Elsevier

Neuropsychologia

Volume 51, Issue 10, August 2013, Pages 1802-1813
Neuropsychologia

Real color captures attention and overrides spatial cues in grapheme-color synesthetes but not in controls

https://doi.org/10.1016/j.neuropsychologia.2013.06.024Get rights and content

Highlights

  • We investigated inhibition and attention in synesthesia using alpha oscillations.

  • Color leads to a location-specific allocation of attention in synesthetes.

  • Attentional capture of color was confirmed by alpha lateralization and RTs.

  • Attentional capture could explain color-to-grapheme binding during development.

Abstract

Grapheme-color synesthetes perceive color when reading letters or digits. We investigated oscillatory brain signals of synesthetes vs. controls using magnetoencephalography. Brain oscillations specifically in the alpha band (∼10 Hz) have two interesting features: alpha has been linked to inhibitory processes and can act as a marker for attention. The possible role of reduced inhibition as an underlying cause of synesthesia, as well as the precise role of attention in synesthesia is widely discussed.

To assess alpha power effects due to synesthesia, synesthetes as well as matched controls viewed synesthesia-inducing graphemes, colored control graphemes, and non-colored control graphemes while brain activity was recorded. Subjects had to report a color change at the end of each trial which allowed us to assess the strength of synesthesia in each synesthete.

Since color (synesthetic or real) might allocate attention we also included an attentional cue in our paradigm which could direct covert attention. In controls the attentional cue always caused a lateralization of alpha power with a contralateral decrease and ipsilateral alpha increase over occipital sensors. In synesthetes, however, the influence of the cue was overruled by color: independent of the attentional cue, alpha power decreased contralateral to the color (synesthetic or real). This indicates that in synesthetes color guides attention. This was confirmed by reaction time effects due to color, i.e. faster RTs for the color side independent of the cue. Finally, the stronger the observed color dependent alpha lateralization, the stronger was the manifestation of synesthesia as measured by congruency effects of synesthetic colors on RTs.

Behavioral and imaging results indicate that color induces a location-specific, automatic shift of attention towards color in synesthetes but not in controls. We hypothesize that this mechanism can facilitate coupling of grapheme and color during the development of synesthesia.

Introduction

In people with grapheme–color synesthesia, the percept of a specific letter or digit causes the additional experience of color, e.g. the letter J might elicit the color orange. The color percept is automatic, involuntary, and idiosyncratic (stable over time) (e.g. Baron-Cohen et al., 1987, Wollen and Ruggiero, 1983). In grapheme–color synesthetes, brain activity to achromatic graphemes is enhanced in visual color area V4 (Hubbard et al., 2005, Sperling et al., 2006, van Leeuwen et al., 2010) and in superior parietal cortex (Esterman et al., 2006, Weiss et al., 2005). In superior parietal cortex, information from different modalities is integrated (Corbetta et al., 1995, Robertson, 2003). Aberrant cross-activation of color area V4 to grapheme and/or parietal areas is proposed to underlie synesthetic color experience.

At least two possible mechanisms of cross-activation have been discussed. The cross-wiring hypothesis proposes that increased anatomical connections between the grapheme area and color area in ventral-occipital cortex might lead to an aberrant cross-activation between these brain areas (Brang et al., 2010, Ramachandran and Hubbard, 2001a, Ramachandran and Hubbard, 2001b, Rouw and Scholte, 2007). Alternatively, the disinhibition model (Grossenbacher & Lovelace, 2001) proposes functional changes in inhibition as a mechanism of synesthesia: after the combination of information in higher-order areas such as parietal lobe, feedback signals to lower sensory areas are disinhibited, leading to aberrant activation of color area V4. Evidence exists for both mechanisms. E.g. diffusion tensor imaging and voxel-based morphometry analyses have revealed anatomical differences in the synesthetes’ brains, supporting the cross-wiring theory (Jäncke et al., 2009, Rouw and Scholte, 2007, Rouw and Scholte, 2010, Weiss and Fink, 2009). However, synesthesia can be induced in non-synesthetes by training, posthypnotic suggestion or the application of drugs (Aghajanian and Marek, 1999, Cohen Kadosh et al., 2009, Hartman and Hollister, 1963, Meier and Rothen, 2009), suggesting that no abnormal anatomical connections are required to elicit synesthesia. Also, synesthetic experiences often resemble normal cross-modal associations (Bien et al., 2012, Cohen Kadosh et al., 2007, Sagiv et al., 2006, Ward et al., 2006), supporting the view that existing connections are functionally altered. In this paper, we address the question whether altered inhibitory processes may underlie synesthesia, using oscillatory activity in the brain as a marker for inhibition.

