The rise and fall of priming: how visual exposure shapes cortical representations of objects.

Abstract

How does the amount of time for which we see an object influence the nature and content of its cortical representation? To address this question, we varied the duration of initial exposure to visual objects and then measured functional magnetic resonance imaging (fMRI) signal and behavioral performance during a subsequent repeated presentation of these objects. We report a novel 'rise-and-fall' pattern relating exposure duration and the corresponding magnitude of fMRI cortical signal. Compared with novel objects, repeated objects elicited maximal cortical response reduction when initially presented for 250 ms. Counter-intuitively, initially seeing an object for a longer duration significantly reduced the magnitude of this effect. This 'rise-and-fall' pattern was also evident for the corresponding behavioral priming. To account for these findings, we propose that the earlier interval of an exposure to a visual stimulus results in a fine-tuning of the cortical response, while additional exposure promotes selection of a subset of key features for continued representation. These two independent mechanisms complement each other in shaping object representations with experience.

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FEATURE ARTICLE
The Rise and Fall of Priming: How Visual
Exposure Shapes Cortical Representations
of Objects
Laure Zago, Mark J. Fenske, Elissa Aminoff and Moshe Bar
Martinos Imaging Center at MGH, Harvard Medical School,
149 Thirteenth Street, Charlestown, MA 02129, USA
How does the amount of time for which we see an object
influence the nature and content of its cortical representation? To
address this question, we varied the duration of initial exposure to
visual objects and then measured functional magnetic resonance
imaging (fMRI) signal and behavioral performance during a sub-
sequent repeated presentation of these objects. We report a novel
‘rise-and-fall’ pattern relating exposure duration and the corre-
sponding magnitude of fMRI cortical signal. Compared with novel
objects, repeated objects elicited maximal cortical response re-
duction when initially presented for 250 ms. Counter-intuitively,
initially seeing an object for a longer duration significantly reduced
the magnitude of this effect. This ‘rise-and-fall’ pattern was also
evident for the corresponding behavioral priming. To account for
these findings, we propose that the earlier interval of an exposure
to a visual stimulus results in a fine-tuning of the cortical response,
while additional exposure promotes selection of a subset of key
features for continued representation. These two independent
mechanisms complement each other in shaping object representa-
tions with experience.
Keywords: behavioral facilitation, fMRI repetition-related response
reduction, object representation, occipito-temporal cortex, priming, prior
exposure duration, response sharpening and selectivity, visual experience,
visual object recognition
Introduction
Prior exposure to a stimulus generally facilitates its recognition
in subsequent encounters. This experience-based phenome-
non, termed priming, has been studied extensively and is
believed to be one of the building blocks of learning and
memory (Tulving and Schacter, 1990). Electrophysiological
recording studies in monkeys have provided important insights
regarding the possible physiological basis of such experience-
related changes in processing: specifically, by showing reduced
neuronal response for repeated, compared with novel, stimuli.
This effect has been found in inferior-temporal regions (Li et al.,
1993; Ringo, 1996; Brown and Xiang, 1998) as well as in the
prefrontal cortex (Rainer and Miller, 2000). In humans, regions
involved in visual recognition have also been observed to
produce a relatively reduced cortical response for repeated
stimuli, as measured in studies using positron emission tomog-
raphy (PET; Buckner et al., 1995; Badgaiyan et al., 2001), event-
related potentials (ERP; Rugg et al., 1995; Puce et al., 1999),
magnetoencephalography (MEG; Noguchi et al., 2004) and
functional magnetic resonance imaging (fMRI; Buckner et al.,
1998; Grill-Spector et al., 1999; James et al., 1999; Henson et al.,
2000; Chao et al., 2002; Vuilleumier et al., 2002). This
experience-based change in cortical response has been as-
signed numerous terms, many of which implicitly assume some
underlying function in the effect they describe [e.g. suppres-
sion (Henson and Rugg, 2003) and adaptation (Grill-Spector and
Malach, 2001), but not attenuation (Yi et al., 2004)]. We adopt
here a functionally neutral working term: repetition-related
response reduction.
