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  • Neuropsychologia 50 (2012) 1471 1477

    Contents lists available at SciVerse ScienceDirect

    Neuropsychologia

    jo u rn al hom epa ge : www.elsev ier .com/ loca

    Disinhibited feedback as a cause of synesthesia: Econnec ete

    J. Neufeld richa Dept. of Psych nyb Center of Syst

    a r t i c l

    Article history:Received 24 NReceived in reAccepted 27 FAvailable onlin

    Keywords:SynesthesiaConnectivityAuditory-visualInferior parietalDisinhibited feedback

    sensoodelsulate

    tivatictivatnd th

    which may be located in the parietal cortex. This latter hypothesis is compatible with the disinhibitedfeedback model, which suggests unusual feedback from multimodal convergence areas as the cause ofsynesthesia. In this study, the relevance of these models was tested in a group (n = 14) of auditory-visualsynesthetes by performing a functional connectivity analysis on functional magnetic resonance imaging(fMRI) data. Different simple and complex sounds were used as stimuli, and functionally dened seedareas in the bilateral auditory cortex (AC) and the left inferior parietal cortex (IPC) were used for the con-

    1. Introdu

    In synesinducer, leainternally gMetzger, Focurrent. Indperiods (Simchological tactivation mfeedback mdisinhibitedcross activaof inducer back model

    Corresponapy, HannoverTel.: +49 511 5

    E-mail add1 These auth

    0028-3932/$ doi:10.1016/j.nectivity calculations. We found no differences in the connectivity of the AC and the visual areas betweensynesthetes and controls. The main nding of the study was stronger connectivity of the left IPC withthe left primary auditory and right primary visual cortex in the group of auditory-visual synesthetes.The results support the model of disinhibited feedback as a cause of synesthetic perception but do notsuggest direct cross-activation.

    2012 Elsevier Ltd. All rights reserved.

    ction

    thesia, the perception of a certain stimulus, called ands automatically and involuntarily to an additionalenerated sensation (Lupianez & Callejas, 2006; Mills,ster, Valentine-Gresko, & Ricketts, 2009), called a con-ucer-concurrent pairings remain stable over long timener & Logie, 2007). Three main classes of neuropsy-

    heories of synesthesia have been discussed: the crossodel (Ramachandran & Hubbard, 2001), the re-entrant

    odel (Smilek, Dixon, Cudahy, & Merikle, 2001), and the feedback model (Grossenbacher & Lovelace, 2001). Thetion model proposes a direct linkage between the areasand concurrent representation. The re-entrant feed-

    suggests crosstalk between the inducer and concurrent

    ding author at: Dept. of Psychiatry, Social Psychiatry and Psychother- Medical School, Carl-Neuberg-Strae 1, 30625 Hanover, Germany.32 9191; fax: +49 511 532 3187.ress: szycik.gregor@mh-hannover.de (G.R. Szycik).ors contributed equally to this study.

    brain areas along with additional feedback from higher-level areas.The disinhibited feedback model proposes an unusual activationof the concurrent-related brain areas caused by the disinhibi-tion of feedback to these areas from a multisensory nexus area,e.g., the parietal cortex. Recently, new models of synesthesia havebeen introduced based on research on grapheme-color synesthetes.These models represent extensions of the cross activation theory inthe form of the so-called two-stage model (Hubbard, 2007) and thenew cascaded cross-tuning model of synesthesia (Hubbard, Brang,& Ramachandran, 2011).

    The majority of the knowledge about synesthesia comesfrom the most commonly investigated type, namely grapheme-color synesthesia (Simner et al., 2006). There is evidence thatthis type of synesthesia involves spatially adjacent brain areasresponsible for color processing (area V4) and grapheme rep-resentation (Brang, Hubbard, Coulson, Huang, & Ramachandran,2010; Hubbard, Arman, Ramachandran, & Boynton, 2005; Nunnet al., 2002), although a recent functional neuroimaging studyin which color processing centers were identied individually ineach participant challenges this view (Hupe, Bordier, & Dojat,2011). The spatial proximity of the two areas suggests directcross-activation as the mechanism responsible for grapheme-color

    see front matter 2012 Elsevier Ltd. All rights reserved.neuropsychologia.2012.02.032tivity study on auditory-visual synestha,b,1, C. Sinkea,b,1, M. Zedlera, W. Dilloa, H.M. Em

    iatry, Social Psychiatry and Psychotherapy, Hannover Medical School, Hanover, Germaems Neuroscience, Hanover, Germany

    e i n f o

    ovember 2011vised form 26 February 2012ebruary 2012e 6 March 2012

    a b s t r a c t

    In synesthesia, certain stimuli to onelated modality. In addition to other mwhich combines two previously formand hyperbinding. The direct cross-acspecic areas are responsible for co-asuggests that the inducing stimulus ate /neuropsychologia

    vidence from a functionalsa,b, S. Bleicha,b, G.R. Szycika,

    ry modality lead to sensory perception in another unstimu-, a two-stage model is discussed to explain this phenomenon,d hypotheses regarding synesthesia: direct cross-activation

    on model postulates that direct connections between sensory-ion and synesthetic perception. The hyperbinding hypothesise synesthetic sensation are coupled by a sensory nexus area,

