Neuropsychologia 42 (2003) 14–24

Brain activity during intra- and cross-modal priming:

new empirical data and review of the literature
G. A. Carlesimo a,b,∗ , P. Turriziani b , E. Paulesu c , A. Gorini e ,
C. Caltagirone a,b , F. Fazio d , D. Perani d,e
a Clinica Neurologica, Università Tor Vergata, Rome, Italy
bIRCCS S. Lucia, V. Ardeatina, 306, 00179 Rome, Italy
c Università Milano-Bicocca, Milan, Italy
d INB-CNR, Milan, Italy
e Università Vita-Salute HSR, Milan, Italy

Received 2 September 2002; received in revised form 19 June 2003; accepted 19 June 2003

Abstract
A positron emission tomography (PET) study was conducted to investigate the neurofunctional correlate of auditory within-modality
and auditory-to-visual cross-modality stem completion priming. Compared to the auditory-to-auditory priming condition, cross-modality
priming was associated with a significantly larger regional cerebral blood flow (rCBF) decrease at the boundary between left inferior temporal
and fusiform gyri, brain regions previously associated with modality independent lexical retrieval and reading. Instead, within-modality
auditory priming was associated with a bilateral pattern of prefrontal rCBF increase. This was likely the expression of more efficient access
to output lexical representations and involuntary retrieval of the recent episode during which the just generated word had been encountered.
© 2003 Elsevier Ltd. All rights reserved.
Keywords: Priming; Stem completion; Memory; PET

1. Introduction The reliance of repetition priming on a different memory

Repetition priming is a form of implicit memory that typ-
ically manifests as a facilitation in re-processing recently
experienced stimuli or as a bias in completing fragments
with recently encountered items when test instructions do
not make any reference to prior events. In most cases, the
magnitude of the priming effect is larger when the same
modality of stimulus presentation is used for study and test-
ing than when it differs (Graf, Mandler, & Haden, 1982).
This supports a prevalent role of facilitated perceptual pro-
cessing at the origin of the priming phenomenon (Tulving &
Schacter, 1990). However, significant cross-modality prim-
ing (i.e. facilitated re-processing of items previously expe-
rienced in a different modality) is also commonly observed
(Graf, Shimamura, & Squire, 1985), suggesting the partici-
pation of more abstract levels of memory representation in
the emergence of the priming effect.
∗ Corresponding author. Tel.: +39-06-5150-1517;
fax: +39-06-5150-1584.
E-mail address: memolab@hsantalucia.it (G.A. Carlesimo).
system from that involved in the deliberate recollection
of episodic memories has been hypothesised on the basis
of neuropsychological evidence of a dissociation between
the two forms of memory in pure amnesic patients. These
patients (with mesio-temporal or diencephalic damage)
generally show normal repetition priming levels despite
severely impaired performances on episodic memory tasks
(Graf, Squire, & Mandler, 1984). The opposite dissociation,
i.e. poor repetition priming (at least for visually presented
words) but normal performance on episodic memory tests,
has also been described in a patient with bilateral occip-
ital lobe lesions (Keane, Gabrieli, Mapstone, Johnson, &
Corkin, 1995).
The positron emission tomography (PET) technique has
been mostly used to investigate the neural substrate of
verbal repetition priming (for a review, see Schacter &
Buckner (1998)). Stem completion has been the most fre-
quently used repetition priming procedure in these studies.
In a typical stem completion paradigm, subjects are first
exposed to a list of words. After a short delay, they are
presented with a list of two- or three-letter stems and are re-
quested to complete them with the first words that come to

