Accessible Requires Authentication Published by De Gruyter June 25, 2014

Neuroscience of synesthesia and cross-modal associations

Marcel Neckar and Petr Bob

Abstract

Synesthesia is a condition in which stimulation of one sensory modality causes unusual experiences in a different, unstimulated modality. Recent findings suggest that research on synesthesia offers a unique opportunity to study the neural basis of subjective experiences in healthy and pathological brains. This review summarizes and reflects current knowledge concerning synesthesia in its various aspects, including its cognitive, neural, and behavioral aspects. In this context, recent data suggest new connections between specific conditions related to synesthesic mechanisms and association processes linked to construction of synesthetic cross-modal metaphors that may play a role in psychopathological thinking and imagination.


Corresponding author: Petr Bob, Center for Neuropsychiatric Research of Traumatic Stress, First Faculty of Medicine, Department of Psychiatry and UHSL, Charles University, Ke Karlovu 11, CZ-128 00 Prague, Czech Republic, e-mail: ; and CEITEC, Masaryk University, Brno, Czech Republic

Acknowledgments

The study was supported by the Charles University grant (PRVOUK and SVV), project provided by Czech Ministry of Education (LH11032), and the project ‘CEITEC–Central European Institute of Technology’ (CZ.1.05/1.1.00/02.0068) from the European Regional Development Fund.

Conflict of interest statement: The authors declare that there are no conflicts of interest.

References

Armel, K.C. and Ramachandran, V.S. (1999). Acquired synesthesia in retinitis pigmentosa. Neurocase 5, 293–296. Search in Google Scholar

Asher, J.E., Lamb, J.A., Brocklebank, D. Cazier, J.B., Maestrini, E., Addis, L., Sen, M., Baron-Cohen, S., and Monaco, A.P. (2009). A whole-genome scan and fine-mapping linkage study of auditory-visual synesthesia reveals evidence of linkage to chromosomes 2q24, 5q33, 6p12, and 12p12. Am. J. Hum. Genet. 84, 1–7. Search in Google Scholar

Baron-Cohen, S., Harrison, J., Goldstein, J.H., and Wyke M. (1993). Coloured speech perception: is synaesthesia what happens when modularity breaks down? Perception 22, 419–426. Search in Google Scholar

Baron-Cohen, S., Burt, L., Smith-Laittan, F., Harrison, J., and Bolton, P. (1996). Synaesthesia: prevalence and familiality. Perception 25, 1073–1079. Search in Google Scholar

Baron-Cohen, S., Bor, D., Billington, J., Asher, J., Wheelwright, S., and Ashwin, C. (2007). Savant memory in a man with colour form-number synaesthesia and Asperger syndrome. J. Conscious. Stud. 14, 237–252. Search in Google Scholar

Brogaard, B. (2013). Serotonergic hyperactivity as a potential factor in developmental, acquired and drug-induced synesthesia. Front. Hum. Neurosci. 7, 657. Search in Google Scholar

Carmichael, D.A. and Simner, J. (2013). The immune hypothesis of synesthesia. Front. Hum. Neurosci. 7, 563. Search in Google Scholar

Cohen Kadosh, R., Henik, A., Catena, A., Walsh, V., and Fuentes, L.J. (2009). Induced cross-modal synaesthetic experience without abnormal neuronal connections. Psychol. Sci. 20, 258–265. Search in Google Scholar

Collier, G.L. (1996). Affective synaesthesia: extracting emotion space from simple perceptual stimuli. Motiv. Emot. 20, 1–32. Search in Google Scholar

Cytowic, R.E. (1989). Synesthesia and mapping of subjective sensory dimensions. Neurology 39, 849–850. Search in Google Scholar

Cytowic, R.E. (2002). Synesthesia: A Union of the Senses. 2nd ed. (Cambridge, MA, UK: MIT Press). Search in Google Scholar

Cytowic, R.E. and Wood, F.B. (1982a). Synesthesia. I. A review of major theories and their brain basis. Brain Cogn. 1, 23–35. Search in Google Scholar

Cytowic, R.E. and Wood, F.B. (1982b). Synesthesia. II. Psychophysical relations in the synesthesia of geometrically shaped taste and colored hearing. Brain Cogn. 1, 36–49. Search in Google Scholar