  • 1472 J. Neufeld et al. / Neuropsychologia 50 (2012) 1471 1477

    synesthesia (Ramachandran & Hubbard, 2001). Evidence for thismodel has been provided by imaging research focusing on neu-roanatomical alterations (Jncke, Beeli, Eulig, & Hanggi, 2009)or effective connectivity analyses (van Leeuwen, den Ouden, &Hagoort, 20several neument of thLeeuwen, PZilles, & Finment of ththe only mof synesthebetween thin which accating thatcould be re2009). Currwith a pariIvry, & Robfor synesthactivation otion of areaand concurexperience (Hubbard, 2model of grporates botFurthermorfeatures of partial activcomes froming visual cletters (Jnctory, visual,was identiinterconnecaberrationscase study osia (Hanggigrapheme-city changesWotruba, &distributedcortex), as rfunctional agyrus can eing spatiallgrapheme-cties of cortithat synestnections becouplings. Fit is conceithat sound-ple, has a dwithin moFurthermorsynesthesiacoming from& Noesselt,

    Until nosynesthesiawithin moother formsstanding ofdue to the

    of the current study was to investigate the connectivity of a priorifunctionally dened brain regions in synesthesia. We decided touse a functional connectivity analysis of functional magnetic reso-nance imaging (fMRI) data from auditory-visual synesthetes and

    ls reuli

    esthestly . Wee conal aunallymodyed hEspoty ofs in ing

    d com to idhesiaour merebage m

    meden the vishe IPuld tivitentat

    ods

    rocedormed

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    teen rt syn, handatz-Inmined

    music partit tonean, Kaed to ind wit matcked tons of d, gre

    itemd betponseesthetould bsia ints e

    uli an

    licit vg thents). nd puhe stimompoer blonter-s11). However, there is also growing evidence fromroimaging studies supporting the additional involve-e parietal cortex (Rouw & Scholte, 2007, 2010; vanetersson, & Hagoort, 2010; Weiss & Fink, 2009; Weiss,k, 2005) in grapheme-color synesthesia. This involve-e parietal cortex speaks against cross-activation asechanism in synesthesia. Furthermore, other formssia combine modalities with more spatial distancee involved brain areas, e.g., auditory-visual synesthesia,oustic stimulation leads to a visual experience, indi-

    additional mechanisms, apart from cross-activation,sponsible for this phenomenon (Goller, Otten, & Ward,ently, a combined model of cross-activation togetheretal hyperbinding mechanism (Esterman, Verstynen,ertson, 2006) is presented as an adequate explanationetic perception. This two-stage model proposes thatf concurrent areas is evoked directly by the activa-s that process the inducing stimuli, but the inducerrent sensations are bound together to form a holisticby parietal modulating mechanisms in a second step007). The recently introduced cascaded cross-tuning

    apheme-color synesthesia (Hubbard et al., 2011) incor-h early direct cross activation and top-down inuences.e, the model suggests that some of the form-relatedthe grapheme, rather than entire letters, may lead toation of color area V4. Support for the two-stage model

    a recent resting-state EEG study on subjects manifest-oncurrents evoked by auditorily presented words andke & Langer, 2011). In this study, in addition to the audi-

    frontal and limbic brain regions, the left parietal cortexed as a major hub region, which was more functionallyted in synesthetes than in non-synesthetes. Structural

    in brain connectivity have also been shown in a singlen a subject with tone-color and interval-taste synesthe-, Beeli, Oechslin, & Jancke, 2008) and in a group study onolor synesthetes, which indicated structural connectiv-

    in the fusiform gyrus and intraparietal sulcus (Hanggi, Jancke, 2011). These latter studies suggest a well-

    network, rather than only color-related areas (visualelevant for synesthetic color perception. The detectednd structural connectivity aberrations in the fusiformxplain the synesthetic perceptions for couplings affect-y adjacent inducer and concurrent brain areas (as inolor synesthesia) based on the small-world proper-cal connectivity (Bargary & Mitchell, 2008). It followshesia could be a result of direct, feedforward con-tween adjacent areas, especially for within-modalityor other kinds of synesthesia (e.g., between-modality),vable th

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