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.

Keywords: Adaptation; Anesthesia; Auditory cortex; Auditory stream segregation; Neuron.

Fig. 1

The steady-state responses of a single neuron in the auditory cortex of anesthetized guinea pig. a) PSTH of the response to a two-tone sequence with a PR of 4 Hz and FD of 3 semitones. b) Two-tone PSTHs of the steady-state (2s onwards) response to the A (2.8 kHz) and B tones as a function of FD and PR. c) The response to the B tone decreased with increasing FD and PR. d) As the FD was increased the response to the A tone increased. e) The ratio of spike counts (B/A) shows that the B tone was suppressed to a larger extent than the A tone as the PR was increased.

Fig. 2

The response of the population of A1 neurons to alternating tone sequences. a) PSTH of the population responses for a tone sequence with a PR of 4 Hz and FD of 3 semitones. b) Two-tone PSTHs of the population of neurons for all conditions tested, including the result of only using those units that significantly locked at 16 Hz (second to bottom row) and the response to tones presented in isolation at the B frequencies (bottom row).

Fig. 3

A) Median and interquartile spike counts across the population in response to each A tone. Asterisks indicate when the population is significantly driven (p < .05). The grey dashed line illustrates increase in A-tone response with FD for 8 Hz. B) Spike counts in response to the B tones. Open bars indicate the responses to isolated tones at the B tone frequencies. C) The B/A spike count ratios as a function of FD and PR. Dashed grey line illustrates the non-monotonicity of ratio as function of PR. D) The proportion of units that exhibited significant locking to the tones in the sequence decreased markedly at faster PRs.

Fig. 4

Responses to AB tone sequences are governed by the tuning of the neuron. a) Two-tone PSTHs display the characteristic pattern exhibited by a unit with the A tone (4.8 kHz, MU) set at BF. Right hand panel shows the spike count in response to A and B tones in the sequence and also to isolated tones (black). b) In this unit, the B tone dominates the response at a 3 semitone difference, however the A tone (1.6 kHz, SU) still dominates at larger semitone differences. c) This neuron responds maximally to the B tone with a 6 semitone FD; there is little response to the A tone (1 kHz, MU) at any FD, despite a robust response to isolated tones. d) In this example, the neuron CF is at frequencies beyond the range of tone frequencies used and there is no response to the A tone (0.7 kHz, MU) in the sequence.

Fig. 5

Variable rates and extents of adaptation were observed across the different PR and FD conditions. a) Mean spike count for each A and B tone fitted with decaying exponential functions for the 8 Hz conditions. SEMs are indicated by shaded patches around the crosses. b) Exponential fits for both the A and B tones for PRs from 4 to 16 Hz and semitone differences of 3–12 semitones. c) The rate of adaptation (R: see methods) for both the A and B tone fits increased as the PR was increased. However, the ratio of R shows that the B tone tended to adapt quicker than the A tone at faster PRs.

Fig. 6

The SDT model. A. Population spike count distributions, tone by tone for A and B tones, for the first 0–2s of the tone sequences when PR is 8 Hz. The grey shaded horizontal bar shows the average spike count distribution in equivalent time windows when no tone is played. B. Distributions of decisions made as to whether tones belong to the same stream (green) or are segregated (2 streams; pink or blue), as a function of position in time during the sequence, and the applied decision criterion. The vertical axis indicates the criterion value or ‘threshold’ population spike count for considering a tone present. Coloured/shaded areas indicate when either or both tones produce more spikes than the criterion 75% or more of the time. White areas correspond to times and criterion when neither tone is detected, or false alarms in the absence of tones exceeds 25%, indicating tones are not distinguishable from background activity. C. Prediction of the probability of the tones being perceived as segregated, as a function of time (0–6 s), for all FDs and PRs of 4 Hz (left), 8 Hz (middle) and 12 Hz (right). This is calculated as the proportion of the criterion range (in Fig. 6B) over which the model predicts two streams will be perceived. Jagged lines at high PRs (12 Hz) indicate detection of either tone is unreliable so the chance of detecting 1 or both fluctuates from tone to tone. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 7

Overall predicted probability of perceiving two streams across all stimulus conditions, for the period 4–8s after the start of the sequence. Thick lines indicate the coherence (green/dark grey) and segregation (pink/light grey) boundaries seen in human psychophysics, with the region in between being the ambiguous region. The probability is calculated in the same manner as Fig. 6C–E. Thus it represents the proportion of criterion for which only 1 tone is reliably detected (compared with all criterion at which one or more tones are detectable). Crossed squares indicate conditions where the A tone was not reliably distinguished from the background at any criterion. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)