Dael, N., Sierro, G., and Mohr, C. (2013). Affect-related synesthesias: a prospective view on their existence, expression and underlying mechanisms. Front. Psychol. 4, 754. Search in Google Scholar

Dailey, A., Martindale, C., and Borkum, J. (1997). Creativity, synesthesia, and physiognomic perception. Creativity Res. J. 10, 1–8. Search in Google Scholar

Day, S. (1996). Synaesthesia and synaesthetic metaphors. Psyche 2, 32. http://psyche.cs.monash.edu.au/v2/psyche-2-32-day.html. Search in Google Scholar

Day, S. (2004). Some Demographic and Socio-Cultural Aspects of Synesthesia. Synesthesia: Perspectives From Cognitive Neuroscience. L.C. Robertson and N. Sagiv, eds. (New York: Oxford University Press), pp. 11–33. Search in Google Scholar

Dixon, M.J., Smilek, D., and Merikle, P.M. (2004). Not all synaesthetes are created equal: projector versus associator synaesthetes. Cogn. Affect. Behav. Neurosci. 4, 335–343. Search in Google Scholar

Eagleman, D.M. and Goodale, M.A. (2009). Why color synesthesia involves more than color. Trends Cogn. Sci. 13, 288–292. Search in Google Scholar

Esterman, M., Verstynen, T., Ivry, R.B., and Robertson, L.C. (2006). Coming unbound: disrupting automatic integration of synaesthetic color and graphemes by TMS of right parietal lobe. J. Cogn. Neurosci. 18, 1570–1576. Search in Google Scholar

Fitzgibbon, B.M., Enticott, P.G., Rich, A.N., Giummarra, M.J., Georgiou-Karistianis, N., Tsao, J.W., Weeks, S.R., and Bradshaw, J.L. (2010a). High incidence of ‘synaesthesia for pain’ in amputees. Neuropsychologia 48, 3675–3678. Search in Google Scholar

Fitzgibbon, B.M., Giummarra, M.J., Georgiou-Karistianis, N., Enticott, P.G., and Bradshaw, J.L. (2010b). Shared pain: from empathy to synaesthesia. Neurosci. Biobehav. Rev. 34, 500–512. Search in Google Scholar

Fuentes, L., Cohen-Kadosh, R., Catena, A., and Henik, A. (2007). Synesthesia experience under posthypnotic suggestion: evidence in favour of the disinhibition hypothesis. Paper presented at the Synaesthesia, Science & Art: Second International Congress, Granada, Spain. Search in Google Scholar

Galeyev, B.M. (2007). The nature and functions of synesthesia in music. Leonardo 40, 285–288. Search in Google Scholar

Galton, F. (1883). Enquiries into the human faculty and its development (London: Everyman). Search in Google Scholar

Goller, A.I., Otten, L.J., and Ward, J. (2009). Seeing sounds and hearing colors: an event-related potential study of auditory-visual synesthesia. J. Cogn. Neurosci. 21, 1869–1881. Search in Google Scholar

Grossenbacher, P.G. and Lovelace, C.T. (2001). Mechanisms of synesthesia: cognitive and physiological constraints. Trends Cogn. Sci. 5, 36–41. Search in Google Scholar

Harrison, J. and Hare, D.J. (2004). Brief report: assessment of sensory abnormalities in people with autistic spectrum disorders. J. Autism Dev. Disord. 34, 727–730. Search in Google Scholar

Hartman, A.M. and Hollister, L.E. (1963). Effect of mescaline, lysergic acid diethylamide and psilocybin on color perception. Psychopharmacolgia 4, 441–451. Search in Google Scholar

Hochel, M. and Milan, E.G. (2008). Synaesthesia: the existing state of affairs. Cogn. Neuropsychol. 25, 93–117. Search in Google Scholar

Hubbard, E.M. (2007). Neurophysiology of synesthesia. Curr. Psychiatry Rep. 9, 193–199. Search in Google Scholar

Hubbard, E.M. and Ramachandran, V.S. (2005). Neurocognitive mechanisms of synesthesia. Neuron 48, 509–520. Search in Google Scholar

Hubbard, E.M., Arman, A.C., Ramachandran, V.S., and Boynton, G.M. (2005). Individual differences among grapheme-color synesthetes: Brain-behavior correlations. Neuron 45, 975–985. Search in Google Scholar

Hubbard, E.M., Brang, D., and Ramachandran, V.S. (2011). The cross activation theory at 10. J. Neuropsychol. 5, 152–177. Search in Google Scholar