While the phenomenon of repetition-related response re-
duction is, by definition, associated with the level of experience
an individual has with a particular stimulus, the precise nature
of this relation remains unclear. Specifically, how does the
duration of our exposure to a certain visual object affect its
cortical representation? We sought to clarify this relation by first
systematically varying the amount of visual experience that
observers acquired for each stimulus during its initial exposure,
where each object was first presented for a duration lasting
between 40 and 1900 ms. Then, using fMRI, we compared the
response when each object was shown again in a subsequent
repetition with that obtained for novel objects. To ensure
identical viewing conditions when assessing the reduction of
fMRI signal and behavioral response for new versus repeated
presentations, additional new objects and all of the previously
seen objects (regardless of their prior exposure duration) were
each presented for 500 ms.
How might the magnitude of cortical response reduction
change as a function of the amount of prior experience? It has
been hypothesized that, at a neuronal level, repetition-related
response reduction reflects the operation of a mechanism that
increases the efficiency of cortical object representations with
added exposure (Desimone, 1996). According to this account,
the representation becomes efficient as the cortical response
displays ‘sharpened’ stimulus selectivity. The use of ‘sharpening’
in this original proposal might mean that groups of neurons
collectively represent all of the features of an object and, with
added experience with the object, come to do so with
increasing fidelity. The prediction that stems from this view is
that increased exposure to a certain stimulus would result in
increased neural selectivity for that stimulus, producing a con-
tinued reduction of the cortical response because neurons that
are not optimally selective for that stimulus gradually stop
participating in the object’s representation. Increasing the
exposure duration in the initial encounter with an object
should, accordingly, lead to a larger response reduction, up to
a certain asymptotic value (Li et al., 1993).
Subsequent theorizing has suggested that rather than
merely sharpening the response to all information about
a stimulus, experience with a visual stimulus might alternately
lead to continued representation of only those features that
are essential for identifying an object, while neurons coding
features that are non-essential stop responding (Wiggs and
Martin, 1998). By this view, the representation of a stimulus
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formed through increased exposure does not maintain exhaus-
tive information about all of an object’s features, but instead
selectively represents only a ‘key’ sub-set of features that may
be useful in distinguishing it from other objects. In light of
the cortical commitment involved in maintaining object repre-
sentations over time, it seems beneficial to have a mechanism
that can increase the distinctiveness of an object’s representa-
tion while also reducing the number of represented features.
However, representing fewer features provides less overlap
between an object’s cortical representation and the corre-
sponding visual input when that object is encountered sub-
sequently. Therefore, if the magnitude of repetition-related
response reduction depends on the similarity between the
object’s features and its primed representation, then a decrease
in the total number of represented features might be expected
to elicit a diminished response reduction with increased prior
exposure to an object.
Both of these prior proposals imply that the magnitude of
response reduction should change as a function of the initial
exposure duration. Accordingly, increases in the magnitude of
response reduction following increased visual experience with
an object might indicate the influence of a ‘sharpening’ mech-
anism, while decreases in the magnitude of response reduction
might indicate the influence of a selective mechanism that
leads to the continued representation of features that are
essential for identifying an object. Our results suggest, in fact,
that both mechanisms are involved across different incremental
periods of visual experience. Specifically, we report a clear ‘rise-
and-fall’ pattern that consists of a distinct period in which
repetition-related response reduction increases (i.e. following
40--250 ms of prior exposure) and a distinct period in which it
decreases (i.e. following 350--1900 ms of prior exposure). We
therefore propose that both fine-tuning and features selection
affect visual representation of objects with increasing exposure.
