Prestimulus influences on auditory perception from sensory representations and decision processes

The qualities of perception depend not only on the sensory inputs but also on the brain state before stimulus presentation. Although the collective evidence from neuroimaging studies for a relation between prestimulus state and perception is strong, the interpretation in the context of sensory computations or decision processes has remained difficult. In the auditory system, for example, previous studies have reported a wide range of effects in terms of the perceptually relevant frequency bands and state parameters (phase/power). To dissociate influences of state on earlier sensory representations and higher-level decision processes, we collected behavioral and EEG data in human participants performing two auditory discrimination tasks relying on distinct acoustic features. Using single-trial decoding, we quantified the relation between prestimulus activity, relevant sensory evidence, and choice in different task-relevant EEG components. Within auditory networks, we found that phase had no direct influence on choice, whereas power in task-specific frequency bands affected the encoding of sensory evidence. Within later-activated frontoparietal regions, theta and alpha phase had a direct influence on choice, without involving sensory evidence. These results delineate two consistent mechanisms by which prestimulus activity shapes perception. However, the timescales of the relevant neural activity depend on the specific brain regions engaged by the respective task.Sensory percepts depend not only on the environmental inputs but also on the internal brain state before stimulus presentation (1). Many studies have shown that the accuracy and speed of sensory performance change with the power and timing (phase) of rhythmic activity during a prestimulus period (2, 3). Studies in the auditory system, for example, have demonstrated that performance in detecting sounds and gaps in noise, or the discrimination of lexical stimuli, varies with the power and phase of rhythmic activity between about 1 and 12 Hz (4–9).Although the collective evidence makes a strong case that prestimulus state shapes the processing and perceptual consequences of sensory inputs, the functional interpretation of these findings in the context of specific sensory computations or higher cognitive processes has remained difficult (7, 10, 11). Electrophysiological studies in animals have described the state dependency of firing rates relative to cortical oscillations (12–15). Hence, it is tempting to interpret the reported prestimulus effects in neuroimaging studies as direct evidence for a link between the neural gain of early sensory cortices and perception. However, this is difficult for two reasons. First, previous studies have used different behavioral protocols (detection and discrimination) and stimuli (tones in silence or noise, gaps in noise, or speech), and each has implied different frequency bands and state parameters as relevant (from 1 to 12 Hz, reporting effects for phase, power, or both). Second, given the coarse spatial resolution of neuroimaging, it has often been difficult to localize the observed correlation of prestimulus state with perception to a specific neural process or brain region. Hence, it remains unclear whether previously reported prestimulus influences indeed originate from auditory cortices, possibly reflecting changes in sensory gain, or result from other high-level regions that are involved in general decision making.To disambiguate these two possibilities, we collected behavioral and EEG data during two auditory discrimination tasks relying on distinct acoustic features in the same participants. To dissect different stages of the sensory–perceptual cascade, we used single-trial decoding to separate earlier auditory from later decision-related activity (16–18). We then used linear modeling to quantify the relation between prestimulus activity, task-relevant sensory evidence, and perceptual choice within each of these components. This allowed us to directly quantify whether putative correlations of prestimulus activity with perceptual choice are mediated by an impact of prestimulus state on early auditory evidence, or arise from higher cognitive processes activated subsequent to early sensory representations.