Ione, A. and Tyler, C. (2004). Neuroscience, history and the arts. Synesthesia: is F-sharp colored violet? J. Hist. Neurosci. 13, 58–65. Search in Google Scholar

Iturria-Medina, Y., Pérez Fernández, A., Morris, D.M., Canales-Rodríguez, E.J., Haroon, H.A., García Pentón, L., Augath, M., Galán García, L., Logothetis, N., Parker, G.J., et al. (2011). Brain hemispheric structural efficiency and interconnectivity rightward asymmetry in human and nonhuman primates. Cereb. Cortex 21, 56–67. Search in Google Scholar

Jewanski, J., Simner, J., Day, S.A., and Ward, J. (2011). The development of a scientific understanding of synesthesia from early case studies (1849–1873). J. Hist. Neurosci. 20, 284–305. Search in Google Scholar

Kadosh, R.C. and Walsh, V. (2008). Synaesthesia and cortical connections: cause or correlation? Trends Neurosci. 31, 549–550. Search in Google Scholar

Kadosh, R.C., Henik, A., and Walsh, V. (2007a). Small is bright and big is dark in synaesthesia. Curr. Biol. 17, 834–835. Search in Google Scholar

Kadosh, R.C., Kadosh, K.C., and Henik, A. (2007b). The neuronal correlate of bi-directional synaesthesia: a combined ERP and fMRI study. J. Cogn. Neurosci. 19, 2050–2059. Search in Google Scholar

Kadosh, R.C., Henik, A., Catena, A., Walsh, V., and Fuentes, L.J. (2008). Induced cross-modal synesthetic experience without abnormal neuronal connections. Psychol. Sci. 20, 258–265. Search in Google Scholar

Kuhbandner, C. and Pekrun, R. (2013). Joint effects of emotion and color on memory. Emotion 13, 375–379. Search in Google Scholar

Lakoff, G. (1993). The Contemporary Theory of Metaphor. Metaphor and Thought. 2nd ed. A. Ortony, ed. (Cambridge, UK: Cambridge University Press). Search in Google Scholar

Lakoff, G. and Johnson, M.H. (1980). Metaphors We Live By (Chicago, IL: University of Chicago Press). Search in Google Scholar

Maddock, R.J. (1999). The retrosplenial cortex and emotion: New insights from functional neuroimaging of the human brain. Trends Neurosci. 22, 310–316. Search in Google Scholar

Marks, L.E. (1975). On colored-hearing synesthesia: cross-modal translations of sensory dimensions. Psychol. Bull. 82, 303–331. Search in Google Scholar

Marks, L.E. (1978). The Unity of the Senses: Interrelations Among the Modalities (New York: Academic Press). Search in Google Scholar

Marks, L.E. (1982). Synesthetic perception and poetic metaphor. J. Exp. Psychol. Hum. Percept. Perform. 8, 15–23. Search in Google Scholar

Marks, L.E. (2011). Synesthesia: then and now. Intellectica 55, 47–80. Search in Google Scholar

Marks, L.E. (2013). Weak Synaesthesia in the General Population. Oxford Handbook of Synaesthesia. J. Simner and E. Hubbard, eds. (Oxford, UK: Oxford University Press). Search in Google Scholar

Marks, L.E. and Mulvenna, C.M. (2013). Synesthesia, at and near its borders. Front. Psychol. 4, 651. Search in Google Scholar

Martino, G. and Marks, L.E. (2001). Synesthesia: strong and weak. Psychol. Sci. 10, 61–65. Search in Google Scholar

Milán, E.G., Hochel, M., González, A., Tornay, F., McKenney, K., Díaz Caviedes, R., Mata Martín, J.L., Rodríguez, A., Domínguez, G.E., and Vila, J. (2007). Experimental study of phantom colors in a color blind synaesthete. J. Conscious. Stud. 14, 75–95. Search in Google Scholar

Moller, A.C., Elliot, A.J., and Maier, M.A. (2009). Basic hue-meaning associations. Emotion 9, 898–902. Search in Google Scholar

Mulvenna, C.M. and Walsh, V. (2006). Synesthesia: supernormal integration? Trends Cogn. Sci. 10, 350–352. Search in Google Scholar