When considering the relation between prior experience
with visual objects and the corresponding repetition-related
reduction in fMRI signal, it is important to remember that
repetition-related response reduction is typically accompanied
by improved recognition and shortened behavioral response
latencies for repeated stimuli. Because cortical response re-
duction and behavioral priming generally occur together and
share similar characteristics (Wiggs and Martin, 1998; Sayres
and Grill-Spector, 2003; Lustig and Buckner, 2004; Maccotta
and Buckner, 2004; Noguchi et al., 2004), it is tempting to think
of them as manifestations of the same mechanism. While
additional evidence is needed to establish an unequivocal causal
link between them, a demonstration that cortical response
reduction and behavioral priming consistently show similar
changes across the experimental conditions of the present
studies would provide converging support for the hypothesis
that these effects are critically related. We therefore asked
subjects in our studies to make a simple judgment about each
presented object (i.e. natural or manufactured). Then, we
compared reaction times, in addition to fMRI signal, for re-
peated objects relative to novel objects, as a function of the
duration of prior visual exposure. This revealed the exact same
‘rise-and-fall’ pattern in the magnitude of behavioral priming as
that found in the magnitude of the fMRI response reduction.
Finally, temporal parameters such as prime duration can
produce quite different effects when manipulated in blocked
versus randomly intermixed designs (Smith et al., 1994; Stolz
and Besner, 1997). We therefore tested separate groups of
subjects in block design and event-related fMRI versions of our
study, as well as in a purely behavioral experiment, to guarantee
results that are robust in the face of differences that these
different experimental designs afford in expectancies, strategies
and contrast effects. Inherent differences in each version of
the study also allowed us to assess the robustness of our results
across differences in the time interval separating the first and
second presentations of each object [average time between
presentations: block design, 40--58 s (9--18 intervening stimuli);
event-related, 2 s--14 min; (1--374 intervening stimuli), behav-
ioral study, 2 s--2 min (2--60 intervening stimuli)].
Materials and Methods
Participants
Forty-four healthy right-handed subjects (mean age: 28.5 years, range:
21--37 years; 27 females) participated in the experiment (12 in each
fMRI experimental design and 20 in the behavioral study). All subjects
had normal or corrected-to-normal vision. None were aware of the
purpose of the experiment. Informed written consent was obtained
from each subject prior to the scanning or behavioral session. All
procedures were approved through Massachusetts General Hospital
Human Studies Protocol number 2001P-001754 and the Harvard
University committee on the use of human subjects in research.
Stimuli and Apparatus
The stimuli were 550 color photographs of familiar everyday objects,
such as tools, furniture, means of transportation, clothes, animals, fruits,
plants and vegetables.Each picturewas presented centrally(mean visual
angle 9?) on a white background, followed immediately thereafter by
a mask (Fig. 1). Ten different masks were used, each a nonsense pattern
of mixed lines and patches of color and texture of a similar size and
contrast to that from the object-pictures.
Stimuli were back-projected (Sharp LCD projector, XG-NV6XU)
onto a translucent screen that subjects viewed through a mirror
mounted on a head coil. A custom-designed magnet-compatible panel
of three keys was used for subjects’ responses. The image presentation
and response collection were controlled by a Macintosh G4 running
PsyScope experimental software (Macwhinney et al., 1997) at a dis-
play resolution of 1024 3 768 pixels and a refresh rate of 75 Hz. Each
subject had 130 practice trials using pictures that were not presented
again in the actual experiment.
Design and Procedure
There were six functional image acquisition runs for each subject in
both fMRI experimental designs. Each run consisted of trials containing
fixation and object displays, each lasting 2 s. On object trials, a picture of
an object was presented and followed immediately by a mask. There
were 13 different object--display conditions: six different First exposure
conditions (40, 150, 250, 350, 500, 1900 ms), six corresponding Repeat
conditions (i.e. the same objects from the First conditions presented
for 500 ms) and a New condition (i.e. novel objects presented for 500
ms). Because total trial duration was 2 s, the duration of the mask varied
across conditions, with a range of 100--1960 ms. For example, the mask
in the 40 ms exposure duration condition was presented for 1960 ms
(i.e. 2000 ms total duration minus 40 ms object duration equaled 1960
ms mask duration). The task on experimental trials was to decide
whether the presented object was natural or manufactured. Subjects
were instructed to respond as accurately and as quickly as possible for
each picture, by pressing a response key with their right hand. When
subjects were unsure about their answer, they could press a third, ‘do
not know’ button. On trials providing the fixation baseline, a black dot
was presented in the center of the display. Subjects were asked to
maintain fixation during these trials without making any response.
