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

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.

The chemical induction of synaesthesia

“…According to this account, disinhibited feedback from higher cortical areas -proposed to be responsible for synaesthesia -are associated with lower GABA levels in brain regions specific to the type of synaesthesia (Hubbard, Brang, & Ramachandran, 2011;Specht, 2012). The aforementioned results regarding selective cortical hyperexcitability in developmental synaesthesia (Terhune et al, 2011; and trained synaesthesia (Rothen et al, 2018) are consistent with this account, as are other data (Brauchli et al, 2018) although this hypothesis has received less attention than a serotonin hypothesis in the context of drug-induced synaesthesia. Moreover, the simplistic notion of lower GABA levels corresponding to cortical inhibition is not consistent with current insights into the complexity of the role of GABA in both cortical inhibition and excitation (Marafiga, Pasquati & Calcagnotto, in press).…”

The chemical induction of synaesthesia

“…According to this account, disinhibited feedback from higher cortical areas ‐ proposed to be responsible for synaesthesia ‐ are associated with lower GABA levels in brain regions specific to the type of synaesthesia (Hubbard et al., 2011; Specht, 2012). The aforementioned results regarding selective cortical hyperexcitability in developmental synaesthesia (Terhune et al., 2011; Terhune, Song, et al, 2015) and trained synaesthesia (Rothen et al., 2018) are consistent with this account, as are other data (Brauchli et al., 2018), although this hypothesis has received less attention than a serotonin hypothesis in the context of drug‐induced synaesthesia. Moreover, the simplistic notion of lower GABA levels corresponding to cortical inhibition is not consistent with current insights into the complexity of the role of GABA in both cortical inhibition and excitation (Marafiga et al., 2021).…”

Functional reorganization of neural networks involved in emotion regulation following trauma therapy for complex trauma disorders

“…Here, we used the in sLORETA implemented 84 Brodmann areas (BA, 42 for each hemisphere) and their corresponding centroid voxels. A similar approach has been applied in several previous studies of our lab (Binder et al, 2017; Brauchli et al, 2018; Klein et al, 2016). We used the Juelich Histological and the Harvard-Oxford cortical atlases provided by the fMRIB software (http://fsl.fmrib.ox.ac.uk/fsl/fslwiki/Atlases) and visual inspection for a more detailed description of brain regions.…”