Double dissociation of spontaneous alpha-band activity and pupil-linked arousal on additive and multiplicative perceptual gain

Abstract

Perception is a probabilistic process dependent on external stimulus properties and ones internal state. However, which internal states influence perception and via what mechanisms remain debated. We studied how spontaneous alpha-band activity (8-12 Hz) and pupil fluctuations impact visual detection and confidence across stimulus contrast levels (i.e., the contrast response function or CRF). We found that weak pre-stimulus alpha power induced an "additive" shift in the CRF, whereby stimuli were reported present more frequently at all contrast levels, including contrast of zero (i.e., false alarms). Conversely, pre-stimulus pupil size had a "multiplicative" effect on detection such that stimuli occurring during large pupil states (putatively corresponding to higher arousal) were perceived more frequently as contrast increased. Signal detection modeling reveals that alpha power changes detection criteria equally across the CRF but not detection sensitivity (d) whereas pupil-linked arousal modulated sensitivity, particularly for higher contrasts. Interestingly, pupil size and alpha power were positively correlated, meaning that some of the effect of alpha on detection may be mediated by pupil fluctuations. However, pupil-independent alpha still induced an additive shift in the CRF corresponding to a criterion effect. Our data imply that weak alpha boosts detection and confidence by an additive factor, rather than by a multiplicative scaling of contrast responses, a profile which captures the effect of pupil-linked arousal. We suggest that alpha-power and arousal fluctuations have dissociable effects on behavior. Alpha reflects the baseline level of visual excitability, which can vary independent of arousal. Significance statementNearly a century ago, brain waves around 8-13 Hz (the "alpha-band") were discovered and linked to visual processing and cortical arousal. However, the precise way that alpha activity shapes perception and relates to arousal is unsettled. We recorded pupillometry and EEG while subjects detected and reported confidence for visual stimuli with varying intensity. Stimuli occurring during states of strong alpha were seen less often, regardless of intensity level, suggesting alpha exerts subtractive inhibition on perception and confidence. Pupil size (a proxy for arousal) was found to correlate with alpha yet, surprisingly, has a different effect on perception. Small pupil lowered perceptual sensitivity more as stimulus intensity increased. Our findings reveal distinct effects of alpha activity and arousal on visual perception.