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Alavash, M.

Publications and source records attributed to Alavash, M..

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Brain network interconnectivity dynamics explain metacognitive differences in listening behavior

Complex auditory scenes pose a challenge to attentive listening, rendering listeners slower and more uncertain in their perceptual decisions. How can we explain such behaviors from the dynamics of cortical networks that pertain to the control of listening behavior? We here follow up on the hypothesis that human adaptive perception in challenging listening situations is supported by modular reconfiguration of auditory-control networks in a sample of N=40 participants (13 males) who underwent resting-state and task functional magnetic resonance imaging (fMRI). Individual titration of a spatial selective auditory attention task maintained an average accuracy of[~] 70% but yielded considerable inter-individual differences in listeners response speed and reported confidence in their own perceptual decisions. Whole-brain network modularity increased from rest to task by reconfiguring auditory, cinguloopercular, and dorsal attention networks. Specifically, interconnectivity between the auditory network and cinguloopercular network decreased during the task relative to the resting state. Additionally, interconnectivity between the dorsal attention network and cinguloopercular network increased. These interconnectivity dynamics were predictive of individual differences in response confidence, the degree of which was more pronounced after incorrect judgments. Our findings uncover the behavioral relevance of functional crosstalk between auditory and attentional-control networks during metacognitive assessment of ones own perception in challenging listening situations and suggest two functionally dissociable cortical networked systems that shape the considerable metacognitive differences between individuals in adaptive listening behavior. Significance StatementThe ability to communicate in challenging listening situations varies not only objectively between individuals but also in terms of their subjective perceptual confidence. Using fMRI and a challenging auditory task, we demonstrate that this variability in the metacognitive aspect of listening behavior is reflected on a cortical level through the modular reconfiguration of brain networks. Importantly, task-related modulation of interconnectivity between the cinguolopercular network and each auditory and dorsal attention network can explain for individuals differences in response confidence. This suggests two dissociable cortical networked systems that shape the individual evaluation of ones own perception during listening, promising new opportunities to better understand and intervene in deficits of auditory perception such as age-related hearing loss or auditory hallucinations.

neuroscience↗

Large-scale cortical connectivity dynamics of intrinsic neural oscillations support adaptive listening behavior

In multi-talker situations individuals adapt behaviorally to the listening challenge mostly with ease, but how do brain neural networks shape this adaptation? We here establish a long-sought link between large-scale neural communications in electrophysiology and behavioral success in the control of attention in difficult listening situations. In an age-varying sample of N = 154 individuals, we find that connectivity between intrinsic neural oscillations extracted from source-reconstructed electroencephalography is regulated according to the listeners goal during a challenging dual{-} talker task. These dynamics occur as spatially organized modulations in power-envelope correlations of alpha and low-beta neural oscillations during ~2 seconds intervals most critical for listening behavior relative to resting-state baseline. First, left frontoparietal low-beta connectivity (16-24 Hz) increased during anticipation and processing of spatial-attention cue before speech presentation. Second, posterior alpha connectivity (7-11 Hz) decreased during comprehension of competing speech, particularly around target-word presentation. Connectivity dynamics of these networks were predictive of individual differences in the speed and accuracy of target-word identification, respectively, but proved unconfounded by changes in neural oscillatory activity strength. Successful adaptation to a listening challenge thus latches onto two distinct yet complementary neural systems: a beta-tuned frontoparietal network enabling the flexible adaptation to attentive listening state and an alpha-tuned posterior network supporting attention to speech. Significance StatementAttending to relevant information during listening is key to human communication. How does this adaptive behavior rely upon neural communications? We here follow up on the long-standing conjecture that, large-scale brain network dynamics constrain our successful adaptation to cognitive challenges. We provide evidence in support of two intrinsic, frequency-specific neural networks that underlie distinct behavioral aspects of successful listening: a beta-tuned frontoparietal network enabling the flexible adaptation to attentive listening state, and an alpha-tuned posterior cortical network supporting attention to speech. These findings shed light on how large-scale neural communication dynamics underlie attentive listening and open new opportunities for brain network-based intervention in hearing loss and its neurocognitive consequences.

neuroscience↗

Neural attention filters do not predict behavioral success in a large cohort of aging listeners