Block Design
For each functional run in the block design, 13 experimental blocks of
pictures — one per object-display condition — alternated with 13
fixation blocks. Each block lasted 20 s and consisted of 10 consecutive
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object or fixation trials, depending on the block. During the fixation
blocks, the last fixation dot was red to signal the next experimental
block. During the experimental blocks, 10 different stimuli were
presented, all for the same exposure duration. For corresponding
First and Repeat blocks, the same pictures were presented in a differ-
ent random presentation order. The time interval between the first
and repeated exposure of the same picture ranged between 40 and 58 s
(9--18 intervening stimuli). The presentation order of the six functional
runs varied randomly across subjects.
Event-related Design
The presentation order of trials for the event-related design was
determined by pseudo-randomly intermixing the 780 trials from the
13 experimental with 264 fixation trials. This was accomplished
using the optseq program within the FreeSurfer Functional Analysis
Stream (FS-FAST) software tools (http://surfer.nmr.mgh.harvard.edu/
optseq). This program optimizes the presentation sequence of exper-
imental and fixation trials for event-related designs to maximize
the efficiency and accuracy of the estimation of the hemodynamic
response for each stimulus presentation (Burock et al., 1998; Dale
et al., 1999). The presentation order provided by optseq was sub-
sequently adjusted to ensure that the First trial for a given object
preceded that object’s Repeat trial. This final sequence was divided
into six sections of 174 consecutive trials for use in each of the
functional runs. Intermixing trials from all conditions across the
entire experiment resulted in a time interval between the first and
repeated exposure of the same picture that ranged between 2 s and
14 min (1--374 intervening stimuli). In contrast to the block design,
the wide range of intervals between First and Repeat trials in the
event-related design provided minimal information about when an
item may be repeated. This served accordingly to minimize any
attentional effects associated with an items’ anticipated recurrence
(Vuilleumier et al., 2002). Intermixing trials from all conditions also
served to minimize any attentional effects associated with an
items’ anticipated exposure duration. To control for item effects,
the assignment of specific objects to each experimental condition
was varied between subjects.
Behavioral Study
The design and procedure for the behavioral study was identical to
that used in the event-related design, with two exceptions. First,
subjects were tested individually in a testing room, outside of the
scanner, with stimuli presented on a 33 cm CRT monitor. Second,
the presentation order of the experimental trials were randomly
intermixed with the sole constraint that the time interval separating
first and second presentations of each object ranged between 2 and
120 s (2--60 intervening stimuli).
Imaging Details
Block design subjects and event-related design subjects were scanned
in a 3T Siemens-Allegra scanner. All images were acquired with
a custom-built head coil. For each subject, a series of conventional
high-resolution structural images (3-D T1-weighted images) was first
collected for cortical surface reconstruction. A series of functional
images was then collected using a gradient echo-planar imaging
(EPI) sequence (block design: TR= 2.31 s, TE= 30 ms; event-related
design: TR= 2.00 s, TE= 25 ms; both designs: flip angle = 90?, field of
view = 256, slice thickness = 3 mm + 1 mm skip, 33 interleaved slices
oriented along the AC--PC line). Each functional acquisition lasted
either 8 min 50 s (block design) or 5 min 48 s (event-related design).
Each scanning session, including the structural and functional sequen-
ces, lasted 1.5--2 h.
Statistical Analysis
Functional data were analyzed using the FS-FAST analysis tools. The
methods used here have been used and elaborated on previously
(Bar et al., 2001; Bar and Aminoff, 2003). Data from individual fMRI
runs were first corrected for motion using the AFNI package (Cox,
1996) and spatially smoothed with a Gaussian full-width, half-maximum
filter of 5 mm (block design) or 8 mm (event-related design). The
intensities for all runs were then normalized to correct for signal
intensity changes and temporal drift, with global rescaling for each
run to a mean intensity of 1000. Signal intensity for each condition was
then computed, excluding trials with incorrect behavioral responses,
and averaged across runs. The estimated hemodynamic response was
defined by a gamma function of 2.25 s hemodynamic delay and 1.25 s
dispersion. To account for intrinsic serial correlation in the fMRI data
within subjects, we used a global autocorrelation function that
computes a whitening filter (Burock and Dale, 2000). The data were
then tested for statistical significance and activation maps were
constructed for comparisons of New versus Repeat conditions (t-test
with a minimal threshold set at P < 0.001, uncorrected for multiple
comparisons) for each fMRI design.
