Neural correlates of imagined and synaesthetic colours

Abstract

The experience of colour is a core element of human vision. Colours provide important symbolic and contextual information not conveyed by form alone. Moreover, the experience of colour can arise without external stimulation. For many people, visual memories are rich with colour imagery. In the unusual phenomenon of grapheme-colour synaesthesia, achromatic forms such as letters, words and numbers elicit vivid experiences of colour. Few studies, however, have examined the neural correlates of such internally generated colour experiences. We used functional magnetic resonance imaging (fMRI) to compare patterns of cortical activity for the perception of external coloured stimuli and internally generated colours in a group of grapheme-colour synaesthetes and matched non-synaesthetic controls. In a voluntary colour imagery task, both synaesthetes and non-synaesthetes made colour judgements on objects presented as grey scale photographs. In a synaesthetic colour task, we presented letters that elicited synaesthetic colours, and asked participants to perform a localisation task. We assessed the neural activity underpinning these two different forms of colour experience that occur in the absence of chromatic sensory input. In both synaesthetes and non-synaesthetes, voluntary colour imagery activated the colour-selective area, V4, in the right hemisphere. In contrast, the synaesthetic colour task resulted in unique activity for synaesthetes in the left medial lingual gyrus, an area previously implicated in tasks involving colour knowledge. Our data suggest that internally generated colour experiences recruit brain regions specialised for colour perception, with striking differences between voluntary colour imagery and synaesthetically induced colours.

Introduction

Colour perception is a fundamental aspect of human vision (Gegenfurtner & Sharpe, 1999). Although several neuroimaging studies have explored the involvement of early visual areas in visual imagery (e.g., D’Esposito et al., 1997; Kosslyn, Thompson, Kim, & Alpert, 1995; Kosslyn, Thompson, & Alpert, 1997; Mellet et al., 2000; Slotnick, Thompson, & Kosslyn, 2005), few investigations have specifically examined the neural correlates of colour imagery. Several areas in the ventral occipital cortex are active when participants view coloured stimuli, or perform colour-related cognitive tasks. These include area(s) in the posterior fusiform gyrus, most often called area V4 (Zeki, 1973, Zeki et al., 1991), and more medial ventral occipital regions that are active particularly during tasks that require retrieval of object-colour knowledge (Chao & Martin, 1999; Martin, Haxby, Lalonde, Wiggs, & Ungerleider, 1995; Price, Moore, Humphreys, Frackowiak, & Friston, 1996). Here, we used fMRI to examine neural activity in these regions in two distinct types of internally generated colour experience. First, we examined colour imagery by having participants imagine the colours of familiar objects. Second, we investigated the involuntary colour experiences that characterise the unusual phenomenon of grapheme-colour synaesthesia.

Individuals with grapheme-colour synaesthesia experience vivid sensations of colour when they see or hear particular letters or digits, and these experiences are highly consistent over time (e.g., Baron-Cohen, Wyke, & Binnie, 1987; Rich, Bradshaw, & Mattingley, 2005; Rich & Mattingley, 2002). Crucially, synaesthetic colours arise as an internally generated colour experience without voluntary effort, and are difficult to fully suppress even when there is a desire to do so (Dixon, Smilek, Cudahy, & Merikle, 2000; Mattingley, Rich, Yelland, & Bradshaw, 2001; Mills, Boteler, & Oliver, 1999; Odgaard, Flowers, & Bradman, 1999; Wollen & Ruggiero, 1983). Thus, grapheme-colour synaesthesia provides a unique opportunity to examine the neural correlates of an internally generated but involuntary colour experience.

The neuroanatomical loci of colour imagery remain controversial. A number of neuropsychological studies have documented an association between impairments of colour perception and deficits in colour imagery in patients with damage to the fusiform gyrus (for review, see Farah, 1988). Other authors, however, argue for a double dissociation between the two functions based on patients who seem to have intact imagery in the context of colour perception deficits or vice versa (for review, see Bartolomeo, 2002). Very few studies have explicitly examined the neural correlates of colour imagery in healthy individuals, and the data they have yielded are somewhat ambiguous. Howard et al. (1998) used fMRI to investigate brain activity during a colour imagery task. They presented non-synaesthetes with tasks that required them to imagine colour (e.g., to judge whether a canary is a darker yellow than a banana) or to imagine a set of spatial relations (e.g., to judge the relative angle between the hour and minute hands on a clock face showing “20 to 7”). Howard et al. found that although coloured stimuli elicited significant activity in the posterior fusiform gyrus, corresponding to area V4, colour imagery yielded no significant activity in the same region. It should be noted, however, that the authors used a whole-brain analysis, which may have reduced the likelihood of detecting a subtle change in V4 activity.

