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An Event-Related Potential Study of Auditory–Visual Synesthesia

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An Event-Related Potential Study of Auditory–Visual Synesthesia Seeing Sounds and Hearing Colors: An Event-related Potential Study of Auditory–Visual Synesthesia Aviva I. Goller1, Leun J. Otten2, and Jamie Ward1 Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/21/10/1869/1759787/jocn.2009.21134.pdf by guest on 18 May 2021 Abstract & In auditory–visual synesthesia, sounds automatically elicit the controls attended to the auditory dimension alone. There conscious and reliable visual experiences. It is presently un- were clear differences between synesthetes and controls that known whether this reflects early or late processes in the emerged early (100 msec after tone onset). These differences brain. It is also unknown whether adult audiovisual synesthe- tended to lie in deflections of the auditory-evoked potential sia resembles auditory-induced visual illusions that can some- (e.g., the auditory N1, P2, and N2) rather than the presence times occur in the general population or whether it resembles of an additional posterior deflection. The differences occurred the electrophysiological deflection over occipital sites that has irrespective of what the synesthetes attended to (although been noted in infancy and has been likened to synesthesia. attention had a late effect). The results suggest that differences Electrical brain activity was recorded from adult synesthetes between synesthetes and others occur early in time, and that and control participants who were played brief tones and re- synesthesia is qualitatively different from similar effects found quired to monitor for an infrequent auditory target. The syn- in infants and certain auditory-induced visual illusions in adults. esthetes were instructed to attend either to the auditory or to In addition, we report two novel cases of synesthesia in which the visual (i.e., synesthetic) dimension of the tone, whereas colors elicit sounds, and vice versa. & INTRODUCTION showing that the auditory-color associations of these In auditory–visual synesthesia, sounds automatically synesthetes are more consistent than controls and by elicit conscious visual percepts in addition to an audi- showing that the synesthetic color of a task-irrelevant tory percept. For example, a cello may sound like a tone interferes with color naming in a Stroop task (Ward ‘‘dark velvet or reddish-brown tree trunk-like texture’’ et al., 2006). However, in other respects there are com- and a flute may be ‘‘dry and transparent with pastel monalities between the nature of synesthetic experiences colors’’ (Mills, Boteler, & Larcombe, 2003). For some and those reported by nonsynesthetes in imagery, match- individuals, the synesthesia is triggered solely by speech ing tasks, or cross-modal interference paradigms (Ward (e.g., Nunn et al., 2002; Paulesu et al., 1995; Baron- et al., 2006; Marks, 2004). In particular, high-pitched Cohen, Harrison, Goldstein, & Wyke, 1993), but for sounds tend to be visually lighter, higher, and smaller others the synesthesia is triggered by all known auditory than low-pitch sounds in both synesthetic experiences stimuli (e.g., Thornley Head, 2006; Ward, Huckstep, & and response biases of nonsynesthetes (Marks, 2004). Tsakanikos, 2006). This may reflect a qualitative dif- This suggests common processes between synesthetic ference between whether synesthesia is linked to linguis- perception and audiovisual processing of nonsynesthetes. tic representations (e.g., graphemes) versus perceptual The present study will use ERPs (small changes in the properties of the stimulus such as its pitch (e.g., Simner, brain’s electrical activity time locked to an event) to ad- Glover, & Mowat, 2006; Frith & Paulesu, 1997). Our study judicate between two different theories. considers the latter, using nonspeech tones. This variety One suggestion is that the newborn infants’ experi- of synesthesia is of particular theoretical interest because ences of the world resemble a form of synesthesia of the large literature on audiovisual interactions in the (Maurer & Mondloch, 2006; Maurer & Maurer, 1988), nonsynesthetic brain (e.g., Calvert, Hansen, Iversen, & in which the senses are yet to be differentiated and Brammer, 2001). It raises the possibility that this type of in which one sense (e.g., audition) can trigger another synesthesia reflects an adaptation of normal multisensory (e.g., vision). For example, infants show cross-modal processes (Ward et al., 2006). Previous research has dem- habituation depending on the intensity of light and onstrated the authenticity of this type of synesthesia by sounds (Lewkowicz & Turkewitz, 1980). A further claim is that, in some individuals, these early multisensory path- ways are retained into adulthood