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Top-down signal transmission and global hyperconnectivity in auditory-visual synesthesia: Evidence from a functional EEG resting-state study


Brauchli, Christian; Elmer, Stefan; Rogenmoser, Lars; Burkhard, Anja; Jäncke, Lutz (2018). Top-down signal transmission and global hyperconnectivity in auditory-visual synesthesia: Evidence from a functional EEG resting-state study. Human Brain Mapping, 39(1):522-531.

Abstract

Auditory-visual (AV) synesthesia is a rare phenomenon in which an auditory stimulus induces a "concurrent" color sensation. Current neurophysiological models of synesthesia mainly hypothesize "hyperconnected" and "hyperactivated" brains, but differ in the directionality of signal transmission. The two-stage model proposes bottom-up signal transmission from inducer- to concurrent- to higher-order brain areas, whereas the disinhibited feedback model postulates top-down signal transmission from inducer- to higher-order- to concurrent brain areas. To test the different models of synesthesia, we estimated local current density, directed and undirected connectivity patterns in the intracranial space during 2 min of resting-state (RS) EEG in 11 AV synesthetes and 11 nonsynesthetes. AV synesthetes demonstrated increased parietal theta, alpha, and lower beta current density compared to nonsynesthetes. Furthermore, AV synesthetes were characterized by increased top-down signal transmission from the superior parietal lobe to the left color processing area V4 in the upper beta frequency band. Analyses of undirected connectivity revealed a global, synesthesia-specific hyperconnectivity in the alpha frequency band. The involvement of the superior parietal lobe even during rest is a strong indicator for its key role in AV synesthesia. By demonstrating top-down signal transmission in AV synesthetes, we provide direct support for the disinhibited feedback model of synesthesia. Finally, we suggest that synesthesia is a consequence of global hyperconnectivity.

Abstract

Auditory-visual (AV) synesthesia is a rare phenomenon in which an auditory stimulus induces a "concurrent" color sensation. Current neurophysiological models of synesthesia mainly hypothesize "hyperconnected" and "hyperactivated" brains, but differ in the directionality of signal transmission. The two-stage model proposes bottom-up signal transmission from inducer- to concurrent- to higher-order brain areas, whereas the disinhibited feedback model postulates top-down signal transmission from inducer- to higher-order- to concurrent brain areas. To test the different models of synesthesia, we estimated local current density, directed and undirected connectivity patterns in the intracranial space during 2 min of resting-state (RS) EEG in 11 AV synesthetes and 11 nonsynesthetes. AV synesthetes demonstrated increased parietal theta, alpha, and lower beta current density compared to nonsynesthetes. Furthermore, AV synesthetes were characterized by increased top-down signal transmission from the superior parietal lobe to the left color processing area V4 in the upper beta frequency band. Analyses of undirected connectivity revealed a global, synesthesia-specific hyperconnectivity in the alpha frequency band. The involvement of the superior parietal lobe even during rest is a strong indicator for its key role in AV synesthesia. By demonstrating top-down signal transmission in AV synesthetes, we provide direct support for the disinhibited feedback model of synesthesia. Finally, we suggest that synesthesia is a consequence of global hyperconnectivity.

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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:04 Faculty of Medicine > Center for Integrative Human Physiology
06 Faculty of Arts > Institute of Psychology
08 University Research Priority Programs > Dynamics of Healthy Aging
Dewey Decimal Classification:150 Psychology
Language:English
Date:January 2018
Deposited On:22 Nov 2017 15:37
Last Modified:20 Feb 2018 08:56
Publisher:Wiley-Blackwell Publishing, Inc.
ISSN:1065-9471
OA Status:Closed
Publisher DOI:https://doi.org/10.1002/hbm.23861
PubMed ID:29086468

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