0028-3932/$ – see front matter © 2003 Elsevier Ltd. All rights reserved.
doi:10.1016/S0028-3932(03)00148-9
 G.A. Carlesimo et al. / Neuropsychologia 42 (2003) 14–24
mind. The priming effect is demonstrated by a bias in com-
pleting the stems with the words of the previously studied
list rather than with unstudied words. Early PET studies in-
vestigated stem completion priming in a condition in which
both words in the study phase and stems in the test phase
were presented visually (within-modality visual priming).
The most consistently replicated finding in these studies is
a decrease in regional cerebral blood flow (rCBF) in the
occipito-temporal extrastriate cortex, more frequently in the
right hemisphere, when subjects were completing stems of
previously studied words as compared to the condition in
which they were completing stems of previously unstudied
words (Backman et al., 1997; Buckner, Koutstaal, Schacter,
& Rosen, 2000; Schacter, Alpert, Savage, Rauch, &
Albert, 1996; Schacter, Badgaiyan, & Alpert, 1999; Yasuno
et al., 2000). The peaks of rCBF suppression associated
with priming in these studies generally do not involve the
striate and extrastriate visual cortex (V1, V2 and V3) but
are localised in the proximity of higher level retinotopic or
“fringe” retinotopic cortical areas such as the V4 and V8
regions (Tootell, Hadjikhani, Mendola, Marrett, & Dale,
1998). More frequently, the foci of activity suppression are
located in the fusiform and inferior temporal gyri, which lie
at the convergence of retinotopically organised visual areas,
and whose neural activity related to visuo-verbal stimuli has
been found invariant across receptive fields (Tootell et al.,
1998). The finding of priming-related rCBF suppression in
cortical areas known to be involved in visual processing
has been generally interpreted as a manifestation of the
reduced neural activity needed to reprocess recently seen
words compared to unseen words (Wiggs & Martin, 1998).
Interestingly, this pattern of metabolic suppression related
to verbal priming agrees with what emerges from studies of
repetition priming evoked by repeated presentations of pic-
tures. In some of these studies, significant deactivations in
occipito-temporal retinotopic visual areas anterior to regions
V1, V2 and V3 (Tootell et al., 1998) or in the fusiform gyrus
(Henson, Shallice, & Dolan, 2000) have also been reported.
More recent PET investigation has been concerned with
the neurofunctional correlate of within-modality auditory
priming. In two studies (Badgaiyan, Schacter, & Alpert,
1999; Badgaiyan, Schacter, & Alpert, 2001), healthy sub-
jects first listened to a word list and were then scanned while
trying to complete auditorily presented three-letter stems
with the first words that came to mind. Quite surprisingly, the
PET correlate of the priming effect in these studies was also
an rCBF decrease in extrastriate cortical visual areas (BA
19). It was bilateral in the first study (Badgaiyan et al., 1999)
and confined to the left side in the second study (Badgaiyan
et al., 2001). No analogous priming-related rCBF decrease
was detected in cortical areas in superior and middle tempo-
ral gyri (BAs 21 and 22) known to be involved in the audi-
tory processing of language (Price et al., 1996). Moreover,
a number of foci with significant priming-related deactiva-
tions were found in the prefrontal regions bilaterally (BAs
9 and 10).
15
Finally, three studies investigated the neurofunctional cor-
relate of cross-modality verbal priming. In the first study
(Badgaiyan et al., 1999), subjects were visually presented
with a word list during the pre-scanning study phase and
were then scanned while trying to complete auditorily pre-
sented stems. In the other two studies (Badgaiyan et al.,
2001; Schacter et al., 1999), the experimental design for
evoking cross-modality priming was reversed by present-
ing the word list auditorily during the study phase and the
stems visually during the PET scanning phase. In strik-
ing contrast with within-modality priming experiments, in
which the PET correlate was mainly a pattern of rCBF
decreases, cross-modality priming was consistently associ-
ated with rCBF increase in prefrontal cortical areas (BAs
9 and 10) of the right (Badgaiyan et al., 2001; Schacter
et al., 1999) or the left (Badgaiyan et al., 1999) hemisphere.
Badgaiyan et al. (1999) and Schacter et al. (1999), but not
Badgaiyan et al. (2001), also reported an area of signifi-
cant rCBF decrease related to cross-modality priming in the
parieto-temporal cortex (BAs 39/40 and 39/22). According
to these authors, the frontal pattern of cortical activation is
likely an expression of contamination of the repetition prim-
ing procedure by explicit strategies of memory retrieval. In
fact, there is usually agreement that deliberate retrieval of
episodic memories is associated with an rCBF increase in
prefrontal cortical areas, mainly on the right side (see Cabeza
& Nyberg (2000) for a review). On the other hand, the incon-
sistently reported rCBF decrease in the temporo-parietal cor-
tex has been interpreted as the expression of priming-related
facilitation in some aspect of phonological or lexical pro-
cessing (Badgaiyan et al., 1999; Schacter et al., 1999).
Here, we report the results of an experiment with PET in
which healthy subjects performed an auditory or a visual
stem completion. Since the word-lists were always pre-
sented auditorily during the pre-scanning study phase, two
main experimental conditions were created: (a) auditory-to-
auditory within-modality priming, (b) auditory-to-visual
cross-modality priming. Our aim was to investigate the neu-
rofunctional correlate of the priming effect when it could
be subsumed (at least partially) by a facilitated perceptual
level of auditory stimulus analysis or when it necessarily
relied on a more abstract level of lexical representation.