giving rise to devel- 1University of Sussex, 2University College London opmental synesthesia whereas in most other individuals D 2008 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 21:10, pp. 1869–1881 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.2009.21134 by guest on 02 October 2021 they are greatly diminished (Maurer, 1997; Baron-Cohen, study, we retest JR using visual- and auditory-evoked 1996). Electrophysiological correlates of infantile auditory– ERPs together with one other synesthete, SL, who re- visual ‘‘synesthesia’’ have been reported. These consist ports a similar pattern to JR. of a large negative deflection between 100 and 500 msec There is, however, an alternative to the hypothesis over occipital sites (absent by 30 months of age), con- of direct auditory–visual connections. This has been trasting with a developmentally more stable potential termed the ‘‘cross-modal transfer hypothesis’’ (Ward over temporal sites (Neville, 1995). Although a direct et al., 2006; Baron-Cohen, 1996). This hypothesis as- comparison between adult audiovisual synesthetes and sumes that connections between auditory and visual normal infants would be impossible to interpret (e.g., regions are indirect and are mediated by multisensory due to developmental changes in conductance), one can audiovisual brain regions. Activation in multisensory Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/21/10/1869/1759787/jocn.2009.21134.pdf by guest on 18 May 2021 nevertheless determine whether a qualitatively similar neurons may feedback and influence activity in regions electrophysiological signature is found in adult synes- traditionally considered to be unisensory (e.g., Driver thetes to that previously documented in infants. Accord- & Spence, 2000). Although multisensory processes may ing to this account, the electrophysiological responses normally be activated when two senses are stimulated, to auditory stimuli should include an early deflection it is also conceivable that they can sometimes be ac- maximal over posterior sites. tivated by a unimodal stimulus in some situations Recent studies have shown that there are direct projec- (e.g., Giraud, Price, Graham, Truy, & Frackowiak, 2001; tions from primary auditory cortex (A1) to primary visual Calvert et al., 1997). Synesthesia may be one such cortex (V1) in the mature primate brain although they example. According to this account, an additional ERP are primarily found in regions representing peripheral deflection (due to multisensory binding) would follow vision (Rockland & Ojima, 2003; Falchier, Clavagnier, the normal early auditory deflections, but would pre- Barone, & Kennedy, 2002). Even in nonsynesthetes, di- cede in time any auditory-evoked visual potential. rect auditory–visual projections may play a functional To date, there have been very few ERP studies of role in multisensory processing. It may even give rise to synesthesia. Two studies have considered grapheme- a synesthesia-like illusion in the normal population. color synesthesia using visually presented graphemes Shams, Kamitani, Thompson, and Shimojo (2001) and (Schiltz et al., 1999) or spoken letter names and words Shams, Kamitani, and Shimojo (2000) report that if two (Beeli, Esslen, & Jancke, 2008). In addition, there are beeps are played in quick succession and are accompa- two single case studies that have specifically investigated nied by a single flash, then participants often perceive electrophysiological correlates of auditory–visual synes- two distinct flashes instead of one: the double-flash illu- thesia using nonlinguistic stimuli (Rao, Nobre, Alexander, sion. The illusion occurs predominantly in peripheral vi- & Cowey, 2007; Rizzo & Eslinger, 1989). sion, consistent with the known anatomy of the direct Schiltz et al. (1999) tested 17 grapheme-color synes- projections. They report that the illusory flash is accom- thetes who were presented with runs of visual letters panied by electrical activity over occipital sites (Oz, O1, and who were required to detect certain target letters and O2) less than 110 msec after the onset of the second (e.g., vowels). They reported an increased positivity at beep (Shams et al., 2001), and a recent fMRI study shows frontal and central scalp sites emerging around 150 msec differences in V1 activity but not in other brain regions and maintained until 600 msec, relative to a nonsynes- (Watkins,Shams,Tanaka,Haynes,&Rees,2006). thetic control group. More recently, an ERP study was Anatomical studies that have attempted to look for reported of grapheme-color synesthesia in which spo- the reverse pathways, from V1 to A1, have not found ken letters and words elicit experiences of color (Beeli them (Innocenti, Berbel, & Clarke, 1988). The apparent et al., 2008). As noted above, in this type of ‘‘color rarity with which
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