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Subliminal and Supraliminal in Reading
Subliminal and Supraliminal in Reading
doi:10.1093/cercor/bhl110
Advance Access publication November 13, 2006
Cerebral Bases of Subliminal and Sid Kouider1,2, Stanislas Dehaene1,3, Antoinette Jobert1 and
Denis Le Bihan4
Supraliminal Priming during Reading
1
Cognitive Neuroimaging Unit, INSERM U562, SHFJ, CEA/DSV,
Orsay, France, 2Laboratoire des Sciences Cognitives et
Psycholinguistique (EHESS/CNRS/DEC-ENS), Paris, France,
3
Collège de France, Paris, France and 4Anatomical and
Functional Neuroimaging Unit, SHFJ, CEA/DSV, Orsay, France
Several studies have investigated the neural correlates of conscious processes will be frequently if not always confounded with
perception by contrasting functional magnetic resonance imaging conscious perception.
Ó The Author 2006. Published by Oxford University Press. All rights reserved.
For permissions, please e-mail: journals.permissions@oxfordjournals.org
Subliminal presentation Supraliminal presentation
e
Tim
Tim
43 ms prime or 43 ms prime or
29 ms %%%%%%% 29 ms
271 ms ####### 271 ms #######
620 ** 620
** ***
Response time (ms)
560 560
500 500
Unrelated Ortho Ortho+Phono Unrelated Ortho Ortho+Phono
(U) (O) (O+P) (U) (O) (O+P)
soutet garape garaje soutet garape garaje
GARAGE GARAGE GARAGE GARAGE GARAGE GARAGE
Figure 1. Experimental procedure and behavioral results for the subliminal (left part) and supraliminal presentation (right part) (n.s. 5 nonsignificant; *P \ 0.02; **P \ 0.002;
***P \ 0.0002).
processing is associated with detectable activity in occipital and repetition suppression phenomenon differs in the subliminal
temporal cortices, and that supraliminal presentation yields and supraliminal conditions.
additional parieto-prefrontal activity (Dehaene et al. 2001). We contrasted 3 conditions (see Fig. 1): The prime could be
Crucially, however, relative to those previous designs, here unrelated to the target, it could be orthographically similar to the
the task required neglecting those initial lower-case stimuli target, or it could be orthographically similar and also homopho-
(hereafter termed the ‘‘primes’’) in order to perform a semantic nic with the target, and thus related at both the orthographic and
decision task on other highly visible ‘‘target’’ words presented phonological levels. Behavioral studies of visual word recogni-
subsequently in upper case and at the same screen location. In tion have suggested that although masked orthographic priming
this manner, we could study the neural correlates of prime obtains easily, this is not the case for phonological priming,
visibility, that is, the fate of subliminal or supraliminal stimuli, especially when using brief prime durations (e.g., below 50 ms).
which did not receive task-related attention. Indeed, priming at the phonological level necessitates longer
Naturally, the status of such brief stimuli in relation to prime durations (Ferrand and Grainger 1992, 1993). However,
consciousness may be debated. Although the unmasked primes because longer durations induce higher visibility, phonological
were, visible, in the sense that they could be reported by effects also correlate with prime visibility (Kouider and Dupoux
subjects when told to do so, it does not necessarily imply that 2001). As both factors were confounded in previous studies, it is
they were consciously seen on every trial of the main task still a matter of debate whether phonological effects are driven
performed on target stimuli. Research on the attentional blink by prime duration (Grainger et al. 2003) or, as we previously
and inattentional blindness (Mack and Rock 1998; Sergent et al. suggested, by prime visibility (Kouider and Dupoux 2001). In the
2005) suggests that unattended stimuli may completely fail to present study, we addressed this issue by taking advantage of the
be registered into consciousness. Indeed, in the present design fact that visible and invisible primes were contrasted while the
it could be advantageous for subjects to actively withdraw prime duration was kept constant (i.e., 43 ms). Under these
attention from the primes, in order to avoid interference with conditions, we expected orthographic, but no phonological
the main target word. Thus, it has been argued that the present priming in the subliminal condition. By contrast, we expected
design merely studies a ‘‘preconscious’’ level of processing phonological effects to emerge with visible primes, even when
where stimuli are potentially accessible but not consciously using the same short prime duration.
accessed (Dehaene et al. 2006). We will return to whether The emergence of phonological priming as a function of
attention is necessary for consciousness and how the pre- prime visibility can be taken, in itself, as an indication that
conscious level is specified in the Discussion. supraliminal primes are able to invade a much larger set of brain
In addition to allowing us to contrast visible versus invisible regions than subliminal primes. If stimulus visibility relates to
stimuli, our design allowed us to study the effect of those stimuli the recurrent activation of a broad network of regions, then in
on the subsequent processing of another conscious target. To the unmasked condition we should see an extension of the fMRI
this end, we exploited the phenomenon of fMRI adaptation repetition suppression effect into a broad set of areas distant
(Grill-Spector and Malach 2001), a reduction of brain activity from visual cortex, some of which should show specific
when some properties are shared between the prime and target, phonological effects.