2. Methods
2.1. Subjects
The experimental protocol was approved by the Ethics
Committee of the Scientific Institute H San Raffaele (Milan)
and IRCCS S. Lucia (Rome). Informed written consent was
obtained from all participants prior to the study. The exper-
iment was conducted with Italian speaking volunteers who
were right-handed as assessed by the Edinburgh handedness
inventory (Oldfield, 1971). Eight male college students (age
range: 20–27) participated in the study. All subjects had
16 G.A. Carlesimo et al. / Neuropsychologia 42 (2003) 14–24
normal or corrected to normal vision and hearing. The ex-
clusion criteria included a history of prolonged use of a pre-
scription or recreational drug, a neurological or psychiatric
condition, claustrophobia. Subjects were advised not to use
alcohol for 24 h and tobacco for 3 h prior to the scan.
2.2. Materials and procedure
2.2.1. Stem completion
Target materials for the stem completion test consisted of
a list of 360 common Italian words, 4–11 letters in length.
Frequency of occurrence of these words in the Italian lan-
guage ranged from 0 to 23 with a mean of 6.51 per mil-
lion (Bortolini, Tagliavini, & Zampolli, 1971). The stem
(i.e. the first three letters) of each word was unique among
the words and constituted the beginning of at least 10 en-
tries in Zingarelli’s Dictionary (Zingarelli, 1983). The 360
words were divided into 12 30-word sets comparable for
frequency of occurrence, word length and number of possi-
ble completions. Another 180 words were selected to form
six foil lists of 30 words each. They were presented dur-
ing the study phase preceding the baseline (non-priming)
scans. Constraints regarding the selection of words for the
foil lists were that they should be comparable in length and
frequency to and not share their initial three letters with the
experimental target words.
Before each PET scan, a list of 30 words, recorded in
a single female voice, was presented through headphones
(one word every 4 s). The subjects were instructed to rate
the pleasantness of each word on a 1–5 point scale. Approx-
imately 5 min after the study list presentation, the partici-
pants were scanned while they were performing the stem
completion test. During this phase, thirty word stems were
presented (one stem every 3 s) and the subjects were asked
to say aloud the first word that came to mind beginning with
each stem. Participants were told to avoid proper nouns and
were assured there were no right or wrong answers.
The PET experiment involved four conditions: (1)
within-modality condition (auditory-to-auditory priming):
the stems were presented auditorily through headphones by
the same female voice used for the study list; (2) cross-
modality condition (auditory-to-visual priming): word stems
were visually presented in the centre of a PC monitor. The
stems presented during the PET scanning phase were the
first three letters of the just studied word list. The only ex-
ceptions were stems 1, 4, 7, 14 and 25. These stems were
derived from non studied words in order to make the rela-
tionship between studied words and stems less transparent
(priming scan). There were two control conditions matched
for conditions 1 and 2. Here the stems presented during the
PET scan did not correspond to the word list presented in
the pre-scanning phase (foil list).
Each subject underwent 12 scans, three in each of the four
conditions (i.e. within-modality and cross-modality priming
and relative baselines). The stimuli were counterbalanced
across subjects so that each 30-word set occurred equally
often in the within and cross-modality condition, priming
and baseline scans. The order of within and cross-modality
conditions as well as priming and baseline scans was also
counterbalanced across blocks and subjects (Latin square
design).
The within-modality priming effect was measured as the
difference between the number of auditorily presented stems
that were completed with a target word from a studied list
and the number of stems that were casually completed with
a target word from an unstudied list. The cross-modality
priming effect was measured in an analogous way on the
basis of completion of visually presented stems.
2.2.2. PET data acquisition and analysis
rCBF was measured by recording the distribution
of radioactivity following the intravenous injection of
15O-labelled water (H2 15 O) with the GE-Advance scan-
ner (General Electric Medical System, Milwaukee, WI)
which has a field of view of 15.2 cm, allowing sampling
of the entire brain and cerebellum at once. Data were ac-
quired by scanning in 3D mode. A 7 mCi slow-bolus of H2
15 O was injected as a tracer of blood flow and 90 s scans
were acquired immediately after initial raise of head-counts
(Silbersweig et al., 1993). After attenuation correction (mea-
sured by a transmission scan), the data were reconstructed
as 31 transaxial planes by three-dimensional filtered back
projection using a Hanning filter (cut-off 4 mm filter width)
in the transaxial plane, and a Ramp filter (cut-off 8.5 mm)
in the axial direction. The integrated counts accumulated
over 90 s scans were used as an index of rCBF.
PET data were analysed with Statistical Parametric Map-
ping 1996 (Wellcome Department of Cognitive Neurology,
London, UK) (Friston et al., 1995a). The original brain im-
ages were first realigned and then transformed into a stan-
dard stereotactic anatomical space (Friston et al., 1995b).
Stereotactically normalised images were also smoothed with
a Gaussian filter (16 mm×16 mm×16 mm). Statistical anal-
yses were performed according to the SPM96 implementa-
tion of the general linear model (Fletcher, Shallice, Frith,
Frackowiak, & Dolan, 1996). Global differences in CBF
across conditions were made using the t statistic (Friston
et al., 1995a). The resulting set of t values constituted a sta-
tistical parametric map (SPM{t}) which was transformed