In a more recent study, Nunn et al. (2002) failed to find significant V4 activation in a group of non-synaesthetes trained on associations between coloured squares and spoken words. In their study, participants were asked to imagine the colour they had been trained to associate with each word, and then to estimate the percentage of colour associations they had correctly imagined. Unfortunately, Nunn et al. did not include an objective measure of their participants’ performance. Moreover, it is not possible to determine whether they were able to imagine the colours, or simply recalled the colour name associated with the spoken word. The same criticism holds for an earlier study using similar methodology (Goldenberg et al., 1989). The hypothesis that colour imagery recruits regions involved in colour perception therefore needs to be tested with a paradigm in which performance can be measured objectively, and in which participants must imagine colour, rather than merely recalling colour names.

There have also been a small number of studies investigating the neural correlates of involuntary colour experiences. Patients with Charles Bonnet syndrome, who experience visual hallucinations following peripheral visual pathology, show activity in the posterior fusiform gyrus for hallucinations that involve colour (Ffytche et al., 1998). For individuals with synaesthesia, who experience colours without chromatic stimulation in the absence of nervous system pathology, the findings of imaging studies have been mixed. Recent studies indicate that, at least in some individuals, area V4 is active during grapheme-colour synaesthesia. Sperling, Prvulovic, Linden, Singer, and Stirn (2006) found increased activity in retinotopically mapped V4 when synaesthetes viewed achromatic letters that induced involuntary colours relative to a condition with letters that did not induce coloured synaesthesia. This pattern was significant for two of the four synaesthetes when analysed individually. Similarly, Hubbard, Annan, Ramachandran, and Boynton (2005) reported that synaesthetes had greater V4 activity than controls for synaesthetic inducers relative to characters that did not induce synaesthesia. Activity in left V4 has also been documented in a late-blind synaesthete, with more anterior fusiform activation in the right hemisphere when the same participant was asked to imagine colours (Steven, Hansen, & Blakemore, 2006). Finally, Nunn et al. (2002) reported increased V4 activity when synaesthetes heard words that elicited colours compared with non-inducing tones. In contrast, other studies of synaesthesia have failed to find significant activation in colour-selective regions of cortex, and have instead documented activations in visual association cortex, including inferior temporal and inferior parietal areas (Paulesu et al., 1995; Weiss, Zilles, & Fink, 2005). These findings suggest that colour-selective areas of cortex are recruited during internally generated colour experiences, but that there may be differences between colour imagery on the one hand, and synaesthetic experiences on the other.

In the present study we used fMRI to characterise brain activation patterns associated with internally generated colour experiences in both synaesthetes and non-synaesthetic controls. We first identified regions in the ventral occipital cortex that responded selectively to colour by presenting large multicoloured rectangles (‘Mondrians’) in alternating blocks with grey-scale luminance equivalent stimuli (McKeefry & Zeki, 1997). Using the peak activations as centres for regions of interest (ROIs), we then analysed data within these regions from separate colour imagery and synaesthetic colour experiments to examine the neural correlates of these colour experiences in the absence of chromatic stimulation.

In one experiment, we had participants perform a colour imagery task, to examine the neural correlates of voluntarily generated colour experiences. Participants viewed greyscale photographs of pairs of objects that have a typical or ’canonical’ colour (e.g., a banana and a cob of corn; Fig. 1A). Participants were asked to judge which object, if seen in its natural chromatic form, would be darker in colour (colour imagery task); in a control condition they were asked to indicate which object would be larger in size (size baseline task). The colour imagery task was designed to maximise the likelihood that participants would voluntarily evoke colour images rather than simply drawing on stored verbal colour labels concerning familiar objects. Thus, for example, simply knowing that bananas are yellow should not help in determining whether they are a darker yellow than a cob of corn. The baseline task, on the other hand, was designed to require a similar judgement of a stimulus attribute that was not related to colour. We used identical pairs of pictures in the two tasks to ensure that any changes in brain activity could not be due to low-level luminance, intensity, contrast, or featural differences between stimuli.

In a second experiment, synaesthesia-inducing letters were presented either in the matching or ‘congruent’ colour for each synaesthete, or in shades of grey (‘achromatic’) equated for luminance. These conditions were compared with a baseline condition of greyscale placeholders (Fig. 2A). A group of sex-, age- and handedness-matched non-synaesthetes viewed the identical stimuli. Participants were required to detect the brief disappearance of one stimulus in the set of four presented in each display in a localisation task.

We hypothesized that if regions of the brain specialised for colour perception are also involved in colour imagery, both synaesthetes and controls should show significant activation within the ROIs defined by the colour localiser. Similarly, if synaesthetic colours recruit areas involved in colour perception, significant activation should be present within the same ROIs for synaesthetes, but not for controls, during presentation of achromatic letters.