Neuroimaging and Electrophysiology of Word Recognition

Using positron emission tomography (PET), several stud-ies have identified a number of brain structures activatedduring language processing (Beauregard et al., 1997; De-monet et al., 1992; Frith, Friston, Liddle, & Frackowiak,1991; Frith, Kapur, Friston, Liddle, & Frackowiak, 1995;Petersen & Fiez, 1993; Petersen, Fox, Posner, Mintun, &Raichle, 1989; Petersen, Fox, Snyder, & Raichle, 1990;Wise et al., 1991; Zatorre, Meyer, Gjedde, & Evans, 1996).The tasks typically used in those studies required either visual processing of words and wordlike stimuli duringsilent reading or “phonetic” processing of words, syn-thetic syllables, pure tones, and clicks while listening tospeech. The activity elicited in these “low-level” processing stages was subtracted from that elicited when sub-jects were instructed to perform higher-level processingsuch as phonologic (e.g., reading aloud) or semantic(e.g., generating the verbs associated with presentednouns). Similar tasks were also used in functional mag-netic resonance imaging (fMRI) studies (e.g., McCarthy,Blamire, Rothman, Gruetter, & Shulman, 1993). Theseneuroimaging studies have contributed to locating brainareas involved in different aspects of processing wordsand word like stimuli, but they do not reveal the timecourse of the different types of brain activation. Therecording of the on-line electrophysiological manifesta-tions of the different levels of visual word processingmay provide information about the time course of those processes. Moreover, topographic analyses of the scalppotentials and of the current densities may provide con-verging information about brain regions activated at thedifferent processing levels.Several main families of ERP components associatedwith language processing have been described inthe electrophysiological literature. These families are represented by the N200, the N400, and the P600components. In the following brief review of the litera-ture, we will only address the first two of the abovecomponents, those elicited by the processing of singlewords.An N200 specific to orthographic stimuli was revealedin a study in which ERPs were recorded using intra-cranial implanted electrodes (Nobre, Allison, & McCarthy,1994). In this study the authors compared the ERPselicited by strings of letters with those elicited by othercomplex visual stimuli such as human faces. They foundthat although all the visual stimuli elicited negative com-ponents peaking around 200 msec from stimulus onset,the intracranial distribution of the N200 elicited by letterstrings (pronounceable words and pseudowords, andunpronounceable nonwords) was distinct from the dis-tribution of N200 elicited by nonorthographic stimuli.Both letter strings and faces elicited activity in theposterior fusiform gyrus, but the regions activated bythe two types of stimuli never overlapped within a sub-ject (Allison, McCarthy, Nobre, Puce, & Belger, 1994).Furthermore, the potentials elicited by words were morenegative in the left than in the right hemisphere,whereas those elicited by faces were either similaracross hemispheres or were more negative in the rightthan in the left. The fact that the intracranial N200 didnot distinguish between pronounceable and nonpro-nounceable letter strings indicates that this componentis elicited by a shallow-level process, one that is notaffected by phonology. On the other hand, the distinc-tion between the N200 distribution elicited by letterstrings compared to that elicited by other visual com-plex stimuli suggests that this component may by asso-ciated with a mechanisms of processing letters. Thusthere are data suggesting the existence of a visual mecha-nism tuned to process orthographic stimuli whose activ-ity is reflected by a negative component peaking around200 msec.Higher-level analysis of words seems to be associatedwith negative potentials peaking later than 200 msec(see reviews by Bentin, 1989; Hillyard & Kutas, 1983;Kutas & Van Petten, 1988). Among those, the most exten-sively investigated potential is the N400 component, firstdescribed by Kutas and Hillyard (1980). Initially, theN400 was linked with the processing of semanticallyanomalous words placed in final sentence positioneither in reading (Kutas & Hillyard, 1980) or in speechperception (McCallum, Farmer, & Pocock, 1984). It wasfound that its amplitude can be modulated by the degreeof expectancy (cloze probability) as well as by theamount of overlap between the semantic characteristicsof the expected and the actually presented words (Kutas,Lindamood, & Hillyard, 1984; see also Kutas & Hillyard,1989). Therefore, it was assumed to reflect a postlexicalprocess of semantic integration and to be modulated bythe difficulty of integrating the word into its sententialcontext (e.g., Rugg, 1990). Other studies, however, re-vealed that the N400 can also be elicited by isolatedprinted or spoken words and pseudowords presented insequential lists and modulated by semantic priming out-side the sentential context (Bentin, Kutas, & Hillyard,1993; Bentin, McCarthy, & Wood, 1985; Holcomb, 1986;Holcomb & Neville, 1990). Consequently, the semanticintegration process that may modulate the N400 hasbeen extended to include semantic priming betweensingle words. It is unlikely, however, that simple lexicalactivation is a major factor eliciting or modulating theN400 because closed-class words, although representedin the lexicon, neither elicit nor modulate this compo-nent (Nobre & McCarthy, 1994). Furthermore, unlike theletter-processing-specific N200, the N400 is not elicitedby letter strings that do not obey the rules of phonologyand cannot be pronounced (i.e., illegal nonwords).This pattern of results suggests that the N400 is notassociated with a visual mechanism dedicated to proc-essing of letters, but rather with a higher-level word-processing system. In particular, the absence of an N400in response to illegal nonwords suggests that it issensitive to the phonologic structure of the stimulus.However, it is probably not elicited by phonologicalprocessing per se because negative waveforms peakingat about 400 msec were modulated by the immediaterepetition of unfamiliar faces (Bentin & McCarthy, 1994)and other pictorial stimuli (Barrett & Rugg, 1989, 1990).Hence, the currently existing evidence indicates that theN400 is elicited only by stimuli that allow deep (se-mantic) processing and that its amplitude is enhancedby semantic incongruity and attenuated by semanticpriming and repetition. This pattern is consistent withthe assumption that the N400 reflects a link searchprocess between a stimulus and its semantic repre-sentation. It is possible, however, that different aspectsof semantic activity in general, and language comprehen-Bentin et al. 237sion processes in particular, are associated with differentnegativities elicited during the same time epoch. Thescalp distribution of the N400 may support this sugges-tion.The description of the N400 scalp distribution seemsto vary according to the task. Elicited by semantic incon-gruities in sentences, the N400 is largest over the cen-tro-parietal regions and slightly larger over the righthemisphere than over the left (Kutas & Hillyard, 1982;Kutas, Hillyard, & Gazzaniga, 1988). In contrast, whenelicited by single words, the N400 has a more anteriordistribution, with maxima over frontal or central sites(Bentin, 1987; Bentin, McCarthy, & Wood, 1985; McCarthy& Nobre, 1993) and a larger amplitude over the left thanover the right hemisphere (Nobre & McCarthy, 1994). Ina recent study, using intracranial ERP recordings,McCarthy, Nobre, Bentin, and Spencer (1995) found largemedio- and antero-temporal distributions of the N400,suggesting the existence of one, or several, deep neuralgenerators bilaterally distributed in the anterior medialtemporal lobe and associated with semantic processing.