into Z score maps (SPM{Z}).
The analysis was based on a 2 (auditory versus visual
modality of stem presentation) × 2 (studied versus unstud-
ied words) factorial design. We first calculated the simple
effects of the rCBF changes (both increases and decreases)
associated with the priming effects (priming minus base-
line scans) (statistical threshold one-tailed, P < 0.001 un-
corrected). Then we directly contrasted the rCBF changes
related to within- and cross-modality priming by means
of analyses of interactions between the two main factors
masked on the relevant simple main effects (threshold for
the mask: P < 0.001). Finally, we performed correlation
analyses for both within- and cross-modality priming scans
 G.A. Carlesimo et al. / Neuropsychologia 42 (2003) 14–24
between rCBF and number of stems that were completed
with a target word. The analysis considered only the regions
showing a significant activation or deactivation in the sub-
tractive analysis.
3. Results
3.1. Behavioural data
The percentage of target words used to complete word
stems in the priming and baseline scans of the within- and
cross-modality conditions are reported in Table 1.
These data were analysed by means of a three-way
ANOVA with modality of stem presentation (auditory ver-
sus visual), condition (priming versus baseline) and block
(from 1 to 3) as repeated factors. The modality effect was
significant (F = 16.8; P < 0.01 with d.f. = 1, 7). Across
the priming and baseline conditions, auditorily presented
stems were completed with the target words more fre-
quently than visually presented stems (6.1 versus 5.1). The
condition effect was also significant (F = 42.2; P < 0.001
with d.f. = 1, 7). More stems were completed with target
words during the priming than the baseline scans (7.7 ver-
sus 3.5). The condition and modality effects did not interact
significantly (F = 0.4; P = n.s. with d.f. = 1, 7), thus
revealing comparably sized priming effects in the within-
and cross-modality conditions (4.4 and 3.9). This is an
unexpected finding. Previous behavioural studies consis-
tently reported significantly larger within-modality than
cross-modality stem completion priming (e.g. Carlesimo,
Marfia, Loasses, & Caltagirone, 1996; Graf et al., 1985).
However, it should be noted that the stem completion rate
with target words during auditory baseline scans (3.9) was
(likely by chance) quite a bit higher than during visual
baseline scans (3.2; P = 0.10). As a consequence, even
though the completion rates with target words during the
auditory priming scans (8.3) were significantly higher than
during visual priming scans (7.1; P < 0.01), a significant
difference between the priming effects in the two condi-
tions failed to emerge. The Block effect was not significant
(F = 0.7; P = n.s. with d.f. = 2, 14) and did not interact
reliably with any of the other factors, thus demonstrating
that the size of the priming effect was similar across repli-
cations. This also suggests that subjects did not use explicit
Table 1
Proportion of stems completed with words from the experimental lists and size of the priming effect in the different conditions and across successive
study-test blocks
Auditory
Studied Unstudied Within-modality priming
Block 1 0.33 0.10 0.23
Block 2 0.31 0.14 0.17
Block 3 0.36 0.15 0.21
Mean 0.33 0.13 0.20
17
retrieval strategies for stem completion. In fact, reliance on
such strategies would have inflated the target completion
rates across successive blocks (Badgaiyan et al., 1999).
Moreover, informal assessment of subjects during postscan
debriefing revealed that nearly all subjects in both within-
and cross-modality conditions were aware of the fact that
some of the stems came from the study list. However, no
subjects reported that they intentionally attempted to recall
studied words in either conditions.
3.2. PET data
Cortical areas showing significant rCBF changes, lo-
calised using the conventional Talairach co-ordinate system
(Talairach & Tournoux, 1988), are reported in Table 2.
Comparison of priming and baseline scans in the within-
modality auditory condition show a pattern of bilat-
eral prefrontal rCBF increases in the left inferior frontal
gyrus (BA 46) and in the right superior (BA 9) and
middle (BA 10) frontal gyri. Another area of significant
within-modality priming-related activation was located in
the right occipito-parietal junction (BA 39/19). There were
no significant rCBF decreases related to within-modality
priming using this threshold. This is in contrast with previ-
ous reports in the literature which showed rCBF decreases
in the lateral occipital cortex (BA 19) during auditory stem
completion priming (Badgaiyan et al., 1999; Badgaiyan
et al., 2001). To make sure that the lack of significant rCBF
decrease in BA 19 was not due to a lack of power of sta-
tistical comparison, we performed an exploratory analysis
in this region at the lowest levels of statistical significance
(P = 0.005). In this analysis, an area of rCBF suppression
in priming with respect to the baseline condition emerged
in right BA 19 (x = 48; y = −84; z = 12; Z = 2.59).
Comparison of priming and baseline scans in the
auditory-to-visual condition (cross-modality priming) was
associated with areas of significant rCBF increase in the
middle frontal gyrus (BA 10) and inferior (BA 20) and
middle (BA 21) temporal gyri of the left hemisphere. There
were also rCBF bilateral increases in the inferior parietal
lobules (BA 39, 40), which were more extended on the right
side, and in the precuneus (BA 7). An area of significant
rCBF decrease was found at the boundary between left
fusiform and inferior temporal gyri (BA 37/20). We also
performed a random effect analysis of PET data and found
Visual
Studied Unstudied Cross-modality priming
0.28 0.09 0.19
0.31 0.12 0.19
0.26 0.11 0.15
0.29 0.11 0.18
18 G.A. Carlesimo et al. / Neuropsychologia 42 (2003) 14–24