Cortical Surface-based Analysis
Once the data from all trials were averaged, the mean and variance
volumes were resampled onto the cortical surface for each subject.
Each hemisphere was then morphed into a sphere in the following
manner: first, each cortical hemisphere was morphed into a metrically
optimal spherical surface. The pattern of cortical folds was then
represented as a function on a unit sphere. Next, each individual
subject’s spherical representation was aligned with an averaged folding
pattern constructed from a larger number of individuals aligned
previously. This alignment was accomplished by maximizing the
correlation between the individual and the group, while prohibiting
Figure 1. Examples of experimental stimuli and procedure. Fixation displays required no response. Object pictures were first presented for different durations: 40, 150, 250, 350,
500 or 1900 ms (First). The same pictures were subsequently repeated for 500 ms (Repeat). Additional pictures appeared only once for 500 ms and provided the control New
condition.Eachpicturewas immediatelyfollowedby acolored non-sensemask, whichtogetheraccumulatedto a2 s totalduration ofeach trial,resultingin asameamount of visual
stimulation for each trial. After each presentation, participants were required to respond ‘natural’, ‘manufactured’ or ‘do not know’ by a keypress.
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changes in the surface topology and simultaneously penalizing exces-
sive metric distortion (Fischl, 1999).
Region of Interest (ROI) Analysis
The ROIs chosen for this analysis were constrained both structurally
and functionally. The structural constraint was based on a hand label-
ing of different brain structures for each subject. These structures
were limited to the temporal--occipital and prefrontal regions that
were expected a priori to show repetition-related response reduction,
and that did indeed show significant (P < 0.01) response reduction in
the present study, as revealed by the New versus Repeat contrast. A
further criterion for inclusion was that these regions had to show
repetition reduction with overlapping extents when compared across
fMRI designs. For the left hemisphere, the structures meeting all of
these requirements (see Fig. 2) included the lateral occipito-temporal
sulcus, the inferior temporal gyrus, the fusiform gyrus, the collateral
sulcus and the inferior frontal sulcus. For the right hemisphere, while
robust repetition reduction was observed in the fusiform gyrus and
the collateral sulcus for both fMRI designs, the extent of repetition
reduction in these structures was anterior and non-overlapping in the
event-related design relative to that observed in the block design. For
this reason, only the left hemisphere structures were included in the
selection of ROIs.
The additional functional constraint for the ROIs was based on
a mask selecting only the subset of the voxels within each anatomical
label that were activated in a positive direction by any component
of the task, as revealed by the main effect (i.e. the contrast of all-
conditions versus fixation-baseline), with a threshold of P < 0.01,
corrected for multiple comparisons. All the voxels that met these
constraints were then averaged, for each anatomical structure,
allowing the contrasts of interest to be computed across the resulting
time courses. The mean percentage of peak signal change was then
calculated for each condition. For the block design, this was calculated
across eight TRs (time points: 2.3--18.4 s). For the event-related design,
this was calculated for the TRshowing peak signal change (time point:
4--6 s).
Results
Our main findings are that: (i) the magnitude of the repetition-
related reduction in fMRI signal increased significantly with
increased duration of prior exposure, peaking at ~250 ms, but
significantly decreased for longer durations of prior exposure;
and (ii) prior visual exposure modulated both fMRI response
reduction and behavioral priming in a highly similar manner.
fMRI Results
Only trials associated with a correct response were included
in subsequent analyses. Categorization performance for both
fMRI designs was consistently high in every condition (<5%
Figure2. New versus Repeat. Statisticalactivation maps illustrating the comparisonbetween Newand Repeat conditions(all repeated conditionscombined, P\0.001). Foreach
fMRI design, the activity was averaged across 12 participants and displayed on ‘inflated’ lateral, medial and ventral views of each hemisphere. The brain was inflated to expose the
sulci, resulting in a smooth surface. Gyri are shown in light gray and sulci in dark gray, and correspond to the averaged curvature of 80 different brains. Lower panel: general
locations of anatomically defined ROIs are shown on the inflated ventral view of an individual brain (left hemisphere) (N: New; R: Repeat; CS: collateral sulcus; FG: fusiform gyrus;
LO: lateral occipito-temporal sulcus; ITG: inferior-temporal gyrus).
