The Emergence of Synaesthesia in a Neuronal Network Model via Changes in Perceptual Sensitivity and Plasticity

Synaesthesia is an unusual perceptual experience in which an inducer stimulus triggers a percept in a different domain in addition to its own. To explore the conditions under which synaesthesia evolves, we studied a neuronal network model that represents two recurrently connected neural systems. The interactions in the network evolve according to learning rules that optimize sensory sensitivity. We demonstrate several scenarios, such as sensory deprivation or heightened plasticity, under which synaesthesia can evolve even though the inputs to the two systems are statistically independent and the initial cross-talk interactions are zero. Sensory deprivation is the known causal mechanism for acquired synaesthesia and increased plasticity is implicated in developmental synaesthesia. The model unifies different causes of synaesthesia within a single theoretical framework and repositions synaesthesia not as some quirk of aberrant connectivity, but rather as a functional brain state that can emerge as a consequence of optimising sensory information processing.

[1]  Anina N. Rich,et al.  A systematic, large-scale study of synaesthesia: implications for the role of early experience in lexical-colour associations , 2005, Cognition.

[2]  L. Hollister,et al.  Effect of mescaline, lysergic acid diethylamide and psilocybin on color perception , 1963, Psychopharmacologia.

[3]  J. Simner.  Defining synaesthesia. , 2012, British journal of psychology.

[4]  Jamie Ward,et al.  Non-random associations of graphemes to colours in synaesthetic and non-synaesthetic populations , 2005, Cognitive neuropsychology.

[5]  Thomas M. Cover,et al.  Elements of Information Theory , 2005 .

[6]  L. Merabet,et al.  The plastic human brain cortex. , 2005, Annual review of neuroscience.

[7]  Marcus R. Watson,et al.  Synesthesia and learning: a critical review and novel theory , 2014, Front. Hum. Neurosci..

[8]  Alan Cowey,et al.  Enhanced Cortical Excitability in Grapheme-Color Synesthesia and Its Modulation , 2011, Current Biology.

[9]  J. Ward,et al.  Enhanced memory ability: Insights from synaesthesia , 2012, Neuroscience & Biobehavioral Reviews.

[10]  Jamie Near,et al.  Phosphene Perception Relates to Visual Cortex Glutamate Levels and Covaries with Atypical Visuospatial Awareness , 2015, Cerebral cortex.

[11]  F. Matsuo,et al.  Acquired auditory-visual synesthesia: A window to early cross-modal sensory interactions , 2009, Psychology research and behavior management.

[12]  W. Dillo,et al.  Is synesthesia more common in patients with Asperger syndrome? , 2013, Front. Hum. Neurosci..

[13]  S. Carpenter,et al.  Early-warning signals for critical transitions , 2009, Nature.

[14]  V. Ramachandran,et al.  Psychophysical investigations into the neural basis of synaesthesia , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[15]  O. Sporns,et al.  Organization, development and function of complex brain networks , 2004, Trends in Cognitive Sciences.

[16]  Jean-Baptiste Cazier,et al.  A whole-genome scan and fine-mapping linkage study of auditory-visual synesthesia reveals evidence of linkage to chromosomes 2q24, 5q33, 6p12, and 12p12. , 2009, American journal of human genetics.

[17]  Fiona N. Newell,et al.  Familial patterns and the origins of individual differences in synaesthesia , 2008, Cognition.

[18]  Vincent Walsh,et al.  Enhanced sensory perception in synaesthesia , 2009, Experimental Brain Research.

[19]  D. Plenz,et al.  Neuronal Avalanches in the Resting MEG of the Human Brain , 2012, The Journal of Neuroscience.

[20]  V. Walsh,et al.  Synesthesia for Color Is Linked to Improved Color Perception but Reduced Motion Perception , 2013, Psychological science.

[21]  Karl J. Friston,et al.  Predictive coding under the free-energy principle , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[22]  Naomi B. Pitskel,et al.  Rapid and Reversible Recruitment of Early Visual Cortex for Touch , 2008, PloS one.

