from adaptation, or forward suppression. Increases in PR resulted in reductions in responses to all tones, but the reduction was greater for tones further from BF. Although asymptotically adapted responses to tones showed behavior that was qualitatively consistent with perceptual stream segregation, responses reached asymptote within 2 s, and responses to all tones were very weak at high PRs (>12 tones per second).A signal-detection model, driven by the cortical population response, made decisions that were dependent on both FD and PR in ways consistent with perceptual stream segregation. This included showing a range of conditions over which decisions could be made either in favor of perceptual integration or segregation, depending on the model ‘decision criterion’. However, the rate of ‘build-up’ was more rapid than seen perceptually, and at high PR responses to tones were sometimes so weak as to be undetectable by the model.Under anesthesia, adaptation occurs rapidly, and at high PRs tones are generally poorly represented, which compromises the interpretation of the experiment. However, within these limitations, these results complement experiments in awake animals and humans. They generally support the hypothesis that ‘bottom-up’ sensory processing plays a major role in perceptual organization, and that processes underlying stream segregation are active in the absence of attention.

Neuronal Correlates of Auditory Streaming in Monkey Auditory Cortex for Tone Sequences without Spectral Differences

“…We found that the similarity of neuronal responses corresponds well to the frequencies with which humans perceive sequences of tone complexes to consist of either one or two auditory streams (Roberts et al, 2002 ). The present study therefore corroborates and extends previous reports also showing correspondences between neuronal activity in the primary auditory cortex and the perceptual grouping of sequences of sounds that differ in frequency (Fishman et al, 2001 , 2004 , 2017 ; Kanwal et al, 2003 ; Noda et al, 2013 ; Farley and Noreña, 2015 ; Scholes et al, 2015 ) or source location (Middlebrooks and Bremen, 2013 ; Yao et al, 2015 ).…”

“…For ambiguous sound sequences, which are perceived either as one or two streams, there is partial overlap of the activated neurons. This neuronal correlate was described in the primary auditory cortex in the two cited studies and in other studies for tones differing only in frequency (Kanwal et al, 2003 ; Scholes et al, 2015 ) or only in source location (Middlebrooks and Bremen, 2013 ; Yao et al, 2015 ). It has also been identified in the auditory brainstem (Pressnitzer et al, 2008 ).…”

“…Virtually all the primary auditory cortex studies cited above found a correlate of auditory streaming in the strength of neuronal activation (Fishman et al, 2001 , 2004 ; Kanwal et al, 2003 ; Middlebrooks and Bremen, 2013 ; Noda et al, 2013 ; Farley and Noreña, 2015 ; Scholes et al, 2015 ; Yao et al, 2015 ). Consistent with these findings, the present study shows a correspondence between auditory streaming and the rate response (the mean firing rate within a fixed interval relative to the tone presentation).…”

Neuronal correlates of auditory streaming in the auditory cortex of behaving monkeys

“…Stream integration was promoted in the AV3 condition, in which every third tone was synchronized with a flash. Thus, our approach potentially has a confound similar to that of all previous studies on neurophysiological correlates of auditory streaming in mammals, in which different auditory percepts were induced with different (auditory) stimulations (Fishman et al., ; Kanwal, Medvedev, & Micheyl, ; Micheyl, Tian, Carlyon, & Rauschecker, ; Scholes, Palmer, & Sumner, ). Indeed, in contrast to the traditional view of primary auditory cortex as a unisensory brain structure (Brosch & Scheich, ), there is converging evidence in different species that some auditory cortical neurons respond to visual stimuli (Bizley, Nodal, Bajo, Nelken, & King, ; Brosch et al., , ; Li et al., ), or that their auditory responses are modulated by concurrent visual stimuli (Bizley et al., ; Falchier, Clavagnier, Barone, & Kennedy, ; Kayser, Petkov, & Logothetis, ; Schroeder & Foxe, ; Schroeder & Lakatos, ).…”

“…Effects may also be obscured by the choice of the auditory stimuli. Previous studies set one of the repeating tones to the best frequency of the auditory cortex neurons under consideration and then varied the frequency of the other tone to determine response ratios (Fishman, Kim, & Steinschneider, ; Fishman et al., ; Kanwal et al., ; Scholes et al., ). In contrast, in most neurons of our study, the tones were not at the best frequency; mostly one of the two tones was above and the other was below the best frequency and both tones had a similar separation from the best frequency.…”