Table 2
Regions showing significant rCBF changes related to within- and cross-modality priming
Condition and cortical area Talairach co-ordinates Z

x y z Fixed effects Random effects

Within-modality auditory-to-auditory condition: priming minus baseline

rCBF increases
(1) Right superior frontal gyrus (BA 9) 30 52 32 4.4 4.2
(2) Right middle frontal gyrus (BA 10) 28 60 12 3.3 3.4
(3) Left inferior frontal gyrus (BA 46) −30 34 4 3.5 3.5
(4) Right occipito-parietal junction (BA 39/19) 48 −74 36 3.3 3.2
Cross-modality auditory-to-visual condition: priming minus baseline
rCBF increases
(1) Left middle frontal gyrus (BA 10) −40 56 0 4.0 3.5
(2) Left/right precuneus (BA 7) −2 −62 48 3.5 3.4
(3) Right inferior parietal lobule (BA 39) 52 −66 32 3.6 3.3
(4) Right inferior parietal lobule (BA 40) 48 −60 44 3.3 3.6
(5) Left inferior parietal lobule (BA 39) −48 −62 28 3.4 4.8
(6) Left middle temporal gyrus (BA 21) −60 −42 −4 3.6 3.5
(7) Left inferior temporal gyrus (BA 20) −64 −34 −16 3.2 3.4
(8) Left inferior temporal gyrus (BA 20) −58 −24 −28 3.6 3.4
rCBF decreases
(1) Left fusiform/inferior temporal gyrus (BA 37/20) −50 −52 −28 3.5 3.5
Interaction: greater activations for within-modality compared with cross-modality priming
rCBF increases
(1) Right middle frontal gyrus (BA 9) 32 48 36 3.3 3.3
Interaction: greater de-activation for cross-modality compared to within-modality priming
rCBF decreases
(1) Left fusiform/inferior temporal gyrus (BA 37/20) −50 −52 −28 4.1 4.2

that all peaks identified by the fixed effects subtractive anal-
ysis were replicated (Table 2).
Finally, we compared the magnitude of rCBF changes in
within- and cross-modality priming as interaction effects.
The analysis showed a significantly greater activation in the
right middle frontal gyrus (BA 9) in the within-modality
than in the cross-modality condition. Conversely, there
was an area of significantly larger rCBF decrease in the
cross-modality condition at the junction between the left
fusiform and inferior temporal gyrus (BA 37/20). The rate
of rCBF decrease in this area showed a significant negative
correlation with the amount of cross-modality priming, as
measured behaviourally (x = −50; y = −48; z = −20;
Z = 2.0; P = 0.02) (Fig. 1).
4. Discussion
A straightforward result of the present study is that
auditory-to-auditory within-modality and auditory-to-visual
cross-modality stem completion priming are associated
with distinct patterns of rCBF changes as detected by PET.
Particularly relevant, in this regard, are the results of the in-
teraction contrasts which highlight those cortical areas that
significantly differ in the within-relative to cross-modality
priming. Indeed, in the context of a bilateral activation of
pre-frontal regions, what differentiates within-respect to
cross-modality priming is a significantly greater activation
in the right middle frontal gyrus. In contrast, in the context
of a temporo-parietal pattern of rCBF changes what charac-
terises the cross-modality with respect to within-modality
priming is a larger rCBF decrease in the left inferior tem-
poral cortex.
The results of the PET investigation will be now dis-
cussed in detail. To ease a comparison of the present re-
sults with the results previously reported in the literature, a
meta-analysis of the activation and de-activation patterns is
shown in Table 3.
4.1. rCBF decreases
An area of rCBF decrease related to within-modality au-
ditory priming was localised in the right BA 19 (x = 48;
y = −84; z = 12) at a level of statistical significance below
the conventional threshold utilised for this kind of compar-
ison (Z = 2.59). This area of sub-threshold deactivation is
important because of its close proximity to the area which
demonstrated a significant rCBF decrease in a previous study
by Badgaiyan et al. (1999). Also in that case it was related
to within-modality auditory stem completion priming (x =
40; y = −80; z = 4). Both of these areas are adjacent to
the retinotopic V3A region whose role in vision is primarily
related to visual motion detection (Braddick et al., 2001).
Badgaiyan et al. (1999, 2001) have extensively discussed
 G.A. Carlesimo et al. / Neuropsychologia 42 (2003) 14–24 19

Fig. 1. The left BA 37/20 (panel a) was an area with significantly larger rCBF reduction during cross-modal than intra-modal priming (panel b); analysis
of data points associated with each subject shows a good within-subject consistency of this effect (panel c); rCBF here showed a negative correlation
with the number of primed words recalled during the scanning phase (panel d). IMP: intra-modal priming; IMPB: baseline for intra-modal priming;
CMP: cross-modal priming; CMPB: baseline for cross-modal priming. In all graphs the ordinate reports rCBF equivalents. Priming effect: number of
primed words that were recalled during the scanning phase (raw values are mean-centred).

