NEUROREPORTCOGNITIVE NEUROSCIENCE AND NEUROPSYCHOLOGYIs the N400 category-speci¢c?
A face and language processing study
Roberto Caldara,CA Francoise Jermann, Gabriela Lo¤pez Arango and Martial Van der Linden
F.P.S.E. University of Geneva, 40, bd du Pont d’Arve,1211Geneva 4, Switzerland
CA

Corresponding author: roberto.caldara@pse.unige.ch

Received 1 September 2004; accepted 11 October 2004

N400 event-related potential (ERP) components have been observed during semantic incongruity detection in language, face
identity and/or expression. However, it is still unclear whether semantic processing is functionally equivalent, since no study has directly investigated within the same participants the occurrence of
the N400s for language and faces. We recorded ERPs while subjects performed incongruity detection on words, facial identities
and facial expressions, with conditions matched to involve context

integration. N400s were identi¢ed on central-parietal electrodes
only for language and face identity processing. Scalp topographiesof these N400s di¡ered but a LORETA inverse solution identi¢ed acommon functional generator in the left lateral frontal cortex, suggesting a general role of this brain region in selecting and contextually integrating semantic information. NeuroReport15:2589^2593
c 2004 Lippincott Williams & Wilkins.

Key words: Event-related potentials; Face processing; Language processing; N170; N400; Source localization

INTRODUCTION
The N400 is an electrophysiological signature of semantic
processing that has been widely investigated in thelanguage domain (for review see [1]). This negative-going
ERP component is maximal over centro-parietal electrodesites and emerges about 250 ms after stimulus onset, with amaximum that peaks at around 400 ms post-stimulus. In theseminal study by Kutas and Hillyard [2], participantssilently read sentences which ended with a congruent or
an incongruent word. The N400 was larger for incongruent(e.g., the hen laid an oven) than for congruent words (e.g.,egg). The better the semantic fit between a word and its
context, the more reduced is the amplitude of the N400 [3].
N400-like components have also been identified for non
linguistic visual stimuli, especially for face processing, andrelated to general contextual integration [4,5], similar to the
linguistic N400 [5]. Several N400-like effects have beenfound during matching tasks in which participants had todecide whether or not two faces depicted the same identity[6] or the same facial expression [7–9]. N400-like components have been inconsistently observed only for identity ataround 350 ms in fronto-central sites [7], across all the scalp[6] or for identity and expression between 350 and 550 ms inparietal sites [9] or at around 400 ms but with different
topographies over the right temporal regions [8]. It is worth
noting that little is known about whether all the N400s,
enhanced during semantic incongruent information processing, elicit common or distinct neuroanatomical substrates
as a function of the visual category of the stimulus (words orfaces). Indeed, none of the reported studies could determine
the exact relationship between the N400 and the N400-like,as these components were not studied within the same
participants.

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The aim of this study is to unravel the precise nature andrelationship of the N400 components by exploring theiroccurrence among the same participants during language
and face processing, with the face tasks designed to involve
context integration in order to give the best match tosentence reading. Since differences between visual categories have been identified for the N170 component [10,11],
its time course for incongruity detection was also investigated. Finally, a LORETA inverse solution was applied todefine the neuronal substrates involved in all the conditions.

MATERIALS AND METHODS
Subjects: Fifteen right-handed native French speakers
voluntarily participate in the study, which was approvedby the ethical committee of the University of Geneva.
Stimuli and procedure: Participants performed a semantic
incongruity detection task with three conditions (word,
identity and expression).
Word stimuli: A total of 140 French congruent sequences(mean (7s.d.) length 7.571.5 words) were devised. The
mean frequency of the final words was 52 per million(Frantext database – http://www.atilf.fr) and their mean
length of letters was 6.271.9 with a cloze probability of 70%
or higher, covering a visual angle of B1.43  2.61. Semantic
incongruent sentences were obtained by randomizing thefinal words. All the sentences and final words werecounterbalanced and presented as congruent and incongruent trials across all the subjects.

