Enhanced Cortical Excitability in Grapheme-Color Synesthesia and Its Modulation

Abstract

Synesthesia is an unusual condition characterized by the over-binding of two or more features and the concomitant automatic and conscious experience of atypical, ancillary images or perceptions [1Rich A.N. Mattingley J.B. Anomalous perception in synaesthesia: A cognitive neuroscience perspective.Nature reviews. 2002; 3: 43-52Crossref Scopus (150) Google Scholar, 2Hubbard E.M. Ramachandran V.S. Neurocognitive mechanisms of synesthesia.Neuron. 2005; 48: 509-520Abstract Full Text Full Text PDF PubMed Scopus (279) Google Scholar, 3Bargary G. Mitchell K.J. Synaesthesia and cortical connectivity.Trends Neurosci. 2008; 31: 335-342Abstract Full Text Full Text PDF PubMed Scopus (88) Google Scholar]. Previous research suggests that synesthetes display enhanced modality-specific perceptual processing [4Barnett K.J. Foxe J.J. Molholm S. Kelly S.P. Shalgi S. Mitchell K.J. Newell F.N. Differences in early sensory-perceptual processing in synesthesia: a visual evoked potential study.Neuroimage. 2008; 43: 605-613Crossref PubMed Scopus (81) Google Scholar, 5Banissy M.J. Walsh V. Ward J. Enhanced sensory perception in synaesthesia.Exp. Brain Res. 2009; 196: 565-571Crossref PubMed Scopus (91) Google Scholar, 6Yaro C. Ward J. Searching for Shereshevskii: what is superior about the memory of synaesthetes?.Q J Exp Psychol (Hove). 2007; 60: 681-695Crossref PubMed Scopus (128) Google Scholar, 7Cohen Kadosh R. Gertner L. Terhune D.B. Exceptional abilities in the spatial representation of numbers and time: Insights from synesthesia.Neuroscientist. 2011; (in press)PubMed Google Scholar], but it remains unclear whether enhanced processing contributes to conscious awareness of color photisms. In three experiments, we investigated whether grapheme-color synesthesia is characterized by enhanced cortical excitability in primary visual cortex and the role played by this hyperexcitability in the expression of synesthesia. Using transcranial magnetic stimulation, we show that synesthetes display 3-fold lower phosphene thresholds than controls during stimulation of the primary visual cortex. We next used transcranial direct current stimulation to discriminate between two competing hypotheses of the role of hyperexcitability in the expression of synesthesia. We demonstrate that synesthesia can be selectively augmented with cathodal stimulation and attenuated with anodal stimulation of primary visual cortex. A control task revealed that the effect of the brain stimulation was specific to the experience of synesthesia. These results indicate that hyperexcitability acts as a source of noise in visual cortex that influences the availability of the neuronal signals underlying conscious awareness of synesthetic photisms.