Mulvenna, C.M., Hubbard, E.M., Ramachandran, V.S., and Pollick, F. (2004). The relationship between synaesthesia and creativity. J. Cogn. Neurosci. Suppl. 16, 188. Search in Google Scholar

Myles, K.M., Dixon, M.J., Smilek, D., and Merikle, P.M. (2003). Seeing double: the role of meaning in alphanumeric-colour synaesthesia. Brain Cogn. 53, 342–345. Search in Google Scholar

Neufeld, J., Sinke, C., Zedler, M., Dillo, W., Emrich, H.M., Bleich, S., and Szycik, G.R. (2012). Disinhibited feedback as a cause of synesthesia: evidence from a functional connectivity study on auditory-visual synesthetes. Neuropsychologia 50, 1471–1477. Search in Google Scholar

Nunn, J.A., Gregory, L.J., Brammer M., Williams, S.C.R., Parslow, D.M., Morgan, M.J., Morris, R.G., Bullmore, E.T., Baron-Cohen, S., and Gray, J.A. (2002). Functional magnetic resonance imaging of synesthesia: activation of V4/V8 by spoken words. Nat. Neurosci. 5, 371–375. Search in Google Scholar

Okubo, M. and Ishikawa, K. (2011). Automatic semantic association between emotional valence and brightness in the right hemisphere. Cogn. Emot. 25, 1273–1280. Search in Google Scholar

Palmer, S.E., Schloss, K.B., Xu Z., and Prado-León, L.R. (2013). Music-color associations are mediated by emotion. Proc. Natl. Acad. Sci. USA 110, 8836–8841. Search in Google Scholar

Parise, C.V. and Spence, C. (2009). ‘When birds of a feather flock together’: synesthetic correspondences modulate audiovisual integration in non-synesthetes. PLoS One 4, 5664. Search in Google Scholar

Pearce, J.M.S. (2006). Synaesthesia. Eur. Neurol. 57, 120–124. Search in Google Scholar

Perry, A. and Henik A. (2013). The emotional valence of a conflict: implications from synesthesia. Front. Psychol. 26, 978. Search in Google Scholar

Radvansky, G.A., Gibson, B.S., and McNerney, M.W. (2011). Synesthesia and memory: color congruency, von Restorff, and false memory effects. J. Exp. Psychol. Learn. Mem. Cogn. 37, 219–229. Search in Google Scholar

Ramachandran, V.S. and Hubbard, E.M. (2001a). Psychophysical investigations into the neural basis of synaesthesia. Proc. R. Soc. Lond. 268, 979–983. Search in Google Scholar

Ramachandran, V.S. and Hubbard, E.M. (2001b). Synaesthesia: a window into perception, thought and language. J. Conscious. Stud. 8, 3–34. Search in Google Scholar

Ramachandran, V.S. and Hubbard, E.M. (2003). Hearing colors, tasting shapes. Sci. Am. 288, 52–59. Search in Google Scholar

Ramachandran, V.S. and Rogers-Ramachandran, D. (1996). Synaesthesia in phantom limbs induced with mirrors. Proc. Biol. Sci. 263, 377–386. Search in Google Scholar

Rotenberg, V.S. (2004). The ontogeny and asymmetry of the highest brain skills and the pathogenesis of schizophrenia. Behav. Brain Sci. 27, 863–864. Search in Google Scholar

Rotenberg, V.S. (2013). Moravec’s paradox: consideration in the context of two brain hemisphere functions. Act. Nerv. Super. (Praha) 55, 108–111. Search in Google Scholar

Rouw, R. and Scholte, S. (2007). Increased structural connectivity in grapheme-color synesthesia. Nat. Neurosci. 10, 792–797. Search in Google Scholar

Rouw, R., Scholte, H.S., and Colizoli, O. (2011). Brain areas involved in synaesthesia: a review. J. Neuropsychol. 5, 214–242. Search in Google Scholar

Sagiv, N. and Ward, J. (2006). Cross-modal interactions: lessons from synesthesia. Prog. Brain Res. 155, 259–271. Search in Google Scholar

Schiltz, K., Trocha, K., Wieringa, B.M., Emrich, H.M., Johannes, S., and Munte, T.F. (1999). Neurophysiological aspects of synesthetic experience. J. Neuropsychiatry Clin. Neurosci. 11, 58–65. Search in Google Scholar

Simner, J. (2012a). Defining synaesthesia. Br. J. Psychol. 103, 1–15. Search in Google Scholar