compared with a situation in which they fully differ (Naccache A final difficulty is that fMRI lacks temporal resolution and
and Dehaene 2001; Henson 2003). We studied whether this therefore lumps together the activation evoked by the masks,
other clusters showed a main effect of visibility, even when also a smaller peak in the right occipito-temporal sulcus (32,
restricting the search only to active voxels, although a trend was –70, –22). Outside the ventral visual pathway, repetition
found in left inferior frontal cortex (–42, 20, 18; Z = 3.62). As suppression was also observed in the left middle temporal
expected, there were no regions of greater activation to gyrus (–56, –50, 10), the depth of the left and right precentral
subliminal than to supraliminal primes. sulci (–36, 4, 30 and 48, 10, 34), the left inferior prefrontal
We then examined the effects of the primes (Fig. 3). A first cortex (–50, 40, 8), the bilateral supplementary motor area
contrast was designed to maximize the detection of ortho- (SMA)/preSMA (12, –10, 54 and –14, 8, 52), the right intraparietal
graphic priming effects, which should be present in both the O cortex (40, –58, 42), and right thalamus (22, –22, 12).
and O + P conditions. We therefore searched for more activity in The vast majority of these regions showed a strong in-
condition U than in the mean of conditions O and O + P (ortho- teraction of orthographic repetition suppression with prime
graphic repetition suppression) as well as the reverse contrast visibility, indicating that they showed more repetition suppres-
(orthographic repetition enhancement). sion with supraliminal than with subliminal primes (Fig. 2,
In the subliminal condition (Fig. 3A), we observed several bottom). The sole exceptions were the left and right ventral
regions with orthographic repetition suppression (but no occipito-temporal and the lateral inferotemporal cortices,
region with repetition enhancement). Repetition suppression where histograms of percent signal change confirmed that
reached corrected significance in a right ventral region with orthographic repetition suppression was approximately as
both mesial (16, –56, –8) and lateral (e.g., 28, –62, –8) subpeaks, at strong for visible than for invisible stimuli (Fig. 4, top left).
a location overlapping mostly with the right cerebellum but A second contrast examined phonological priming by com-
encroaching partially into the right lingual gyrus. Two symmet- paring conditions O + P and O. No supraliminal repetition
rical regions were also observed, just below significance, at suppression was observed (O + P < O). In the converse contrast
a location corresponding to the left and right frontal eye fields for supraliminal repetition enhancement, although no differ-
(FEF) (–22, –14, 66, Z = 4.56, corrected P = 0.055; and 26, –6, 70, ence was found at the conventional voxel-level threshold of P <
Z = 4.09, corrected P = 0.081). Another a priori location of 0.001, lowering this threshold to P < 0.005 revealed an
interest, the VWFA previously reported in several studies of extended cluster of greater activation for phonologically related
subliminal priming during reading (Dehaene et al. 2001, 2004; trials than for orthographically related trial (corrected cluster-
Devlin et al. 2004), also showed a small repetition suppression level P = 0.002), with subpeaks in the left inferior frontal (–32,
effect (–38, –62, –20; peak Z = 3.56; voxel-level P = 0.0002, 28, –6) and left anterior insula (–34, 12, –6). No subliminal
uncorrected; cluster extent 23 voxels). phonological effect was observed, as either suppression or
When tested in the supraliminal condition (Fig. 3B), ortho- enhancement, and both of the above peaks showed a small
graphic repetition suppression became extensive (still without interaction effect suggesting greater priming in the supraliminal
any region of repetition enhancement). Repetition suppression compared with the subliminal condition (respectively Z = 3.61
was significant in the left occipito-temporal sulcus, within and 2.99), although this interaction did not reach significance at
a large cluster extended from the posterior occipito-temporal the cluster level.
sulcus (–40, –70, –4) to the VWFA and the lateral inferotemporal Figure 4 summarizes the major task-related regions and their
multimodal area (Cohen et al. 2004) (–50, –58, –10). There was profile of activity across the 6 conditions. Examination of those
profiles shows that, in many regions, the main difference arises Dehaene et al. (2001). Such a difference might be related to the
from a stronger activation in the unrelated, supraliminal progressive posterior-to-anterior anatomo-functional hierarchy
condition compared with all of the others. This is the principal thought to be involved in visual word recognition (Dehaene
reason underlying the above-described priming by visibility in- et al. 2004; Nakamura et al. 2005). Although Dehaene et al.
teraction. To demonstrate this effect more directly, we reex- (2001) used word repetition priming, the present study relied
amined the visibility contrast (supraliminal minus subliminal on orthographic priming by a pseudoword prime, which shared
trials) as a function of the prime-target relation. When the prime all but one letter with the target. Such priming may engage only
was related (O and O + P conditions), the visibility contrast was sublexical letter and bigram levels, which are thought to engage
entirely confined to bilateral occipito-temporal regions, as the posterior occipito-temporal sulcus (Dehaene et al. 2004;
described earlier. However, when the prime was unrelated, in Nakamura et al. 2005). Devlin et al. (2004) also used subliminal
addition to this major occipito-temporal difference, an addi- orthographic priming with partial letter overlap rather than
tional increase in activation with visibility was seen in left and repetition priming and also observed a posterior peak of
right precentral sulci (–42, 2, 38 and 54, 2, 30), the left inferior repetition suppression very close to the one in the current
prefrontal cortex (–44, 22, 10), and the bilateral SMA/preSMA study (respectively, –40, –60, –20 and –38, –62, –20).