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errors for each condition) except for First items shown for
40 ms (>70% errors). Regarding the conditions of primary
interest (New and Repeat), a mixed-factor analysis of varian-
ce (ANOVA) conducted on the mean proportions of errors
revealed that neither the main effects of prior exposure
duration and experimental design nor the interaction term
for these factors were significant (all Ps > 0.1).
Repetition-related Changes in fMRI Signal
As an overall test for repetition-related response reduction,
we first compared fMRI signal change between the combined
Repeat conditions (all prior-exposure durations) and the
New condition. Note that all of these conditions had identical
viewing conditions, with each object presented for 500 ms, and
differed from each other only in the level of prior exposure.
Several brain regions elicited lower activation for Repeat
objects compared with New objects. Of these areas, we focused
our ROI analysis only on those showing overlapping extents of
repetition reduction across both experimental designs (Fig. 2;
New > Repeat): the posterior part of the left inferior temporal
gyrus (Talairach coordinates of greatest common activation,
–58, –49, –4) the left lateral occipito-temporal sulcus (–45, –50,
–12), the left fusiform gyrus (–39, –34, –17) and the left collateral
sulcus (–31, –34, –9). Although robust repetition-related re-
sponse reduction was observed in the right fusiform gyrus
and the right collateral sulcus for both fMRI designs (see Fig. 2),
the extent of the response reduction produced using the event-
related design was anterior to, and non-overlapping with, that
produced using the block design (fusiform: event-related, 36,
–25, –16; block design, 27, –45, –13; collateral sulcus: event-
related, 31, –28, –14; block design, 26, –40, –8). In the frontal
lobe, relatively reduced activation was found in both experi-
mental designs in the left inferior frontal sulcus (–47, 35, 4).
Some brain regions showed higher activation in both exper-
imental designs for Repeat objects relative to New objects
(Fig. 2; Repeat >New). Such increases of the BOLD signal were
detected in the right intraparietal sulcus (32, –52, 43) and in
precuneus (left: –10, –72, 40; right: 3, –56, 46), extending to the
right parieto-occipital sulcus (36, –58, 25). Similar repetition
enhancements in the same regions have been also found in
priming studies during implicit and explicit tasks (Chao et al.,
2002; Henson et al., 2002) and have been hypothesized to
reflect recollection processes (Heun et al., 1999).
Effect of Prior Exposure Duration on fMRI Signal Reduction
To evaluate the impact of level of visual experience on the
subsequent repetition-related response reduction within each
ROI and for each fMRI design, we subtracted the percentage of
fMRI signal change for each Repeat condition from the
percentage of fMRI signal change elicited by the New condition
(see Fig. 3). Maximal prior exposure-related reduction in
fMRI signal was obtained for prior exposures of 250 ms. This
was specifically indicated by two-tailed paired t-tests on the
ROI data within each fMRI design (250 ms Repeat versus the
other Repeat conditions) in the left inferior temporal gyrus,
the left lateral occipito-temporal sulcus, the left fusiform gyrus,
the left collateral sulcus and the left inferior frontal cortex (all
Ps < 0.05). Longer prior exposures durations (350--1900 ms)
not only failed to increase the magnitude of the repetition
reduction, but actually resulted in a significantly smaller effect
in all of these cortical regions. Consistent with the poor
categorization performance for 40 ms First presentations, no
fMRI reduction was detected for repeated objects with 40 ms
prior exposure in the majority of the ROIs, except for the
block design in the left fusiform gyrus (P < 0.05) and the left
inferior temporal gyrus (P < 0.01).
