Spatiotemporal dynamics of auditory attention synchronize with speech

Abstract

Attention plays a fundamental role in selectively processing stimuli in our environment despite distraction. Spatial attention induces increasing and decreasing power of neural alpha oscillations (8-12 Hz) in brain regions ipsilateral and contralateral to the locus of attention, respectively. This study tested whether the hemispheric lateralization of alpha power codes not just the spatial location but also the temporal structure of the stimulus. Participants attended to spoken digits presented to one ear and ignored tightly synchronized distracting digits presented to the other ear. In the magnetoencephalogram, spatial attention induced lateralization of alpha power in parietal, but notably also in auditory cortical regions. This alpha power lateralization was not maintained steadily but fluctuated in synchrony with the speech rate and lagged the time course of low-frequency (1-5 Hz) sensory synchronization. Higher amplitude of alpha power modulation at the speech rate was predictive of a listener's enhanced performance of stream-specific speech comprehension. Our findings demonstrate that alpha power lateralization is modulated in tune with the sensory input and acts as a spatiotemporal filter controlling the read-out of sensory content.attention | neural oscillations | alpha lateralization | synchronization | speech N eural oscillations are tenable biological substrates to instantiate attentional selection of sensory information from our environment (1-3). The power of alpha oscillations (8-12 Hz) is modulated by the degree of selective attention to a behaviorally relevant stimulus (4-6). Attentive focusing to one side in auditory, visual, or tactile space leads to a relative decrease in alpha power in contralateral compared with ipsilateral sensory brain regions (7-10) and governs success of selective attention, that is, of isolating one stimulus at a specific spatial location (11-13) in the context of other distracting stimuli. In speech, however, spatial selective attention alone does not suffice for successful speech comprehension given the multiple timescales (e.g., syllable and word rate) over which speech varies. Any attentional neural mechanism that respects the temporal structure of auditory sensory inputs must therefore be dynamic over time. Here, we tested the hypothesis that spatial attention to one of two concurrent speech streams induces a lateralization of alpha power that synchronizes with the speech rate over time and enhances speech comprehension.In addition to neural alpha oscillations and their role in selective attention, low-frequency neural oscillations (delta/theta band; 1-5 Hz) in sensory cortices synchronize with the temporal structure of acoustic stimuli (14, 15) such as human speech (16,17), and this synchronization supports perception (18). Furthermore, synchronization of low-frequency neural oscillations with speech is enhanced for speech streams to which participants attend (19,20). Critically, low-frequency oscillations are commonly specified as phase-locked activity (synchroni...

Lateral prefrontal cortex lesion impairs regulation of internally and externally directed attention

“…First, electrophysiological studies of selective attention have demonstrated that auditory tasks can modulate posterior alpha (Foxe et al, 1998; Wöstmann et al, 2016), as was observed in our data. Furthermore, alpha activity has been theorized as a gating mechanism of task-irrelevant information (Jensen and Mazaheri, 2010).…”

Prefrontal cortex modulates posterior alpha oscillations during top-down guided visual perception

“…Previous studies in the auditory domain had localized the origin of the low-frequency activity to sensory areas and not frontal regions (13,14,35) but were confounded by the presentation rate, which likely evoked activity (14,35,36). Given that exogenous stimulation induces a strong phase alignment (Fig.…”

“…It has been argued that lowfrequency neuronal oscillations might reflect a cortical mechanism for sensory selection, attentional allocation, and evidence updating during decision making (9,11,13,14,32). If the underlying functional brain architecture is inherently rhythmic, then we should be able to observe rhythmic patterns in behavior.…”

“…It has been suggested that slow-frequency activity in the delta range (<5 Hz) might reflect a mechanism for endogenous attentional selection and predictions (9, 10). In particular, endogenous low-frequency entrainment is thought to reflect a substrate of top-down processing (11)(12)(13)(14). Importantly, endogenous entrainment does not require rhythmicity in the input stream but reflects an intrinsic mechanism to enable predictions (15).…”

Suppression of irrelevant sounds during auditory working memory

“…There is some evidence of lateralized alpha-power increases in ACs ipsilateral to the attended ear (Müller and Weisz, 2012). However, only a few previous studies have been able to show a direct relationship between AC alpha oscillations and distracter-elicited neuronal responses (Wöstmann et al, 2016). The alpha inhibition hypothesis is contrasted by an alternative interpretation that alpha synchronization enhances stimulus maintenance at the network level (Leiberg et al, 2006; Obleser et al, 2012; Palva and Palva, 2007; Wilsch and Obleser, 2015).…”