the reasons for the quite surprising finding that the neural
correlate of auditory-verbal priming is localised in a cortical
area known to be implicated in vision. After ruling out al-
ternative explanations, Badgaiyan et al. argued for the pres-
ence of a distinct neuronal subpopulation, in the context of
the V3A region, implicated in the processing on nonvisual
stimuli (Nakamura & Colby, 2000). These neurons might
modulate their own activity when repeatedly exposed to the
same auditory-verbal stimuli.
Likely the most intriguing result of the present study
is an area of significant rCBF decrease associated to
cross-modality auditory-to-visual stem completion prim-
ing in the left inferior temporal gyrus extending somewhat
medially and dorsally to involve the fusiform gyrus (BA
20 G.A. Carlesimo et al. / Neuropsychologia 42 (2003) 14–24

Table 3
Cortical areas of significant priming-related rCBF change in previous PET studies using the word-stem completion paradigm
Author Cortical area rCBF decreases rCBF increases

x y z x y z

Within-modality visual-to-visual condition: priming minus baseline

Buckner et al. (1995) L posterior insular cortex (BA 41) −35 −18 −9
R middle occipital/fusiform gyrus (BA 19) 28 −63 4
Schacter et al. (1996) R inferior occipital gyrus (BA 19) 33 −74 0
L middle occipital gyrus (BA 19) −33 −79 24
R insular cortex (BA 41) 39 −26 0
R motor–premotor cortex (BA 4/6) 61 −8 28
R superior parietal lobule (BA 7) 30 −55 52
L inferior frontal gyrus (BA 47) −39 30 −8
L precuneus (BA 7) −13 −51 56
Backman et al. (1997) R lingual gyrus (BA 19) 31 −67 −17
Schacter et al. (1999) R lingual gyrus (BA 19/37) 42 −58 −8
R precuneus (BA 7) 6 −64 32
Yasuno et al. (2000) R inferior frontal gyrus (BA 47) 62 20 2
L inferior temporal/fusiform gyrus (BA 37) −42 −46 −16
R cuneus (BA 19) 16 −96 22
R superior frontal gyrus (BA 6) 32 8 42
Within-modality auditory-to-auditory condition: priming minus baseline
Badgaiyan et al. (1999) R middle occipital gyrus (BA 19) 40 −80 4
L middle occipital gyrus (BA 19) −44 −82 4
R angular gyrus (BA 39/40) 50 −66 28
R precuneus (BA 7) 2 −62 48
R middle frontal gyrus (BA 10) 26 62 12
L middle temporal gyrus (BA 38/21) −26 6 −28
Badgaiyan et al. (1999) L medial/superior frontal gyrus (BA 10) −6 48 0
R angular gyrus (BA 39/40) 42 −46 24
L lingual gyrus (BA 19) −20 −56 4
R precuneus (BA 7) 0 −46 44
L superior frontal gyrus (BA 10) −6 58 28
R middle frontal gyrus (BA 9) 36 42 36
L middle frontal gyrus (BA 9) −36 30 36
R middle temporal gyrus (BA 37) 42 −58 8
Cross-modality visual-to-auditory condition: priming minus baseline
Badgaiyan et al. (1999) L angular gyrus (BA 39/40) −40 −46 28
R medial frontal gyrus (BA 10) 0 48 20
R middle frontal gyrus 36 60 8
Cross-modality auditory-to-visual condition: priming minus baseline
Schacter et al. (1999) L superior/middle temporal gyrus (BA 39/22) −34 −46 12
R superior frontal gyrus (BA 10) 28 50 24
In all of these studies, the critical subtraction was between completion of studied and unstudied words (priming and baseline conditions, respectively).

