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Prestimulus Network Integration of Auditory Cortex Predisposes Near-Threshold Perception Independently of Local Excitability.

ABSTRACT: An ever-increasing number of studies are pointing to the importance of network properties of the brain for understanding behavior such as conscious perception. However, with regards to the influence of prestimulus brain states on perception, this network perspective has rarely been taken. Our recent framework predicts that brain regions crucial for a conscious percept are coupled prior to stimulus arrival, forming pre-established pathways of information flow and influencing perceptual awareness. Using magnetoencephalography (MEG) and graph theoretical measures, we investigated auditory conscious perception in a near-threshold (NT) task and found strong support for this framework. Relevant auditory regions showed an increased prestimulus interhemispheric connectivity. The left auditory cortex was characterized by a hub-like behavior and an enhanced integration into the brain functional network prior to perceptual awareness. Right auditory regions were decoupled from non-auditory regions, presumably forming an integrated information processing unit with the left auditory cortex. In addition, we show for the first time for the auditory modality that local excitability, measured by decreased alpha power in the auditory cortex, increases prior to conscious percepts. Importantly, we were able to show that connectivity states seem to be largely independent from local excitability states in the context of a NT paradigm.

SUBMITTER: Leske S

PROVIDER: S-EPMC4635927 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:ObjectivesAge-related speech perception difficulties may be related to a decline in central auditory processing abilities, particularly in noisy or challenging environments. However, how the activation patterns related to speech stimulation in different noise situations change with normal aging has yet to be elucidated. In this study, we aimed to investigate the effects of noisy environments and aging on patterns of auditory cortical activation.DesignWe analyzed the functional near-infrared spectroscopy signals of 20 young adults, 21 middle-aged adults, and 21 elderly adults, and evaluated their cortical response patterns to speech stimuli under five different signal to noise ratios (SNRs). In addition, we analyzed the behavior score, activation intensity, oxyhemoglobin variability, and dominant hemisphere, to investigate the effects of aging and noisy environments on auditory cortical activation.ResultsActivation intensity and oxyhemoglobin variability both showed a decreasing trend with aging at an SNR of 0 dB; we also identified a strong correlation between activation intensity and age under this condition. However, we observed an inconsistent activation pattern when the SNR was 5 dB. Furthermore, our analysis revealed that the left hemisphere may be more susceptible to aging than the right hemisphere. Activation in the right hemisphere was more evident in older adults than in the left hemisphere; in contrast, younger adults showed leftward lateralization.ConclusionsOur analysis showed that with aging, auditory cortical regions gradually become inflexible in noisy environments. Furthermore, changes in cortical activation patterns with aging may be related to SNR conditions, and that understandable speech with a low SNR ratio but still understandable may induce the highest level of activation. We also found that the left hemisphere was more affected by aging than the right hemisphere in speech perception tasks; the left-sided dominance observed in younger individuals gradually shifted to the right hemisphere with aging.

Project description:Sensorineural hearing loss during early childhood alters auditory cortical evoked potentials in humans and profoundly changes auditory processing in hearing-impaired animals. Multiple mechanisms underlie the early postnatal establishment of cortical circuits, but one important set of developmental mechanisms relies on the neuromodulator serotonin (5-hydroxytryptamine [5-HT]). On the other hand, early sensory activity may also regulate the establishment of adultlike 5-HT receptor expression and function. We examined the role of 5-HT in auditory cortex by first investigating how 5-HT neurotransmission and 5-HT(2) receptors influence the intrinsic excitability of layer II/III pyramidal neurons in brain slices of primary auditory cortex (A1). A brief application of 5-HT (50 ?M) transiently and reversibly decreased firing rates, input resistance, and spike rate adaptation in normal postnatal day 12 (P12) to P21 rats. Compared with sham-operated animals, cochlear ablation increased excitability at P12-P21, but all the effects of 5-HT, except for the decrease in adaptation, were eliminated in both sham-operated and cochlear-ablated rats. At P30-P35, cochlear ablation did not increase intrinsic excitability compared with shams, but it did prevent a pronounced decrease in excitability that appeared 10 min after 5-HT application. We also tested whether the effects on excitability were mediated by 5-HT(2) receptors. In the presence of the 5-HT(2)-receptor antagonist, ketanserin, 5-HT significantly decreased excitability compared with 5-HT or ketanserin alone in both sham-operated and cochlear-ablated P12-P21 rats. However, at P30-P35, ketanserin had no effect in sham-operated and only a modest effect cochlear-ablated animals. The 5-HT(2)-specific agonist 5-methoxy-N,N-dimethyltryptamine also had no effect at P12-P21. These results suggest that 5-HT likely regulates pyramidal cell excitability via multiple receptor subtypes with opposing effects. These data also show that early sensorineural hearing loss affects the ability of 5-HT receptor activation to modulate A1 pyramidal cell excitability.

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Prestimulus Network Integration of Auditory Cortex Predisposes Near-Threshold Perception Independently of Local Excitability.

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