Behavioral Results
On average, correct RTs for Repeat presentations were shorter
than those for New presentations, for both the block (646
versus 696 ms) and event-related (717 versus 770 ms) designs. A
mixed-factor ANOVA indicated that this behavioral priming
effect by prior exposure was significant (P <0.001) and did not
vary across experimental design (P > 0.1). This comparison
indicates robust behavioral priming with both experimental
designs for conditions that were all presented for the same
duration at the testing stage (i.e. 500 ms). Differences due to
experimental design were limited to marginally faster RTs for
the block design than the event-related design (P < 0.07).
Effect of Exposure Duration on Subsequent Priming
To evaluate the effect of prior exposure duration on the
magnitude of behavioral priming, we calculated individual
priming values by separately subtracting RTs obtained for
each of the Repeat conditions from those for the New condition
(Fig. 4). A mixed-factors ANOVA revealed a significant main
effect of prior exposure on priming magnitude (P < 0.001)
within each experimental design, which did not reliably differ
across experimental design (P > 0.21). Because experimental
design had no significant effects on the magnitude of priming
with varying prior exposure (P > 0.21), the data from each
condition were averaged across the different versions of the
experiment to simplify subsequent analyses.
Maximal priming occurred for repeated objects with prior
exposures of 250 ms. Two-tailed paired t-tests indicated that
the magnitude of priming for 250 ms of prior exposure was
greater than that for 40 ms (P <0.01), 150 ms (P = 0.05), 350 ms
(P < 0.05), 500 ms (P < 0.01) and 1900 ms (P < 0.01) of prior
exposure. As in the fMRI response reduction results, repeated
objects with longer prior visual exposure (350--1900 ms) not
only failed to show an increase in behavioral priming, but
actually resulted in less priming compared with repeated
objects with a prior exposure of 250 ms. Of additional interest
is the fact that 40 ms of prior exposure was not sufficient to
produce reliable behavioral priming (P >0.1), just as it was not
sufficient to produce reliable repetition-related reduction in the
fMRI signal. Again, this may be attributable to the poor
categorization performance on first exposure to items in this
condition.
That very brief exposure to objects (40 ms) did not produce
subsequent behavioral priming, despite above-chance perfor-
mance, is interesting in light of the fact that previous studies
have shown that even shorter presentations can induce reliable
priming (Bar and Biederman, 1998, 1999). The procedures used
in such demonstrations of subliminal visual priming, however,
differ in critical ways from those used in the present studies.
For instance, in these subliminal priming studies, the pre-
sentation conditions (e.g. exposure duration, contrast, quality
of masking) were optimized individually for each experimental
object. It has been shown in visual psychophysics that such
subliminal improvements can be obtained only when operating
near the threshold of conscious perception (e.g. Tanaka and
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Sagi, 1998). Therefore, pre-adjustments of viewing parameters
to increase the likelihood that perception will be below
but near the threshold are crucial. No such preparations were
made here. Furthermore, in those previous studies the task
and paradigm were different (naming with a four-alternative
forced-choice), and priming was measured by improvement
in percent of correct responses rather than reaction times
(RTs) (i.e. subjects had unlimited time to consider their
response). Finally, the majority of the incorrect responses
in the 40 ms here were ‘do not know,’ indicating that subjects
responded correctly only when they were confident of their
response. Therefore, any RT priming found in this condition
would have not been considered to be subliminal because
RT was only calculated using correct trials.
We conducted an additional behavioral experiment with 20
additional subjects using randomly intermixed conditions to
ensure that the novel and potentially important rise-and-fall
pattern of priming results would replicate outside of the
magnet. The time interval separating first and second presenta-
tions of each object in this study ranged between 2 and 120 s
(2--60 intervening stimuli). Despite this additional difference,
the results of this behavioral study precisely replicated the
pattern of behavioral results from both versions of the fMRI
study (Fig. 4). These results provide converging evidence that
behavioral priming for repeated objects with 250 ms of prior
exposure was greater than that for 40 ms (P <0.01), 150 ms (P <
0.01), 350 ms (P < 0.01), 500 ms (P < 0.05) and 1900 ms (P <
0.01) of prior exposure. Repeated objects with longer prior
visual exposure (350--1900 ms) resulted in less priming than
repeated objects with a prior exposure of 250 ms.