A second unsolved question is the role of attention in synesthetic percept. There is an ongoing discussion whether overt attention to the grapheme is necessary to elicit synesthesia or not. Behavioral studies have shown that synesthetic color can increase the efficiency of visual search tasks (Carriere et al., 2009, Palmeri et al., 2002, Ramachandran and Hubbard, 2001a, Smilek et al., 2003, Ward et al., 2010), but this result has not been replicated in all cases (Edquist et al., 2006, Rothen and Meier, 2009). Full attention does not seem to be necessary to elicit synesthesia (Rich & Mattingley, 2003), however, true (pre-attentional) pop-out effects have not been reported. In the current study, we investigate the physiological underpinnings of attentional processes in synesthesia, aiming to see whether synesthesia requires full attention or not.

Brain oscillations specifically in the alpha band (∼10 Hz) as described by Berger (Berger, 1929) have two interesting features which might help to answer our questions: alpha power can act as a marker for attention and additionally has been linked to inhibitory processes. Alpha power is strongly modulated by attention showing a decrease in alpha power in areas that process the attended input and a power increase in areas that process distracting input (task-irrelevant areas). This has been observed in visual, auditory and somatosensory domains (Foxe et al., 1998, Fu et al., 2001, Haegens et al., 2010, Jensen et al., 2002, Jokisch and Jensen, 2007, Kelly et al., 2006, Rihs et al., 2007, Van Dijk et al., 2010, Worden et al., 2000, Yamagishi et al., 2003). Additionally, within one attentional state, alpha power is negatively correlated with perception. Low prestimulus alpha activity in visual areas is associated with good perceptual performance and fast reaction times to visual detection tasks, and vice versa (Ergenoglu et al., 2004, Hanslmayr et al., 2007, Thut et al., 2006, Van Dijk et al., 2008, Zhang et al., 2008). Such increases and decreases in alpha power seem actively controlled in order to follow the demands of the task at hand (Haegens et al., 2011, Händel et al., 2011). The fact that a task is solved better if alpha oscillations are high in task irrelevant areas but low in task relevant areas leads to the belief that alpha reflects active inhibition of task-irrelevant regions and active disinhibition of task-relevant areas (Klimesch, Sauseng, & Hanslmayr, 2007).

The disinhibition theory of synesthesia predicts that in synesthetes, alpha power would be decreased, reflecting reduced inhibition. Importantly, this decrease in alpha power should occur specifically for synesthesia-inducing stimuli. Besides testing this clear prediction, we further investigated the role of attention in synesthesia. Alpha lateralization can indicate the attentional allocation providing a tool to investigate attention during synesthetic color percept.

We measured the oscillatory brain activity of synesthetes and matched controls with magnetoencephalography (MEG). An attentional cueing task to assess attentional processes was combined with a color decision task (synesthetic Stroop task, Wollen & Ruggiero, 1983) to assess behavioral effects of synesthesia and attention. Using alpha power as an indicator of inhibitory activity, we investigated whether synesthetes show any decreases in alpha power specifically for synesthesia-inducing stimuli. We further assessed whether there were any global or color-related differences in inhibitory processes for synesthetes compared to controls. Additionally, we investigated the attentional allocation during percept of non-colored, colored, and synesthesia-inducing graphemes.

Section snippets

Participants

Eleven grapheme-color synesthetes (9 female, mean age 27 years (SD=3.8 years), 2 left-handed) and 11 controls matched on age, handedness and educational level (8 female, mean age 25 years (SD=4.1 years), 2 left-handed) participated in the study. The mean ages of the two groups did not differ (t(10)=1.687, n.s.). Developmental synesthesia was established by means of an extensive questionnaire on the synesthetes’ experiences similar to the procedure in van Leeuwen, Petersson, & Hagoort (2010). In

Behavioral results

Reaction times (RTs) from all 22 participants (11 synesthetes, 11 controls) were entered into analyses of variance (ANOVA). Misses amounted to 2.4% (SD=4.8%) of trials for synesthetes, and 3.2% (SD=3.1%) for controls (no group difference, t(20)=−0.476, n.s.). Outliers were removed prior to analysis by removing all RTs that were faster than 250 ms or slower than 2000 ms (synesthetes, 1.9%; controls, 0.4%, no group difference, t(20)=0.906, n.s.). Only correct responses were included in the analyses.

Discussion

This study addressed the effect of real and synesthetic colored graphemes in comparison to non-colored graphemes in synesthetes vs. controls focusing on behavioral responses as well as alpha oscillations using MEG. This paper demonstrates that both these measures (RT and alpha power) are affected differently by color percept in synesthetes vs. controls. Below we will discuss a common interpretation of our neural and behavioral findings.

The alpha inhibition theory interprets alpha power

Acknowledgements

This work was supported by the Volkswagen-Foundation [grant number I/80743]. We would like to thank Jason Chan and Ayelet Landau for comments on the manuscript.

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