The lexical processing of abstract and concrete nouns

Abstract

Recent activation studies have suggested different neural correlates for processing concrete and abstract words. However, the precise localization is far from being defined. One reason for the heterogeneity of these results could lie in the extreme variability of experimental paradigms, ranging from explicit semantic judgments to lexical decision tasks (auditory and/or visual). The present study explored the processing of abstract/concrete nouns by using repetitive Transcranial Magnetic Stimulation (rTMS) and a lexical decision paradigm in neurologically-unimpaired subjects. Four sites were investigated: left inferior frontal, bilaterally posterior-superior temporal and left posterior-inferior parietal. An interference on accuracy was found for abstract words when rTMS was applied over the left temporal site, while for concrete words accuracy decreased when rTMS was applied over the right temporal site. Accuracy for abstract words, but not for concrete words, decreased after frontal stimulation as compared to the sham condition. These results suggest that abstract lexical entries are stored in the posterior part of the left temporal superior gyrus and possibly in the left frontal inferior gyrus, while the regions involved in storing concrete items include the right temporal cortex. It cannot be excluded, however, that additional areas, not tested in this experiment, are involved in processing both, concrete and abstract nouns.

Introduction

A better performance with concrete as compared to abstract nouns (e.g., lexical decision is faster and recall is superior for concrete terms than abstract items) has been demonstrated in a number of psycholinguistic studies (for a review see Paivio, 1991), and is the rule in aphasia (e.g., Coltheart et al., 1980), although neuropsychological patients with a reversal of concreteness effect have been reported (Breedin et al., 1994, Macoir, 2008, Papagno et al., in press, Sirigu et al., 1991, Warrington, 1975, Warrington, 1981).

Two main models have been proposed to explain the concreteness effect. The dual-coding theory claims that the processing of abstract nouns relies on verbal code representations of the left cerebral hemisphere only, whereas concrete nouns additionally access a second image-based processing system eventually located in the right hemisphere (Paivio, 1991). The alternative model, the context availability theory (Schwanenflugel and Shoben, 1983), argues that the faster recognition of concrete vs. abstract nouns results from a larger contextual support of concrete words and not from a distinct non verbal system; this theory does not explicitly rule out a right hemisphere involvement, but attributes the concreteness effect purely to the access of more verbal information, which implies a predominantly left-hemisphere-based processing system. These theories assume a quantitative distinction between concrete and abstract concepts, but none of them can explain the presence of brain-damaged patients with a reversal of concreteness effect, i.e., a superiority of abstract concepts with respect to concrete ones. So far, a few single cases have been reported in the literature with poorer concrete than abstract concept knowledge (Breedin et al., 1994, Macoir, 2008, Marshall et al., 1996, Papagno et al., in press, Sirigu et al., 1991, Warrington, 1975, Warrington, 1981, Warrington and Shallice, 1984) (see Table 1), supporting however the view that concrete and abstract words are represented in a different qualitative way in the brain.

The association of a poorer performance with concrete than abstract concept with semantic dementia or herpes simplex encephalitis is striking. Both these pathological conditions systematically affect anterior temporal regions. Therefore, the anatomoclinical correlates of the reverse concreteness effect prompt considerations on the role of these regions in processing abstract and concrete terms.

Neuroimaging studies have produced inconsistent results on this topic, possibly because of the use of different experimental paradigms. Concrete, relative to abstract word processing produced greater activation in a bilateral network of associative areas, including temporal, parietal and prefrontal cortex, while processing of abstract words produced greater activation almost exclusively in the left superior temporal and inferior frontal cortex, using a semantic similarity judgment task on concrete and abstract noun triads (Sabsevitz et al., 2005), or synonymy judgments (Noppeney and Price, 2004). But semantic similarity judgment tasks also produced an area of greater activation on the left medial fusiform gyrus for concrete words, and a greater activation on the right medial fusiform gyrus for abstract words (e.g., Whatmough et al., 2004).

In the case of lexical decision, three studies, among others, report (i) a selective activation of the temporal pole and amygdala on the right, and of the inferior frontal cortex bilaterally for abstract word processing, while no brain areas were more active in response to concrete words (Perani et al., 1999), (ii) a significant area of activation in the right anterior temporal cortex for abstract words as compared to concrete stimuli, and a right posterior temporal lobe engagement during lexical decision for both abstract and concrete words, the statistical significance of the activation being greater for the abstract words (Kiehl et al., 1999); (iii) a bilateral activation of the angular gyrus and dorsal prefrontal cortex for auditory-presented concrete words and a left lateral temporal lobe activation for both types of words (Binder et al., 2005) (see Table 2).

Therefore, results differ even when the same type of task is used, possibly depending on the stimuli features, such as the degree of imageability: although concrete material is mostly imageable, abstract words present a high degree of variability within this dimension (Paivio, 1971). Response type can also have a relevant effect in semantic memory tasks with a significant interaction between response type and brain regional activation (Jennings et al., 1997).

To summarize, most (but not all) neuroimaging studies suggest a bilateral representation for concrete items, essentially involving several structures almost invariably including the fusiform gyrus, while abstract word representation is less defined, resulting either in a left, right, or bilateral activation.

Therefore, neither neuropsychological nor neuroimaging studies can prove the case conclusively: concerning anatomical lesions, one cannot exclude reorganization processes and compensatory strategies. In the case of neuroimaging studies, only correlations between brain and behaviour are indicated, but we do not know for sure that those areas are essential to normal task performance. In 2003, Fiebach and Friederici reviewed the literature on functional neuroimaging studies of abstract and concrete nouns and concluded that there is no evidence for a right hemispheric system specifically associated with concrete nouns, since there are more often right-lateralized peaks of activation associated with the processing of abstract than concrete words.

Given these premises, we sought to further explore and verify previous results by means of repetitive Transcranial Magnetic Stimulation (rTMS). Since it is an interventional technique to investigate causality in the brain–behaviour relationship, it has the advantage that it can be used to demonstrate not only that a brain region is active while a given task is performed, but also that the area is actually essential for task performance. In addition, it allows studying healthy subjects, eliminating the confounding effects of the diffuse impairment and compensatory cortical plasticity associated with brain lesions, and thus complementing neuropsychological studies. Finally, in studying healthy subjects we can use them as their own controls, thus increasing experimental power and retest reliability.