In this study, we investigated the neural representation underlying the visual recognition of letters and numbers by directly contrasting neural activation patterns elicited by letters and numbers. In Experiment 1, we found letter-preferred activity in the left occipito-temporal cortex and number-preferred activity in the right occipito-temporal cortex at the group level (). In Experiment 2, we demonstrated that individual differences in the cerebral lateralization of number-preferred activity in visual cortex could be explained by individual differences in the lateralization of numerical processing in parietal cortex ().
Left-lateralized letter-preferred activity in ventral visual cortex is consistent with reports showing robust and reproducible neural activation in left occipito-temporal cortex in response to words and letters (Polk et al., 2002
; Cohen et al., 2000
; Polk & Farah, 1998
; Puce et al., 1996
; Petersen, Fox, Snyder, & Raichle, 1990
). What is more novel in the results from Experiment 1 is the neural dissociation of numbers from letters: The number versus letter contrast produced significant activation in right lateral occipital cortex at the group level.
The identification of this neural double dissociation and the right-lateralized number-preferred activity are important for at least three reasons. First, the double dissociation rules out alternative explanations that assume that the observed letter-preferred or number-preferred neural activity is an artifact of difficulty or effort. Second, the neural dissociation between letters and numbers is consistent with previously reported behavioral double dissociations (Hamilton et al., 2006
; Jonides & Gleitman, 1972
), providing further evidence of experience-dependent changes in the neural architecture underlying visual recognition. Third, the fact that number-preferred activity was localized in the right occipito-temporal region is problematic for the “interhemispheric differences hypothesis,” which assumes that letter and word recognition is localized in the left hemisphere because of that hemisphere’s superiority in processing fine-grained and local visual features (see Robertson & Lamb, 1991
, for a review). That hypothesis would predict that numbers should also be processed primarily in the left hemisphere given that they also involve processing fine-grained and local visual features.
We also observed individual differences in the lateralization of neural representations for visual and numerical processing, which is a topic that has not yet received much attention. A few studies have reported different patterns of functional cerebral asymmetries between right- and left-handed subjects in the domain of vision. For example, as described in the Introduction, Cai et al. (2008)
studied the relationship between cerebral lateralization of VWFA and anterior language processing sites in right- and left-handed subjects. A recent neuroimaging study has also reported that cerebral lateralization for the fusiform face area and the extrastriate body area was coupled with handedness (Willems, Peelen, & Hagoort, 2010
). Of course, all of our participants were right-handed, so the individual differences in lateralization that we observed cannot be attributed to differences in handedness.
The visual processing of numbers has also received relatively little attention in the literature. Besides a previous study by Polk et al. (2002)
, Arabic digits have typically been used as control stimuli when looking for letter- and word-specific neural activity (Reinke et al., 2008
; Baker et al., 2007
; James et al., 2005
) or have been compared with verbal numerals when looking for notation effects in number processing (Pinel, Dehaene, Riviere, & LeBihan, 2001
; Pinel et al., 1999
; Dehaene, 1996
). Here, we extended the work by Polk et al. (2002)
and found significant neural activation in response to numbers compared with letters in right visual cortex.
The observed neural dissociation between letters and numbers is noteworthy given that the distinction between letters and numbers is culturally defined and in some sense arbitrary. How might such a dissociation emerge? Polk and Farah (1995
) proposed a bottom–up model on the basis of a co-occurrence hypothesis. According to this model, letter and number recognition become differentiated because letters tend to co-occur with letters (and numbers with numbers) in the environment. Correlation-based learning mechanisms in the brain are assumed to pick up on these co-occurrence patterns to lead to neural segregation (Polk & Farah, 1995
). Although this purely bottom–up hypothesis is plausible for the neural dissociation of letters and numbers, it does not predict why the VWFA consistently forms in the left hemisphere rather than the right (or why number recognition tends to be right-lateralized).
According to the neuronal recycling hypothesis (Dehaene & Cohen, 2007
), one of the reasons that VWFA tends to develop in the left occipito-temporal cortex is because this area has relatively direct connections to and from anterior language processing sites in the left hemisphere (McCandliss et al., 2003
). Consistent with this view, the pattern of activation in VWFA is closely related to components of language-related functions. For instance, it is invariant to letter case (Dehaene et al., 2004
; Polk & Farah, 2002
; Dehaene et al., 2001
) and is greater when the orthographic stimuli are familiar to subjects than when they are unfamiliar (i.e., Hebrew to Hebrew readers vs. to non-Hebrew readers; Baker et al., 2007
). Activation in VWFA is hierarchically organized so that the strength of activation increases with orthographic regularities (Vinckier et al., 2007
) and bigram frequency (Binder, Medler, Westbury, Liebenthal, & Buchanan, 2006
). As noted, it has been shown that VWFA is right-lateralized in a subsample of left-handed subjects who showed right-lateralized language sites (Cai et al., 2008
Our findings support another aspect of this hypothesis in the numerical cognition framework. We found that individual differences in the lateralization of numerical processing in the parietal cortex predicted the lateralization of the visual Arabic number form processing in visual cortex. These results are consistent with the hypothesis that top–down influences from parietal numerical activity play an important role in the neural localization of number recognition in ventral visual cortex.2
To conclude, the current findings demonstrate a neural double dissociation between letter and number recognition and suggest that top–down influences play an important role in experience-dependent neural reorganization.