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NEUROREPORT

R. CALDARA ETAL.

hen

The

+

300

500 300

+

an

+

egg
oven

Congruent word
Incongruent word

500 300500

300 ms

2.5 −3 slaid+

500 300

Incongruent emotion+

Congruentidentity and emotion+

Incongruent identity

300

500

300

500

300 ms

2.5 −3 s

Response
Fig. 1. Top: experimental design used for the word condition. Centre: experimental design used for the identity and expression conditions; congruency
depends on the instruction given (identity vs emotion incongruity detection).

Word incongruity detection condition: Participants silently
read 140 sentences (half congruent) presented one word at atime in black on a white background on a computer monitor
120 cm away. The final word appeared in red, indicating to
the subjects to decide whether or not the sentence wassemantically congruent (Fig. 1).
Face stimuli: Seventy unfamiliar face identities (35 female,
35 male) each posing with a neutral, happy and fearfulexpression (Karolinska Directed Expressional Faces set,
Lundqvist, D., Flykt, A. and Ohman, A., 1998) were used
for creating identity and expression incongruity detection
conditions in sequences of one by one face presentations:profile, three-quarter and full frontal views (Fig. 1). Externalfeatures (e.g. hair) were removed, and the images occupied
a visual angle of B4.29 2.621. Congruent sequences (n¼70)
consisted of the presentation of faces with the same identity
and the expression. In the incongruent identity list (n¼70), achange of identity, but not gender and expression, occurred
during full frontal face presentation. In the incongruent
expression list (n¼70), a change of expression, but not
identity, occurred during the full frontal face presentation.
The nature of the expression was counterbalanced acrosslists and conditions.
Identity and expression incongruity detection conditions:
For each full frontal face presentation, in their respective
condition, participants had either to decide whether the
depicted identity or the expression was congruent orincongruent with previous presented faces.
All the sequences were interleaved with a randomized
interval between 2 and 2.5 s during which a fixation cross
was presented on all trials.

2 59 0The order of the experimental conditions and the labels of
the keys (congruent or incongruent) used for the responses
were counterbalanced across subjects.
Behavioural analysis: Mean reaction times and the percentage of errors were statistically analysed using repeatedmeasures ANOVAs.
ERP recordings and analysis: EEG was continuously
recorded from 64 Ag/AgCl electrodes. A left mastoid
electrode was used as a reference. Ocular artefacts weremonitored and vertical blinks were corrected off-line by anautomatic algorithm. The recorded signal was low-passfiltered at 30 Hz and rescaled across the average reference.
EEG epochs were baseline corrected to the first 200 ms.
Finally, all the epochs resulting in a correct answer were
carefully scanned and remaining artefacts were rejected
before being averaged to give individual and grand-mean
ERPs.
In order to investigate the N400, the electrode showing
the largest effect for the language condition was selected
and repeated measures ANOVAs were performed, for time
windows of 50 ms each, on the amplitude with condition(word, identity vs expression) and semantic congruency(congruent vs incongruent) as factors. The N170 component
was investigated by analyzing ERP peak amplitudes andlatencies on the P7 and P8 occipito-temporal electrode sites
between 140 and 190 ms. A repeated measures ANOVA was
performed with condition (word, identity vs expression)and semantic congruency (congruent vs incongruent) andhemisphere (left vs right) as factors.
Greenhouse-Geisser adjusted degrees of freedom arereported.

