Attention-driven auditory cortex short-term plasticity helps segregate relevant sounds from noise

Abstract

How can we concentrate on relevant sounds in noisy environments? A "gain model" suggests that auditory attention simply amplifies relevant and suppresses irrelevant afferent inputs. However, it is unclear whether this suffices when attended and ignored features overlap to stimulate the same neuronal receptive fields. A "tuning model" suggests that, in addition to gain, attention modulates feature selectivity of auditory neurons. We recorded magnetoencephalography, EEG, and functional MRI (fMRI) while subjects attended to tones delivered to one ear and ignored opposite-ear inputs. The attended ear was switched every 30 s to quantify how quickly the effects evolve. To produce overlapping inputs, the tones were presented alone vs. during white-noise masking notch-filtered ±1/6 octaves around the tone center frequencies. Amplitude modulation (39 vs. 41 Hz in opposite ears) was applied for "frequency tagging" of attention effects on maskers. Noise masking reduced early (50-150 ms; N1) auditory responses to unattended tones. In support of the tuning model, selective attention canceled out this attenuating effect but did not modulate the gain of 50-150 ms activity to nonmasked tones or steady-state responses to the maskers themselves. These tuning effects originated at nonprimary auditory cortices, purportedly occupied by neurons that, without attention, have wider frequency tuning than ±1/6 octaves. The attentional tuning evolved rapidly, during the first few seconds after attention switching, and correlated with behavioral discrimination performance. In conclusion, a simple gain model alone cannot explain auditory selective attention. In nonprimary auditory cortices, attention-driven short-term plasticity retunes neurons to segregate relevant sounds from noise.

Fig. 1.

Task design and hypotheses. (A) Auditory selective attention task. Two asynchronous standard-tone streams (0.5 vs. 2 kHz) were presented to different ears, in separate blocks with or without notch-filtered white-noise masking. Subjects were instructed to press a button upon hearing a target stimulus (“difficult” 1/24- or “easy” 1/12-octave frequency increase) in the designated ear and to ignore the opposite-ear stimulation. To distinguish short-term “tuning” effects from longer-term learning, the attended ear was shifted after every 30 s, as signaled by a buzzer sound in the designated ear (during fMRI, attention was shifted after every other TR). (B) Tuning hypothesis: Notch-filtered noise results in adaptation/lateral inhibition that decreases response amplitudes. Left: Attention increases single neurons’ selectivity to the attended frequency. In the presence of notch-filtered masking noise (Upper), the response of the single neuron is attenuated due to adaptation in the ignored condition but not in the attended condition. Center: Consequently, in the attended condition, a smaller proportion of neurons responding to the relevant tone frequency become stimulated, and subsequently adapted, by the masker. In contrast, in the ignored condition, the number of neurons responding to the relevant tone is reduced in the presence of the masking noise. Right: In MEG/EEG, the attentional tuning effect is observable as a release from adaptation that counterbalances the attenuating effects of noise masking on N1 activity that is evidenced during the ignored condition. (According to an alternative “gain” hypothesis, attention would significantly increase N1 amplitude also without masking.)

Fig. 2.

Event-related MEG responses. (A) MEG signals to attended and ignored sounds from sensors directly above the left and right auditory cortices, averaged across eight subjects. (B) Average MEG activity 50–150 ms after stimulus in six gradiometer pairs encompassing the left and the right temporal areas. The vector sums of signals of each gradiometer pair were averaged and normalized within each hemisphere and then pooled across hemispheres for the display (Table S1 shows mean amplitudes within each hemisphere). Taken together (A and B), these data show a significant masking-related reduction of early auditory cortex N1 activity (50–150 ms after stimulus) to unattended tones. Selective attention canceled out this attenuation effect, as shown by the significant enhancement of N1 activity that was observable only in the masking condition. *P < 0.05; error bars represent SEM. See also Fig. S1.

Fig. 3.

MEG/EEG/fMRI estimates of attentional modulation of auditory cortex activation. The MNE was computed for the difference in the response to attended vs. ignored right-ear tones, with and without masking. Attention-driven inward currents are shown at locations where the corresponding group t statistics were significant at FDR < 0.05. The earlier effect (50–150 ms; approximately N1 peak latency) was only present during masking, which supports our hypothesis that attention enhances feature tuning in auditory cortex. The later “processing negativity” effect (150–350 ms) was not modulated by masking and could reflect more sustained and nonspecific attentional feedback to the auditory cortex. The effects were similar in the right auditory cortex (Fig. S2). PT, planum temporale; HG, Heschl's gyrus; STG, superior temporal gyrus; PP, planum polare.

Fig. 4.

MEG/EEG/fMRI ROI analysis of attentional enhancement of activations in the left and right auditory cortices 50–150 ms after stimulus. The attention effect was significantly stronger with noise masking than without it. Error bars indicate SEM between subjects. **P = 0.01.

Fig. 5.

Correlations between attentional modulation of auditory cortex activation and behavioral discrimination of target tones (as measured from the difference in the hit rate for easier vs. difficult targets delivered to the right ear). Only statistically significant MEG/EEG/fMRI activations were considered in this analysis. The clearest behavioral correlations were observed during noise masking 50–150 ms after stimulus: improved accuracy of target discrimination correlated with the attentional tuning (release from adaptation caused by masking).