Coordinated neural, behavioral, and phenomenological changes in perceptual plasticity through overtraining of synesthetic associations

Abstract

Synesthesia is associated with additional perceptual experiences, which are automatically and consistently triggered by specific inducing stimuli. Synesthesia is also accompanied by more general sensory and cortical changes, including enhanced modality-specific cortical excitability. Extensive cognitive training has been shown to generate synesthesia-like phenomenology but whether these experiences are accompanied by neurophysiological changes characteristic of synesthesia remains unknown. Addressing this question provides a unique opportunity to elucidate the neural basis of perceptual plasticity relevant to conscious experiences. Here we investigate whether extensive training of letter-color associations leads not only to synesthetic experiences, but also to changes in cortical excitability. We confirm that overtraining synesthetic associations results in synesthetic phenomenology. Stroop tasks further reveal synesthesia-like performance following training. Electroencephalography and transcranial magnetic stimulation show, respectively, enhanced visual evoked potentials (in response to untrained patterns) and lower phosphene thresholds, demonstrating specific cortical changes. An active (using letter-symbol training) and a passive control confirmed these results were due to letter-color training and not simply to repeated testing. Summarizing, we demonstrate specific cortical changes, following training-induced acquisition of synesthetic phenomenology that are characteristic of genuine synesthesia. Collectively, our data reveal dramatic plasticity in human visual perception, expressed through a coordinated set of behavioral, neurophysiological, and phenomenological changes.

Primary visual cortex excitability is not atypical in acquired synaesthesia

“…It was recently proposed that drug-induced synaesthesia results from serotonin cascades triggering elevated cortical excitability in layer V pyramidal neurons, resulting in anomalous perceptual states that are mapped onto inducers, yielding synaesthetic experiences [6]. This hypothesis is consistent with research showing selective hyperexcitability in primary visual cortex, as measured by transcranial magnetic stimulation (TMS) phosphene thresholds, but not motor (control) thresholds, in developmental synaesthesia [7] and after synaesthesia training in controls [8]. If cortical hyperexcitability plays a role in induced synaesthesias, individuals with acquired synaesthesia will display selectively lower phosphene thresholds similar to developmental synaesthetes.…”

“…We tested the prediction that a case of acquired synaesthesia would be characterized by selective hyperexcitability in primary visual cortex, as observed in developmental synaesthesia [7] and induced synaesthesia [8]. In contrast with this prediction, we found that LW, an acquired synaesthete with previously-demonstrated inducer-concurrent automaticity and consistency [3], displayed typical TMS phosphene thresholds that were within 25% of a SD of the mean phosphene threshold in controls.…”

Primary visual cortex excitability is not atypical in acquired synaesthesia

“…It was recently proposed that drug-induced synaesthesia results from serotonin cascades triggering elevated cortical excitability in layer V pyramidal neurons, resulting in anomalous perceptual states that are mapped onto inducers, yielding synaesthetic experiences . This hypothesis is consistent with research showing selective hyperexcitability in primary visual cortex, as measured by transcranial magnetic stimulation (TMS) phosphene thresholds, but not motor (control) thresholds, in developmental synaesthesia (Terhune, Song, & Cohen Kadosh, 2015) and after synaesthesia training in controls (Rothen, Schwartzman, Bor, & Seth, 2018). If cortical hyperexcitability plays a role in induced synaesthesias, individuals with acquired synaesthesia will display selectively lower phosphene thresholds similar to developmental synaesthetes.…”

“…We tested the prediction that a case of acquired synaesthesia would be characterized by selective hyperexcitability in primary visual cortex, as observed in developmental synaesthesia and induced synaesthesia (Rothen et al, 2018). In contrast with this prediction, we found that LW, an acquired synaesthete with previously-demonstrated inducer-concurrent automaticity and consistency (Yanakieva et al, 2019), displayed typical TMS phosphene thresholds that were within 25% of a SD of the mean phosphene threshold in controls.…”

How non-veridical perception drives actions in healthy humans - Evidence from Synaesthesia

“…the inducer) consistently and automatically elicits a vivid experience in another modality (i.e. the concurrent) (Grossenbacher and Lovelace, 2001;Hubbard and Ramachandran, 2005;Rothen et al, 2018;Simner and Hubbard, 2013;Ward, 2013). Importantly, individuals with synaesthesia know that the inducer is objectively 'there', while the perceived synaesthetic concurrent is lacking objective perceptual presence (i.e.…”