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NEUROREPORTSPECIFICITY OF THE N400

Table 1. Mean (7s.e.) reaction times and percentage of errors for all the conditions.
Word

Reaction times
ErrorsIdentity

Expression

Congruent

Incongruent

Congruent

Incongruent

Congruent

Incongruent

777 (47)
0.55 (0.2)

822 (50)
0.55 (0.2)

628 (41)
3.9 (1.15)

836 (46)
26 (2.3)

719 (33)
1.5 (0.3)806 (36)
9.1 (1.5)

Congruent
Incongruent
CP4

Word
(µV)

4

N400

N400

2
0

−2

Identity
(µV)

N400

2 µV

N400

4

1µV

2
0
−3µV

−2

−1µV

Expression
(µV)

4
2
0
Incongruent−

Congruent=

N400

LORETA

0
50
10
150
0
20
25 0
0
30
350
0
40
0
45
0
50
0

−2
ms

Fig. 2. Left: grand-averaged ERP waveforms recorded at centro-parietal electrode (CP4) in response to word, identity and expression processing.
Positive values are up. Centre: map topographies from 300^ 400 ms for all the conditions and their subtraction. Right: 3D brain activity estimated forthe surface maps. Solutions are represented in eight transverse slices through the spherical head model with the lowest slices to the left (nose up, left earleft).

Source localization: To estimate the brain activity underlying the ERP signal, inverse solutions were calculated withLORETA [12].

RESULTS
Behavioural results: Mean reaction times and the percentage of errors for each condition are shown in Table 1.
Statistical analysis revealed a significant effect of thesemantic congruency factor (F(1,14)¼32.37, po0.001): congruent trials were faster processed than the incongruent
trials. A significant interaction effect was also found(F(1.34,18.76)¼11.52, po0.001), showing faster processing
for the identity in the congruent situations. Regarding thepercentage of errors, a significant interaction was foundbetween the conditions and the semantic congruency(F(1.58,22.24)¼45.67, po0.001). Identity and expression
conditions induced more errors than words, especially in
the incongruent situations.
ERPs: Figure 2 shows the time course of the N400 on theright centro-parietal electrode (CP4) as well as the topo-

graphies and source localizations for all the conditions.
Repeated measures ANOVAs were performed on four time
windows of 50 ms each, going from 250 to 450 ms. Semantic
incongruity elicited larger negativities over all these time
periods (po0.01 at least) and no significant differences wereobserved for the condition as factor. Crucially, however,significant interactions between conditions and semantic
congruency were found in two time windows, going from
300 to 350 ms (F(1.94,27.2)¼5.53, po0.01) and 350 to 400 ms(F(1.73,24.3)¼3.76, po0.05). Post-hoc analysis revealed that
this effect was present only for the word and face identity
conditions (po0.001). For the word condition, LORETA
localized the generators of electrophysiological incongruities in the left lateral frontal cortex. Detection of face identity
incongruities involved a more distributed region on the left
frontal cortex, accompanied by a right occipito-temporal
activity. For face expression, the greatest activity wasobserved in the right occipito-temporal region rather thanin the left frontal cortex.
The time course of the N170 component is reported in
Figure 3. A significant interaction was found between thecondition and electrodes (F(1.35,19.01)¼26.84, po0.001),

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NEUROREPORT

R. CALDARA ETAL.

Word incongruent
Identity congruent
Expression incongruent

Word congruent
Identity incongruent
Expression congruent

P8

P7
8

8

6

6

4

4

2

2
(µV)

(µV)

Word

0

2 µV
Identity

0

−2

−2

−4

−4

−6

−6

−2 µV

Expression
0

50 100 150 200 250 300
ms

050 100 150 200 250 300
ms

LORETA

Fig. 3. Left: grand-averaged ERP waveforms for the N170 component recorded at lateral temporo-occipital electrodes (P7 and P8) in response to word,
identity and expression. Positive values are up. Middle: map topographies from 140 to 190 ms for the congruent conditions only. Right: 3D brain activity
estimated between140 and190 ms. Solutions are represented in eight transverse slices through the spherical head model with the lowest slices to the left
(nose up, left ear left).

words eliciting a larger negativity on the left (7.25 m vs
3.9 m for faces) and faces on the right hemisphere (4.9 m
vs 3.35 m for words). A trend was observed for the sameinteraction on latencies (F(1.31,18.47)¼2.57, p¼0.094). In thistime period, LORETA identified bilateral generators in theoccipito-temporal regions, dominant in the right hemisphere
for face conditions, and only a left unilateral source in thesame region for words.