Successful listening crucially depends on intact attentional filters that separate relevant from irrelevant information. Research into their neurobiological implementation has focused on two potential auditory filter strategies: the lateralization of alpha power and selective neural speech tracking. However, the functional interplay of the two neural filter strategies and their potency to index listening success in an ageing population remains unclear. Using electroencephalography and a dual-talker task in a representative sample of listeners (N=155; age=39-80 years), we here demonstrate an often-missed link from single-trial behavioural outcomes back to trial-by-trial changes in neural attentional filtering. First, we observe preserved attentional-cue-driven modulation of both neural filters across chronological age and hearing levels. Second, neural filter states vary independently of one another, demonstrating complementary neurobiological solutions of spatial selective attention. Stronger neural speech tracking but not alpha lateralization boosts trial-to-trial behavioural performance. Our results highlight the translational potential of neural speech tracking as an individualized neural marker of adaptive listening behaviour.

neuroscience↗

Alpha oscillations in the human brain implement distractor suppression independent of target selection

In principle, selective attention is the net result of target selection and distractor suppression. The way in which both mechanisms are implemented neurally has remained contested. Neural oscillatory power in the alpha frequency band (~10 Hz) has been implicated in the selection of to-be-attended targets, but there is lack of empirical evidence for its involvement in the suppression of to-be-ignored distractors. Here, we use electroencephalography (EEG) recordings of N = 33 human participants (males and females) to test the pre-registered hypothesis that alpha power directly relates to distractor suppression and thus operates independently from target selection. In an auditory spatial pitch discrimination task, we modulated the location (left vs right) of either a target or a distractor tone sequence, while fixing the other in the front. When the distractor was fixed in the front, alpha power relatively decreased contralaterally to the target and increased ipsilaterally. Most importantly, when the target was fixed in the front, alpha lateralization reversed in direction for the suppression of distractors on the left versus right. These data show that target-selection-independent alpha power modulation is involved in distractor suppression. While both lateralized alpha responses for selection and for suppression proved reliable, they were uncorrelated and distractor-related alpha power emerged from more anterior, frontal cortical regions. Lending functional significance to suppression-related alpha oscillations, alpha lateralization at the individual, single-trial level was predictive of behavioral accuracy. These results fuel a renewed look at neurobiological accounts of selection-independent suppressive filtering in attention.\n\nSignificance statementAlthough well-established models of attention rest on the assumption that irrelevant sensory information is filtered out, the neural implementation of such a filter mechanism is unclear. Using an auditory attention task that decouples target selection from distractor suppression, we demonstrate that two sign-reversed lateralized alpha responses reflect target selection versus distractor suppression. Critically, these alpha responses are reliable, independent of each other, and generated in more anterior, frontal regions for suppression versus selection. Prediction of single-trial task performance from alpha modulation after stimulus onset agrees with the view that alpha modulation bears direct functional relevance as a neural implementation of attention. Results demonstrate that the neurobiological foundation of attention implies a selection-independent alpha oscillatory mechanism to suppress distraction.

neuroscience↗

Individual listening success explained by synergistic interaction of two distinct neural filters

Successful speech comprehension requires the listener to differentiate relevant from irrelevant sounds. Recent neurophysiological studies have typically addressed one of two candidate neural filter solutions for this problem: the selective neural tracking of speech in auditory cortex via the modulation of phase-locked cortical responses, or the suppression of irrelevant inputs via alpha power modulations in parieto-occipital cortex. However, empirical evidence on their relationship and direct relevance to behavior is scarce. Here, a large, age-varying sample (N=76, 39-70 years) underwent a challenging dichotic listening task. Irrespective of listeners age, measures of behavioral performance, neural speech tracking, and alpha power lateralization all increased in response to spatial-attention cues. Under most challenging conditions, individual listening success was predicted best by the synergistic interaction of these two distinct neural filter strategies. Trial-by-trial fluctuations of lateralized alpha power and ignored-speech tracking did not co-vary, which demonstrates two neurobiologically distinct filter mechanisms.

neuroscience↗

Modular reconfiguration of an auditory-control brain network supports adaptive listening behavior

Speech comprehension in noisy, multi-talker situations poses a challenge. Human listeners differ substantially in the degree to which they adapt behaviorally and can listen successfully under such circumstances. How cortical networks embody this adaptation, particularly at the individual level, is currently unknown. We here explain this adaptation from reconfiguration of brain networks for a challenging listening task (i.e., a novel linguistic variant of the Posner paradigm with concurrent speech) in an age-varying sample of N = 49 healthy adults undergoing resting-state and task fMRI. We here provide evidence for the hypothesis that more successful listeners exhibit stronger task-specific reconfiguration, hence better adaptation, of brain networks. From rest to task, brain networks become reconfigured towards more localized cortical processing characterized by higher topological segregation. This reconfiguration is dominated by the functional division of an auditory and a cingulo-opercular module, and the emergence of a conjoined auditory and ventral attention module along bilateral middle and posterior temporal cortices. Supporting our hypothesis, the degree to which modularity of this fronto-temporal auditory-control network is increased relative to resting state predicts individuals listening success in states of divided and selective attention. Our findings elucidate how fine-tuned cortical communication dynamics shape selection and comprehension of speech. Our results highlight modularity of the auditory-control network as a key organizational principle in cortical implementation of auditory spatial attention in challenging listening situations.\n\nSignificance StatementHow do brain networks shape our listening behavior? We here develop and test the hypothesis that, during challenging listening situations, intrinsic brain networks are reconfigured to adapt to the listening demands, and thus to enable successful listening. We find that, relative to a task-free resting state, networks of the listening brain show higher segregation of temporal auditory, ventral attention, and frontal control regions known to be involved in speech processing, sound localization, and effortful listening. Importantly, the relative change in modularity of this auditory-control network predicts individuals listening success. Our findings shed light on how cortical communication dynamics tune selection and comprehension of speech in challenging listening situations, and suggest modularity as the network principle of auditory spatial attention.