20/37). This finding is robust because it was reliable both
in the simple main effect and interaction analyses. More-
over, the magnitude of priming-related rCBF decrease in
this region was significantly correlated with the behavioural
index of cross-modality priming (Fig. 1). As noted above,
an area of rCBF decrease in the occipito-temporal cortex
was the most consistent finding in previous PET studies
of within-modality visual stem completion priming (e.g.
Backman et al., 1997; Buckner et al., 2000; Schacter et al.,
1996). Moreover, in fMRI studies of object priming, the
fusiform gyrus also showed an attenuated response to re-
peated presentations of the same visual stimuli (Buckner
et al., 1998; Henson et al., 2000). Interestingly, in most of
these studies the functional suppression in response to stim-
ulus repetition was prevalent (Buckner et al., 2000; Schacter
et al., 1996) or also exclusively localised (Backman et al.,
1997; Henson et al., 2000; Schacter et al., 1999) in the
right hemisphere. In our case, instead, the region of rCBF
suppression related to auditory-to-visual cross-modality
priming was strictly left lateralised. The reasons for distinct
lateralisation patterns in the neurofunctional correlate of
repetition priming should be considered.
There is converging behavioural, neuropsychological and
functional neuroimaging evidence that the right and left
 G.A. Carlesimo et al. / Neuropsychologia 42 (2003) 14–24
hemispheres make a distinct contribution to repetition prim-
ing. In particular, consistent with current conceptualisations
that emphasise the role of the right hemisphere in retaining
instance-based representations of visual stimuli (Gauthier,
Behrmann, & Tarr, 1999; Warrington & Taylor, 1978), this
hemisphere seems to be specifically involved in a kind of
perceptual priming (both verbal and non-verbal) requiring
that the same physical format of stimulus presentation be
reinstated in both study and test phases. The left hemi-
sphere, instead, is likely involved in the visual processing
of more abstract representations of both words and pictures
(Marsolek, Squire, Kosslyn, & Lulenski, 1994). Thus, it
plays a prevalent role when the priming experiment involves
changes in the physical format of visual stimuli from study
to testing.
Support for the view of a prevalent role of the right hemi-
sphere in strictly perceptually-driven visual priming comes
from a series of behavioural studies by Marsolek, Kosslyn,
and Squire (1992) with healthy subjects. Neuropsycholog-
ical evidence supporting the view of specialisation of the
right hemisphere in mediating a strictly perceptual form of
priming is provided by the case of a patient who failed to
show the generally observed font-specificity effect in word
priming (i.e. more priming when the same print font is rein-
stated at study and test phases than when it differs) following
a right occipital lobectomy. However, this patient showed
a priming effect of the same magnitude as normal controls
when different fonts were used for study and testing (Vaidya,
Gabrieli, Verfaellie, Fleischman, & Askari, 1998). A recent
event-related fMRI investigation also provided relevant data
for the hypothesis that the right and left inferior temporal
cortices play distinct roles in repetition priming. Dehaene
et al. (2001) reported two areas of attenuated response in
the right extrastriate occipital cortex when subjects re-read
words printed in the same case. However, when the words
were printed in different cases for study and testing, then
the neurofunctional correlate of priming was an area of sig-
nificant attenuation in the left fusiform gyrus.
The results of the present study, which document a peak
of rCBF decrease in the left inferior temporal and fusiform
gyri when the experimental subjects were completing visu-
ally presented stems with words that had been previously
listened to, suggest that the level of abstraction of word rep-
resentation underlying repetition priming in these cortical
areas is more pronounced than previously thought. In par-
ticular, it suggests that this cortical region might be involved
in the complex interactions between the phonological and
orthographic codes of words which ultimately allow for the
cross-modality facilitation in verbal stimulus re-processing.
Support for the view that regions in the left inferior tem-
poral cortex can modulate their neural activity in response
to verbal stimuli independent of stimulus-driven perceptual
processes comes from an fMRI study by Buckner et al.
(2000). This study shows a common area of activity reduc-
tion in this region whether the verbal cue prompting the
word generation task was visual or aural. Based on findings
21
from pre-surgical exploration in epileptic patients (Schaffler,
Luders, Morris, & Wyllie, 1994), the term “basal tempo-
ral language area” was proposed to define a cortical region
involving the left fusiform, inferior temporal and parahip-
pocampal gyri. Electrical stimulation of these areas produces
pervasive language impairment, including reading disorders,
speech arrest and comprehension deficits (Schaffler, Luders,
& Beck, 1996). PET investigation has provided additional
data about the role of this region in integrating multimodal
language processes. Based on the finding that processing
both words and non-word letter-strings elicited a common
area of rCBF increase in BA 37, regardless of the modality
used (visual or tactile), Buchel, Price, and Friston (1998)
proposed that this area has a specific role in integrating “con-
verging inputs from many regions” (p. 274).
4.2. rCBF increases
A greater rCBF increase in the within-modality than in
the cross-modality priming condition was observed in the
right middle frontal gyrus (BA 9). As previously noted, a
metabolic activation in the right prefrontal areas is com-
monly associated with deliberate retrieval of recently learned
information in episodic memory tasks (e.g. Tulving et al.,
1994). Could this finding imply that experimental subjects
were engaging in the deliberate recollection of words of the
study list to complete the stems? Although this possibility
cannot be completely dismissed, the analysis of behavioural
data does not support this hypothesis. First, the magnitude
of priming in the present study is more similar to that ob-
served in previous behavioural studies in which healthy sub-
jects and memory disordered patients completed the stems
implicitly than when they performed an explicit cued recall
task (e.g. Carlesimo, 1994; Carlesimo et al., 1996). More-
over, in the present experiment the completion rate of the
stems with the target words remained substantially the same