Simner, J. (2012b). Defining synaesthesia: a response to two excellent commentaries. Br. J. Psychol. 103, 24–27. Search in Google Scholar

Simner, J. (2013). Why are there different types of synesthete? Front. Psychol. 2, 558. Search in Google Scholar

Simner, J. and Hubbard, E. eds. (2013). Oxford Handbook of Synaesthesia. (Oxford: Oxford University Press). Search in Google Scholar

Simner, J., Gärtner O., and Taylor M. D. (2011). Cross-modal personality attributions in synaesthetes and non-synaesthetes. J. Neuropsychol. 5, 283–301. Search in Google Scholar

Sinke, C., Halpern, J.H., Zedler, M., Neufeld, J., Emrich, H.M., and Passie, T. (2012). Genuine and drug-induced synesthesia: a comparison. Conscious. Cogn. 21, 1419–1434. Search in Google Scholar

Smilek, D., Dixon, M.J., Cudahy, C., and Merikle, P.M. (2001). Synaesthetic photisms influence visual perception. J. Cogn. Neurosci. 13, 930–936. Search in Google Scholar

Smilek, D., Dixon, M.J., and Merikle, P.M. (2005). Synaesthesia: discordant male monozygotic twins. Neurocase 11, 363–370. Search in Google Scholar

Spector, F. and Maurer, D. (2009). Synesthesia: a new approach to understanding the development of perception. Dev. Psychol. 45, 175–189. Search in Google Scholar

Spence, C. (2002). Multisensory attention and tactile information-processing. Behav. Brain Res. 135, 57–64. Search in Google Scholar

Steven, M.S. and Blakemore, C. (2004). Visual synaesthesia in the blind. Perception 33, 855–868. Search in Google Scholar

Steven, M.S., Hansen, P.C., and Blakemore, C. (2006). Activation of color-selective areas of the visual cortex in a blind synesthete. Cortex 42, 304–308. Search in Google Scholar

Stuckey, D.E., Lawson, R., and Luna, L.E. (2005). EEG gamma coherence and other correlates of subjective reports during ayahuasca experiences. J. Psychoactive Drugs 37, 163–178. Search in Google Scholar

Terhune, D.B., Cardena, E., and Lindgren, M. (2010). Disruption of synaesthesia by posthypnotic suggestion: an ERP study. Neuropsychologia 48, 3360–3364. Search in Google Scholar

Tomson, S.N., Narayan, M., Allen, G.I., and Eagleman, D.M. (2013). Neural networks of colored sequence synesthesia. J. Neurosci. 33, 14098–14106. Search in Google Scholar

van der Veen, F.M., Aben, H.P., Smits, M., and Röder, C.H. (2014). Grapheme-color synesthesia interferes with color perception in a standard Stroop task. Neuroscience 258, 246–253. Search in Google Scholar

Volberg, G., Karmann, A., Birkner, S., and Greenlee, M.W. (2013). Short- and long-range neural synchrony in grapheme-color synesthesia. J. Cogn. Neurosci. 25, 1148–1162. Search in Google Scholar

Voskuil, P.H. (2013). Van Gogh’s disease in the light of his correspondence. Front. Neurol. Neurosci. 31, 116–125. Search in Google Scholar

Walsh, R. (2005). Can synesthesia be cultivated? Indications from surveys of meditators. J. Consc. Stud. 12, 5–17. Search in Google Scholar

Ward, J. (2004). Emotionally mediated synaesthesia. Cogn. Neuropsychol. 21, 761–772. Search in Google Scholar

Ward, J. (2013). Synesthesia. Annu. Rev. Psychol. 64, 49–75. Search in Google Scholar

Ward, J. and Mattingley, J.B. (2006). Synaesthesia: an overview of contemporary findings and controversies. Cortex 42, 129–136. Search in Google Scholar

Ward, J. and Simner, J. (2005). Is synaesthesia an X-linked dominant trait with lethality in males? Perception 34, 611–623. Search in Google Scholar

Ward, J., Huckstep, B., and Tsakanikos, E. (2006). Sound-colour synaesthesia: to what extent does it use cross-modal mechanisms common to us all? Cortex 42, 264–280. Search in Google Scholar

Received: 2014-5-2
Accepted: 2014-6-5
Published Online: 2014-6-25
Published in Print: 2014-12-1

©2014 by De Gruyter