neuroscience↗

Dopaminergic Modulation Of Brain Signal Variability And The Functional Connectome During Cognitive Performance

Dopamine underlies important aspects of cognition, and has been suggested to boost cognitive performance. However, how dopamine modulates the large-scale cortical dynamics during cognitive performance has remained elusive. Using functional MRI during a working memory task in healthy young human listeners (N=22), we investigated the effect of levodopa (L-dopa) on two aspects of cortical dynamics, blood oxygen-level-dependent (BOLD) signal variability and the functional connectome of large-scale cortical networks. We here show that enhanced dopaminergic signaling modulates the two potentially interrelated aspects of large-scale cortical dynamics during cognitive performance, and the degree of these modulations is able to explain inter-individual differences in L-dopa-induced behavioral benefits. Relative to placebo, L-dopa increased BOLD signal variability in task-relevant temporal, inferior frontal, parietal and cingulate regions. On the connectome level, however, L-dopa diminished functional integration across temporal and cingulo-opercular regions. This hypo-integration was expressed as a reduction in network efficiency and modularity in more than two thirds of the participants and to different degrees. Hypo-integration co-occurred with relative hyper-connectivity in paracentral lobule and precuneus, as well as posterior putamen. Both, L-dopa-induced BOLD signal variability modulation and functional connectome modulations proved predictive of an individuals L-dopa-induced gain in behavioral performance, namely response speed and perceptual sensitivity. Lastly, L-dopa-induced modulations of BOLD signal variability were correlated with L-dopa-induced modulation of nodal connectivity and network efficiency. Our findings underline the role of dopamine in maintaining the dynamic range of, and communication between, cortical systems, and their explanatory power for inter-individual differences in benefits from dopamine during cognitive performance.

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Large-scale network dynamics of beta-band oscillations underlie auditory perceptual decision making

Perceptual decisions vary in the speed at which we make them. Evidence suggests that translating sensory information into behavioral decisions relies on distributed interacting neural populations, with decision speed hinging on power modulations of neural oscillations. Yet, the dependence of perceptual decisions on the large-scale network organization of coupled neural oscillations has remained elusive. We measured magnetoencephalography signals in human listeners who judged acoustic stimuli made of carefully titrated clouds of tone sweeps. These stimuli were used under two task contexts where the participants judged the overall pitch or direction of the tone sweeps. We traced the large-scale network dynamics of source-projected neural oscillations on a trial-by-trial basis using power envelope correlations and graph-theoretical network discovery. Under both tasks, faster decisions were predicted by higher segregation and lower integration of coupled beta-band (~16-28 Hz) oscillations. We also uncovered brain network states that promoted faster decisions and emerged from lower-order auditory and higher-order control brain areas. Specifically, decision speed in judging tone-sweep direction critically relied on nodal network configurations of anterior temporal, cingulate and middle frontal cortices. Our findings suggest that global network communication during perceptual decision-making is implemented in the human brain by large-scale couplings between beta-band neural oscillations.\n\nAuthor SummaryThe speed at which we make perceptual decisions varies. This translation of sensory information into behavioral decisions hinges on dynamic changes in neural oscillatory activity. However, the large-scale neural network embodiment supporting perceptual decision-making is unclear. Alavash et al. address this question by experimenting two auditory perceptual decision-making situations. Using graph-theoretical network discovery, they trace the large-scale network dynamics of coupled neural oscillations to uncover brain network states supporting the speed of auditory perceptual decisions. They find that higher network segregation of coupled beta-band oscillations supports faster auditory perceptual decisions over trials. Moreover, when auditory perceptual decisions are relatively difficult, the decision speed benefits from higher segregation of frontal cortical areas, but lower segregation and integration of auditory cortical areas.

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