PI: Berit Brogaard
1. Theoretical background
Unconscious vision has been found in patients with lesions to striate (V1) cortex (Weiskrantz et al. 1995, Weiskrantz 1998, Weiskrantz 2009). This sort of residual sight in patients with V1 lesions is also known as ‘blindsight’. Owing to functional pre-striate brain regions (the retina and the dorsal lateral geniculate nucleus), people with blindsight can detect the location, direction and color of stimuli presented to them in their blind field, but blindsight is not associated with a distinctly visual phenomenology (Stoerig and Cowey 1992). One explanation of the lack of visual awareness in blindsight is that reentrant information processing in V1 is required for visual awareness. In a recent TMS study it was shown that color experience could be induced with bilateral magnetic stimulation but the color phosphene depended exclusively on the stimulus to which the sighted hemifield had been adapted (silvanto et al. 2007, Silvanto et al. 2008). One hypothesis is that color experience arose because of magnetically induced interhemispheric interaction, indicating that striate cortex is required for color experience.
Unconscious brain processing of form and chromatic color has been found in patients with intact striate areas but lesions to extra-striate areas, for example patients with visual form agnosia and achromatopsia, suggesting that extra-striate areas may be a neural correlate of chromatic color experience and form experience, though not for simple shape experience and achromatic color experience (Aglioti et al. 1999, Danckert and Goodale 2000, Sacks 1996).
Here we set out to test the hypothesis that subjects with thought-induced synesthesia can process colored visual stimuli unconsciously. Synesthesia is a relatively rare neurological condition in which stimulation in one sensory or cognitive stream leads to associated experiences in a second unstimulated stream (Cytowic 1989). In most subjects with color synesthesia the perception of sounds or shapes automatically triggers color perception. This is also known as projector-synesthesia (Dixon et al. 2004), though a better term may be ‘lower synesthesia’, as projection sometimes occurs in thought-induced synesthesia (Hubbard and Ramachandran 2005). In thought-induced color synesthesia (‘associator synesthesia’ or ‘higher synesthesia’) perception alone does not trigger color perception but thoughts about sounds or shapes trigger a perception of particular colors. In general, graphemes elicit strong externally projected photisms in projector synesthetes, whereas thoughts about numbers or letters elicit internally experienced sensations of color that is similar to vivid visual imagery but usually with a more intense phenomenology. Because of this difference, the two kinds of synesthetes have different patterns of Stroop interference (Dixon et al. 2004). For projector synesthetes, a greater Stroop interference was gotten when the color of the ink in which a grapheme was presented was named. Associator synesthetes show less Stroop interference when the color of the ink is named.
The neural mechanisms underlying the two forms of synesthesia are not completely understood. Some have speculated that primitive perceptual experiences in the limbic system are involved in synesthetic experiences (for discussion see Hubbard and Ramachandran 2005). Others have suggested that different sense modalities or cognitive streams interact through an abnormally high number of interconnecting pathways (Hubert et al. 2005). A third group of more skeptical thinkers hold that synesthesia is particularly vivid cognitive associations. The currently most dominant theory is that the usual feedback circuits that play a role in normal visual perception transmit information from other senses or memory. On this theory, synesthesia is the result of unusual activation of lower visual areas (disinhibition of feedback) (Hubbard 2007, Hubbard and Ramachandran 2005, Sperling et al., 2005, Grossenbacher, P.G. and Lovelace C.T. 2001). Cross-activation is believed to occur in the ventral part of parietal cortex (Hubbard et al. 2005). Re-entrant information processing in the primary visual cortex thus consists in normal color processing but triggered by signals from distinct sense modalities or cognitive streams. fMRI studies have shown that synesthesia involves activation of striate (V1) cortex in the absence of a visual stimulus (Aleman et al. 2001). This adds support to the hypothesis that awareness of color in synaesthesia is the result of unusual feedback activation of early visual areas.
Feedback activation of early visual areas in color synesthesia is normally associated with visual awareness. It has not yet been shown whether higher color synesthetes when exposed to achromatic visual stimuli undergo unconscious color processing. If they do, then black and white strings of numbers that are uniformly colored when the higher synesthetes are thinking about them should trigger unconscious color processing when the number strings are visually presented to the synesthetes. Synesthetes should thus be able to identify these strings of numbers faster in visual search tests than normal subjects. We have found some confirmation of this hypothesis in a number of recent beta-testings. To further test this hypothesis, we will give 40 subjects with color-number synesthesia and 400 control subjects four visual number search tests and two visual shape search tests. The purpose of the experiments is to investigate whether, owing to unconscious color processing, higher synesthetes can identify black and white numbers quicker in the visual number search tests compared to the control subjects. The visual shape search tests will be used as controls. A demonstration of this sort of unconscious color processing in higher synethetes might tend to suggest that higher and lower synesthesia have similar neural correlates. Our hypothesis is that both lower and higher synesthesia are the result of cross-activation in higher areas (e.g. parietal cortex) and feedback to lower visual areas, but that the brain activation in lower visual areas is too weak in higher synesthetes to give rise to conscious color experience.
Subjects: 40 subjects who have reported color-number synesthesia will be asked to give their informed consent/assent to participate in the experiments. The subjects will be asked whether they have a known history of neurological or psychiatric illness, whether they take hallucinogenic medication and whether they suffer from frequent migraines. Evidence for genuine color-number synesthesia will be obtained with a number-color test (Baron-Cohen et al. 1987) in which the subjects will be asked which color they experience for each number from 1-20. According to the criterion of synesthesia, the colors reported for each number or letter should be demonstrated to be highly stable across a considerable period of time. All test subjects will be tested on two occasions 6 weeks apart. A neuropsychological examination of the subjects will be done by a trained psychiatrist and interviews with the subjects will be done by the PI. Sample size calculation determined an n=400 for the control group with a power = 80% and an alpha = 0.05 (two-tailed). Accordingly, 400 controls, who test negative for synesthesia, will be asked to give their informed consent/assent to participate in the studies. All test subjects will be interviewed about the phenomenology of their synesthetic experience. They will be given four visual search tests and two visual shape search tests.
The protocol was approved by the UM-St. Louis Human Subjects Committee. Protocol number: 100108P