[23]  Jamie Ward,et al.  Synaesthesia: The Prevalence of Atypical Cross-Modal Experiences , 2006, Perception.

[24]  A. Seth.  A predictive processing theory of sensorimotor contingencies: Explaining the puzzle of perceptual presence and its absence in synesthesia , 2014, Cognitive neuroscience.

[25]  Romke Rouw,et al.  Brain areas involved in synaesthesia: a review. , 2011, Journal of neuropsychology.

[26]  Jonathan Winawer,et al.  Prevalence of Learned Grapheme-Color Pairings in a Large Online Sample of Synesthetes , 2015, PloS one.

[27]  Steven C.R. Williams,et al.  Implications of synaesthesia for functionalism - Theory and experiments , 2002 .

[28]  S. Baron-Cohen,et al.  Coloured Speech Perception: Is Synaesthesia what Happens when Modularity Breaks Down? , 1993, Perception.

[29]  W. Brogden.  Annual Review of Psychology , 1957 .

[30]  Clare Press,et al.  Back to the future: synaesthesia could be due to associative learning , 2014, Front. Psychol..

[31]  Christopher T. Lovelace,et al.  Mechanisms of synesthesia: cognitive and physiological constraints , 2001, Trends in Cognitive Sciences.

[32]  Jamie Ward,et al.  Seeing Sounds and Hearing Colors: An Event-related Potential Study of Auditory–Visual Synesthesia , 2009, Journal of Cognitive Neuroscience.

[33]  Edward M. Hubbard,et al.  Neurocognitive Mechanisms of Synesthesia , 2005, Neuron.

[34]  Jamie Ward,et al.  Sound-Colour Synaesthesia: to What Extent Does it Use Cross-Modal Mechanisms Common to us All? , 2006, Cortex.

[35]  J. Ward,et al.  Haptic perception and synaesthesia , 2008 .

[36]  P. Hagoort,et al.  Behavioral/systems/cognitive Effective Connectivity Determines the Nature of Subjective Experience in Grapheme-color Synesthesia , 2022 .

[37]  Woodrow L. Shew,et al.  The Functional Benefits of Criticality in the Cortex , 2013, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[38]  Oren Shriki,et al.  Optimal Information Representation and Criticality in an Adaptive Sensory Recurrent Neuronal Network , 2016, PLoS Comput. Biol..

[39]  P. Huttenlocher,et al.  Regional differences in synaptogenesis in human cerebral cortex , 1997, The Journal of comparative neurology.

[40]  Marc O Ernst,et al.  Natural auditory scene statistics shapes human spatial hearing , 2014, Proceedings of the National Academy of Sciences.

[41]  H. Stanley,et al.  Introduction to Phase Transitions and Critical Phenomena , 1972 .

[42]  Oren Shriki,et al.  Near-Critical Dynamics in Stimulus-Evoked Activity of the Human Brain and Its Relation to Spontaneous Resting-State Activity , 2015, The Journal of Neuroscience.

[43]  H. Flor,et al.  Phantom limb pain: a case of maladaptive CNS plasticity? , 2006, Nature Reviews Neuroscience.

[44]  S. Makioka.  A self-organizing learning account of number-form synaesthesia , 2009, Cognition.

[45]  Daniel D. Lee,et al.  An Information Maximization Approach to Overcomplete and Recurrent Representations , 2000, NIPS.

[46]  G. Bargary,et al.  Synaesthesia and cortical connectivity , 2008, Trends in Neurosciences.

[47]  Avishai Henik,et al.  Small is bright and big is dark in synaesthesia , 2007, Current Biology.

[48]  David Brang,et al.  The cross-activation theory at 10. , 2011, Journal of neuropsychology.

[49]  D. Plenz,et al.  Criticality in neural systems , 2014 .

[50]  Avishai Henik,et al.  When Blue is Larger than Red: Colors Influence Numerical Cognition in Synesthesia , 2005, Journal of Cognitive Neuroscience.

[51]  Sang Joon Kim,et al.  A Mathematical Theory of Communication , 2006 .