Consistent pre-stimulus influences on auditory perception across the lifespan.

As we get older, perception in cluttered environments becomes increasingly difficult as a result of changes in peripheral and central neural processes. Given the aging society, it is important to understand the neural mechanisms constraining perception in the elderly. In young participants, the state of rhythmic brain activity prior to a stimulus has been shown to modulate the neural encoding and perceptual impact of this stimulus - yet it remains unclear whether, and if so, how, the perceptual relevance of pre-stimulus activity changes with age. Using the auditory system as a model, we recorded EEG activity during a frequency discrimination task from younger and older human listeners. By combining single-trial EEG decoding with linear modelling we demonstrate consistent statistical relations between pre-stimulus power and the encoding of sensory evidence in short-latency EEG components, and more variable relations between pre-stimulus phase and subjects' decisions in longer-latency components. At the same time, we observed a significant slowing of auditory evoked responses and a flattening of the overall EEG frequency spectrum in the older listeners. Our results point to mechanistically consistent relations between rhythmic brain activity and sensory encoding that emerge despite changes in neural response latencies and the relative amplitude of rhythmic brain activity with age.

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.

Sounds facilitate visual motion discrimination via the enhancement of late occipital visual representations.

Sensory discriminations, such as judgements about visual motion, often benefit from multisensory evidence. Despite many reports of enhanced brain activity during multisensory conditions, it remains unclear which dynamic processes implement the multisensory benefit for an upcoming decision in the human brain. Specifically, it remains difficult to attribute perceptual benefits to specific processes, such as early sensory encoding, the transformation of sensory representations into a motor response, or to more unspecific processes such as attention. We combined an audio-visual motion discrimination task with the single-trial mapping of dynamic sensory representations in EEG activity to localize when and where multisensory congruency facilitates perceptual accuracy. Our results show that a congruent sound facilitates the encoding of motion direction in occipital sensory - as opposed to parieto-frontal - cortices, and facilitates later - as opposed to early (i.e. below 100ms) - sensory activations. This multisensory enhancement was visible as an earlier rise of motion-sensitive activity in middle-occipital regions about 350ms from stimulus onset, which reflected the better discriminability of motion direction from brain activity and correlated with the perceptual benefit provided by congruent multisensory information. This supports a hierarchical model of multisensory integration in which the enhancement of relevant sensory cortical representations is transformed into a more accurate choice.

Neural correlates of multisensory reliability and perceptual weights emerge at early latencies during audio-visual integration.

To make accurate perceptual estimates, observers must take the reliability of sensory information into account. Despite many behavioural studies showing that subjects weight individual sensory cues in proportion to their reliabilities, it is still unclear when during a trial neuronal responses are modulated by the reliability of sensory information or when they reflect the perceptual weights attributed to each sensory input. We investigated these questions using a combination of psychophysics, EEG-based neuroimaging and single-trial decoding. Our results show that the weighted integration of sensory information in the brain is a dynamic process; effects of sensory reliability on task-relevant EEG components were evident 84 ms after stimulus onset, while neural correlates of perceptual weights emerged 120 ms after stimulus onset. These neural processes had different underlying sources, arising from sensory and parietal regions, respectively. Together these results reveal the temporal dynamics of perceptual and neural audio-visual integration and support the notion of temporally early and functionally specific multisensory processes in the brain.

Irregular Speech Rate Dissociates Auditory Cortical Entrainment, Evoked Responses, and Frontal Alpha.

The entrainment of slow rhythmic auditory cortical activity to the temporal regularities in speech is considered to be a central mechanism underlying auditory perception. Previous work has shown that entrainment is reduced when the quality of the acoustic input is degraded, but has also linked rhythmic activity at similar time scales to the encoding of temporal expectations. To understand these bottom-up and top-down contributions to rhythmic entrainment, we manipulated the temporal predictive structure of speech by parametrically altering the distribution of pauses between syllables or words, thereby rendering the local speech rate irregular while preserving intelligibility and the envelope fluctuations of the acoustic signal. Recording EEG activity in human participants, we found that this manipulation did not alter neural processes reflecting the encoding of individual sound transients, such as evoked potentials. However, the manipulation significantly reduced the fidelity of auditory delta (but not theta) band entrainment to the speech envelope. It also reduced left frontal alpha power and this alpha reduction was predictive of the reduced delta entrainment across participants. Our results show that rhythmic auditory entrainment in delta and theta bands reflect functionally distinct processes. Furthermore, they reveal that delta entrainment is under top-down control and likely reflects prefrontal processes that are sensitive to acoustical regularities rather than the bottom-up encoding of acoustic features. SIGNIFICANCE STATEMENT: The entrainment of rhythmic auditory cortical activity to the speech envelope is considered to be critical for hearing. Previous work has proposed divergent views in which entrainment reflects either early evoked responses related to sound encoding or high-level processes related to expectation or cognitive selection. Using a manipulation of speech rate, we dissociated auditory entrainment at different time scales. Specifically, our results suggest that delta entrainment is controlled by frontal alpha mechanisms and thus support the notion that rhythmic auditory cortical entrainment is shaped by top-down mechanisms.

Shared Physiological Correlates of Multisensory and Expectation-Based Facilitation.

Perceptual performance in a visual task can be enhanced by simultaneous multisensory information, but can also be enhanced by a symbolic or amodal cue inducing a specific expectation. That similar benefits can arise from multisensory information and within-modality expectation raises the question of whether the underlying neurophysiological processes are the same or distinct. We investigated this by comparing the influence of the following three types of auxiliary probabilistic cues on visual motion discrimination in humans: (1) acoustic motion, (2) a premotion visual symbolic cue, and (3) a postmotion symbolic cue. Using multivariate analysis of the EEG data, we show that both the multisensory and preceding visual symbolic cue enhance the encoding of visual motion direction as reflected by cerebral activity arising from occipital regions ∼200-400 ms post-stimulus onset. This suggests a common or overlapping physiological correlate of cross-modal and intramodal auxiliary information, pointing to a neural mechanism susceptive to both multisensory and more abstract probabilistic cues. We also asked how prestimulus activity shapes the cue-stimulus combination and found a differential influence on the cross-modal and intramodal combination: while alpha power modulated the relative weight of visual motion and the acoustic cue, it did not modulate the behavioral influence of a visual symbolic cue, pointing to differences in how prestimulus activity shapes the combination of multisensory and abstract cues with task-relevant information.

Trial by trial dependencies in multisensory perception and their correlates in dynamic brain activity.

A well-known effect in multisensory perception is that congruent information received by different senses usually leads to faster and more accurate responses. Less well understood are trial-by-trial interactions, whereby the multisensory composition of stimuli experienced during previous trials shapes performance during a subsequent trial. We here exploit the analogy of multisensory paradigms with classical flanker tasks to investigate the neural correlates underlying trial-by-trial interactions of multisensory congruency. Studying an audio-visual motion task, we demonstrate that congruency benefits for accuracy and reaction times are reduced following an audio-visual incongruent compared to a congruent preceding trial. Using single trial analysis of motion-sensitive EEG components we then localize current-trial and serial interaction effects within distinct brain regions: while the multisensory congruency experienced during the current trial influences the encoding of task-relevant information in sensory-specific brain regions, the serial interaction arises from task-relevant processes within the inferior frontal lobe. These results highlight parallels between multisensory paradigms and classical flanker tasks and demonstrate a role of amodal association cortices in shaping perception based on the history of multisensory congruency.