across successive blocks. Thus, it is unlikely that the subjects
became progressively more aware of the memory nature of
the stem completion task as the study-test blocks repeated.
To account for the pattern of right prefrontal activa-
tion related to auditory-to-visual and visual-to-auditory
cross-modality stem completion priming Badgaiyan et al.
(1999), Badgaiyan et al. (2001) and Schacter et al. (1999)
proposed the rCBF increase in this region could be the
manifestation of a sort of post-completion awareness that
the words used for completing the stems had been re-
cently encountered rather than evidence of a deliberate
strategy to complete stems with previously studied words.
Schacter (1987) coined the expression “involuntary con-
scious memory” to describe this phenomenon. To ac-
count for rCBF increases in the right prefrontal regions
related to cross-modality but not to within-modality prim-
ing, Badgaiyan et al. (1999) and Schacter et al. (1999)
argued that the contamination of repetition priming by ex-
plicit memory processes (mainly as “involuntary conscious
memory”) is more frequent when a different rather than
22 G.A. Carlesimo et al. / Neuropsychologia 42 (2003) 14–24
the same modality of stimulus presentation is used during
the study and test phases of a stem completion paradigm.
However, the conclusion that cross-modality priming is
more exposed to contamination by explicit retrieval strate-
gies than within-modality priming is not supported by
neuropsychological evidence. The latter generally shows
normal repetition priming in memory disordered patients
both when the same or when a different modality of stim-
ulus presentation is used for study and testing (Carlesimo,
1994; Carlesimo et al., 1996; Graf et al., 1985).
In conclusion, the right prefrontal activation found in the
present study confirms the possible participation of explicit
memory mechanisms in stem completion priming. The sub-
stantially low level of the completion rate and the lack of an
increase in priming magnitude across successive study-test
blocks suggest that the contribution of such mechanisms is
more in eliciting post-retrieval awareness of a recent en-
counter with the generated word than in actual support for
active retrieval. In the present study, this mechanism was par-
ticularly active in the within-modality condition. This sug-
gests that in the specific experimental condition of our study
such “involuntary conscious memory” was more likely to
occur when the same experimental context of stimulus pre-
sentation (modality and specific voice) was reinstated for
study and testing than when experimental contexts differed
from study (hearing words) to testing (reading stems).
In addition to the rCBF increase in the right frontal polar
region, the within-modality condition activated a cluster of
left prefrontal areas in the middle and inferior frontal gyri.
In this case, however, the interaction analysis failed to doc-
ument a greater activation in the within-modality respect
to cross-modality condition. For this reason, the peculiarity
of left prefrontal activation in the within-modality priming
can be regarded as only suggestive. rCBF changes related
to stem completion priming in the left prefrontal cortex
have already been described (Schacter et al., 1996). A sig-
nificant left frontal activation is generally found in word
fluency tasks which, analogously to the stem completion
procedure, require generating words from a common first
letter (Frith, Friston, Liddle, & Frackowiak, 1991; Paulesu
et al., 1997). However, it is unlikely that the priming-related
rCBF increase in this region is the expression of cortical
activity generically related to phonological word fluency
since the same number of words was generated with visual
and auditory stems and during priming and baseline scans.
Rather, rCBF changes in this region should be considered
as the expression of more efficient access to output rep-
resentations of recently encountered words prompted by
either phonological or semantic cues.
In the present study, cross-modality priming was associ-
ated with rCBF increases in the inferior parietal lobule bilat-
erally (with a right side prevalence) and in the left inferior
and middle temporal gyri (BAs 20 and 21). Also in this case,
however, the lack of significance of the interaction contrasts
suggests caution in attributing a peculiar role of this cluster
of activations in the genesis of cross-modality priming. The
involvement of regions in the left temporal lobe appears to be
theoretically relevant. BAs 21 and 22 in the middle and supe-
rior temporal gyri are consistently activated in word recog-
nition tasks whether the modality of stimulus presentation is
auditory or visual and whether or not a spoken response is
required (Howard et al., 1992). Moreover, the participation
of these cortical regions is not limited to lexical retrieval
but also involves semantic processing, as documented by
their activation during semantic retrieval tasks whether
words (Wise et al., 1991), pictures (Martin, Haxby, Lalonde,
Wiggs, & Ungerleider, 1995) or faces (Gorno-Tempini
et al., 1998) are involved. Ishitobi et al. (2000) pointed out
the existence of axonal connections between the regions in
the “basal temporal language area” and the linguistic areas
in the dorso-lateral surface of the temporal lobe.
5. Conclusions
In the present study, priming is associated with both
rCBF increases and decreases in different neocortical areas
of the brain. These results as well as full consideration of
findings from previous studies suggest that verbal repeti-
tion priming is associated with a complex re-modulation of
rCBF activity both in the sense of neocortical distribution
and in direction of changes. In the posterior regions of the
brain, the most consistent correlate of repetition priming
is an rCBF decrease in cortical areas known to be impli-
cated in lexical processing. When the priming test involves
re-processing the verbal stimulus in the same modality as the
previous presentation (either visual or auditory), the right
temporo-occipital extrastriate cortex is the most consistent
site of rCBF change. If, instead, re-processing facilitation
is mediated by more abstract levels of lexical-semantic
representations, then the inferior and lateral surfaces of the
left temporal cortex are more directly involved. In the pre-
frontal regions, the main PET correlate of verbal priming
is a bilateral rCBF increase, likely the expression of more
efficient access to output phonological representations and
of the involuntary retrieval of the recent episode during
which the just generated word has been encountered.
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