Bottom-up versus top-down: Effective connectivity reflects individual differences in grapheme-color synesthesia
In grapheme-color synesthesia, letters elicit a color. Neural theories propose that synesthesia is due
to changes in connectivity between sensory areas. However, no studies on functional connectivity in
synesthesia have been published to date. Here, we applied psycho-physiological interactions (PPI)
and dynamic causal modeling (DCM) in fMRI to assess connectivity patterns in synesthesia. We
tested whether synesthesia is mediated by bottom-up, feedforward connections from grapheme areas
directly to perceptual color area V4, or by top-down feedback connections from the parietal cortex to
V4. We took individual differences between synesthetes into account: 'projector'synesthetes
experience their synesthetic color in a spatial location, while 'associators'only have a strong
association of the color with the grapheme.
We included 19 grapheme-color synesthetes (14 projectors, 5 associators) and located group effects
of synesthesia in left superior parietal lobule (SPL) and right color area V4. With PPI, taking SPL as a seed region, we found an increase in functional coupling with visual areas (also V4), for the
synesthesia condition. With PPI, however, we can not determine the direction of this functional
coupling. Based on the GLM results, we specified 2 DCMs to test whether a bottom-up or a top-down
model would provide a better explanation for synesthetic experiences. Bayesian Model Selection
showed that overall, neither model was much more likely than the other (exceedance probability of
0.589). However, when the models were divided according to projector or associator group, BMS
showed that the bottom-up, feedforward model had an exceedance probability of 0.98 for the
projectors: it was strongly preferred for this group. The top-down, feedback model was preferred for the associator group (exceedance probability = 0.96).
To our knowledge, we are the first to report empirical evidence of changes in functional and effective
connectivity in synesthesia. Whether bottom-up or top-down mechanisms underlie synesthetic
experiences has been a long-time debate: that different connectivity patterns can explain differential
experiences of synesthesia may greatly improve our insight in the neural mechanisms of the
phenomenon.
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