(6, 6, 50 and –8, 8, 54). Thus, when the subject was presented However, by contrast to previous work, we also observed
with 2 completely distinct strings, these regions showed more subliminal orthographic effects in 2 additional regions. First,
activity when this pair was visible than when it was subliminal. repetition suppression was observed in the left and right FEF
known to be involved in saccadic eye and attention movements
(Schall 2004). In spite of their anterior localization, the FEF are
Discussion increasingly thought of as early visual processing areas with
a fast connection to visual cortex (Schmolesky et al. 1998) and a
Neural Correlates of Subliminal Priming demonstrable activation by subliminal visual stimuli (Thompson
In accord with previous studies of masked priming during and Schall 1999). However, the FEF were not observed in
reading (Dehaene et al. 2001, 2004; Devlin et al. 2004), previous studies of subliminal priming during reading. This
subliminal priming was associated with repetition suppression discrepancy might be explained by the use of pseudoword
in left occipito-temporal cortex, at a location roughly corre- primes in the present study, whereas only word primes were
sponding to the VWFA. In the present study, however, the peak used in previous work. Pseudowords involve serial rather than
of fMRI adaptation was slightly posterior to the one reported by parallel reading, as demonstrated by a significant word length
0.2
0.2 0.1 0.1
0.1
0 0 0 0
U O O+P U O O+P U O O+P U O O+P U O O+P U O O+P U O O+P U O O+P
Subliminal Supraliminal Subliminal Supraliminal Subliminal Supraliminal Subliminal Supraliminal
0.2
0 0 0 0
U O O+P U O O+P U O O+P U O O+P U O O+P U O O+P U O O+P U O O+P
Subliminal Supraliminal Subliminal Supraliminal Subliminal Supraliminal Subliminal Supraliminal
0
-0.05
0 0
U O O+P U O O+P U O O+P U O O+P U O O+P U O O+P U O O+P U O O+P
Subliminal Supraliminal Subliminal Supraliminal Subliminal Supraliminal Subliminal Supraliminal
Figure 4. Histograms of percent BOLD signal change across the 6 conditions of the experimental design, for several brain regions of interest showing orthographic repetition
suppression from subliminal primes (A) and/or supraliminal primes (B), or phonological repetition enhancement from supraliminal primes (C).
effect (Weekes 1997; Rastle et al. 2000, 2003, 2005; Coltheart As concerns phonological priming, as predicted on the basis
et al. 2001). It is therefore possible that pseudowords flashed of our previous work (Kouider and Dupoux 2001), phonological
subliminally would nevertheless evoke a brief activation in eye- effects did not show up under subliminal conditions, either at
and attention-movement circuitry, thus creating a repetition the behavioral or at the neural level. Phonological priming was
suppression effect in those regions if the subsequent word shares only observed under supraliminal conditions. Those results are
most of its constituent letters with the pseudoword prime. consistent with previous research indicating that suprathres-
Subliminal repetition suppression was also observed in the hold primes are necessary to obtain phonological effects in
right superior cerebellum. Cerebellar activations, with a consis- word recognition tasks (Shen and Forster 1999; Kouider and
tent right lateralization, have been observed consistently in Dupoux 2001). Relative to these previous findings, the present
fMRI studies of reading (Fulbright et al. 1999; Turkeltaub et al. effect was rather small and the interaction of phonological
2002). The activation we observed matches tightly with that priming with visibility did not quite reach significance, perhaps
observed by Fulbright et al. (1999) in an fMRI study using due to a small degradation of stimulus visibility related to the
orthographic, phonological, and category judgment tasks on projector, screen and mirror used to present stimuli in the fMRI
written words. Although these observations suggest a potential scanner. Nevertheless, the present experiment is the first to
cerebellar contribution to visual word recognition processes, afford an examination of the cerebral mechanisms of such
which remains to be characterized functionally, great caution phonological priming. Unexpectedly, instead of being associ-
remains needed in drawing such a conclusion because the ated with repetition suppression, phonological priming was
activation might also be imputed to contamination from the associated with a small increase in activation of the left inferior
neighboring lingual gyrus, due to spatial smoothing and group frontal cortex and anterior insula. These regions are well known
analysis. In future work, the issue of a specific contribution of to be implicated in phonological and articulatory processing
the cerebellum to reading and to orthographic priming could be (Dronkers 1996; Burton 2001; Booth et al. 2002; Poeppel and
further clarified by high-resolution fMRI studies and single- Hickok 2004). The left inferior frontal cortex has been
subject analysis. associated with sublexical phonological processing during