DISCUSSION
Behavioural results showed that congruent detections areprocessed faster than incongruent detections for all conditions. Word processing induced considerably less errors
than face processing, with face identity being the moredifficult condition [5,9]. Recognition of unfamiliar faces
relies mainly on the external features [13], removing suchfacial information increased the difficulty for the identity
condition and provide an explanation of the observed
results.
Regarding ERPs, three important results were established.
First, a classical N400 was identified between 300 and
400 ms at the central-parietal sites during semantic incongruity detection in the word condition [1–3]. In the same
period and location, a N400 component was also identified
for identity [5,7,9], but not in the expression condition [7]. It
is worth noting that using unfamiliar faces did not influence
the occurrence of the N400 for incongruent identities [6,8].
These observations provide direct evidence that thiscomponent is not category-specific (words vs faces), butinstead condition-specific (word and identity vs expression).
Scalp topographies of the N400s and LORETA source
localizations refined these observations at the functional
level. LORETA identified an activity in the left lateral frontal
cortex (lFC) for the N400 elicited in the word condition. A

2 59 2

recent fMRI study [14] identified an increase of the
responses in the left inferior frontal gyrus (lIFG), a region
within the lFC, for semantic incongruities occurring on thelast word of a sentence. Thus, a critical contribution of thelIFG [14], within the lFC activity defined by LORETA, can beinferred. For face Identity condition LORETA identified awidespread activity over the lFC, in line with fMRI studies
on face working memory tasks showing left prefrontal [15]or frontal [16] activations accompanied by face-sensitive
responses [15] in the fusiform face area (FFA) [17]. Crucially,
the lFC was activated in both of our ERP conditions. The
functional role of the left prefrontal cortex for faces [15] orlanguage (for review see [18]) has been related in selecting
semantic knowledge from a set of alternatives. Thus, ourfindings posit the lFC as a critical candidate in controllingand integrating semantic information independently of thevisual category at hand (words or faces) during context
integration.
Second, critically, the lFC was sensitive to the nature of
the handled information (word, identity vs expression),since only weak activations of the lFC and no enhanced
N400 were observed for face expression incongruity. Thisfinding confirms that identity and expression processing aresubserved by different neural pathways [7,9], and indicatethat expression incongruity detections take part in otherregions of the brain, most likely in the amygdala, a structure
highly involved in emotion processing (for recent review see[19]). However, because the activations arising from theamygdala are not directly recordable with the ERP
technique, future fMRI studies are planned to define where
expression incongruity detection occurs in the brain.
Third, regarding the category-specific N170 component,
no differences between the conditions were found for thedetection of incongruities at the semantic level. However, inline with recent findings [11], the N170 component was

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SPECIFICITY OF THE N400

larger on the right hemisphere for the faces, and in the left
for the words, suggesting a functional difference between
these categories during this time period. LORETA inverse
solution refined these findings by defining a bilateralpattern of activity in the FFA regions for faces [10], with aright hemisphere advantage. For words, a unilateral sourceof activation in the left part of the occipito-temporal cortex
was observed [11,20]. These findings complete the knowledge, established by using the LORETA algorithm, of theneuronal structures engaged in this critical time period ofhigh-level visual categories processing (for a detailed review
on faces and objects see [10]).

CONCLUSION
Larger N400s, but with different topographies, were evokedfor incongruent trials during language and face identity
processing. Such enhanced negativities were absent for
facial expressions processing. Although the N400 for words
and faces elicited distinct semantic pathways, they recruited
a common generator in the left lateral frontal cortex,
reflecting a functional involvement of this brain region in
selecting and integrating information at the semantic level.
Altogether, these observations indicate that the N400s are
sensitive to the nature of semantic information processing,rather than the visual categories per se.

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Acknowledgements: R.C. is currently supported by a post-doctoral fellowship provided by the Swiss National Science Foundation.
We would like to thank Anders Flykt for access to the face stimuli and Denis Brunet for his ERPs analysis software: CarTool.

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