Correlation between fMRI Signal Reduction and
Behavioral Priming
The results reported above indicate very similar dynamics for
repetition-related reduction in fMRI response and behavioral
priming: both phenomena maximized for a level of visual
experience analogous to 250 ms of previous stimulus exposure
and then decreased for longer prior exposures. To quantify
the link between response reduction and priming, we tested the
correlation between the effects of exposure duration on the
dynamics of both. Averaging the magnitude of repetition
reduction and behavioral priming across all ROIs revealed
common experience-related changes that showed reliable
average correlations (block design: r = 0.41, P < 0.01; event-
related design: r = 0.36, P < 0.05), suggesting a direct connec-
tion between the cortical and the behavioral phenomena.
Discussion
Our results demonstrate that visual experience with an object
has a highly similar influence on the dynamics of overall fMRI
signal reduction and behavioral priming. Both were observed to
be (i) relatively small for briefly presented stimuli that were
hardly recognized; (ii) increase with level of prior visual
exposure to be maximal for a duration of 250 ms; (iii) decrease
in magnitude for prior exposures longer than 250 ms; and
(iv) remain significant for at least 1900 ms of prior visual
exposure. The data reported here reveal a novel and counter-
intuitive property of both repetition reduction and behavioral
priming. Specifically, for both phenomena, this is the first
demonstration that a maximal effect is obtained only for a prior
Figure 3. Exposure-related response reduction within ROIs. Response reduction within each ROI is expressed as differences in percent fMRI signal change for New -- Repeat.
Maximal repetition-related reduction in both designs was found after 250 ms of prior exposure in left CS, left FG, left LOS, and left ITG and left IFS; (a) block design and (b) event-
related design. Average repetition-related response reduction expressed as differences in percent fMRI signal change for New -- Repeat collapsed across ROIs for (c) block design
and (d) event-related design. Error bars represent standard errors of the means.
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exposure of 250 ms, and that the magnitude of these effects is
reduced for longer durations. While our primary focus concerns
experience-related reductions in cortical response and the
general effect of visual exposure on object representations in
the cortex, the striking similarity of the dynamics of repetition
reduction and behavioral priming resonates strongly with the
hypothesis that these two phenomena are critically related.
The cortical regions showing repetition-related response
reduction in our fMRI results include bilateral collateral sulcus
and fusiform gyrus, left lateral occipito-temporal sulcus, inferior
temporal gyrus and inferior frontal cortex. Each of these regions
has previously been found to exhibit reduced activity for
repeated objects when compared with that for novel objects
(Buckner et al., 1998; Vuilleumier et al., 2002; Sayres and
Grill-Spector, 2003; Maccotta and Buckner, 2004). Although we
did not test for distinct processing contributions of different
regions, the sensory processing function typically associated
with relatively posterior occipital--temporal regions suggests
that the specific reduction found there might reflect perceptual
priming. Results of previous fMRI studies also implicate more
anterior regions of temporal--occipital and inferior prefrontal
cortices, especially in left hemisphere, to be associated with
object representations that generalize across different exem-
plars (Koutstaal et al., 2001; Simons et al., 2003) or viewpoints
(Vuilleumier et al., 2002) that involve lexical/semantic in-
formation (Demb et al., 1995; Thompson-Schill et al., 1999;
Koutstaal et al., 2001), or that concern task-specific (Wagner
et al., 2000) and response-related (Dobbins et al., 2004)
information associated with an object. We therefore take
response reductions in these regions to reflect perceptually
abstract and non-perceptual (e.g. conceptual, linguistic and
response-related) components of priming (cf. Schacter et al.,
2004). As shown in Figure 3, all of these regions produced
similar ‘rise-and-fall’ patterns of exposure-related fMRI repeti-
tion reduction, suggesting that each of these areas either
mediates, or is affected by, the processes involved in the
response reduction. Thus, while the nature of the object-related
information represented in these various cortical regions
may differ, the processes that shape the representations found
in each may be the same.
The different versions of our study yielded highly similar
results. This suggests that our results are robust in the face of
differences in the time interval separating the first and second
presentations of each object, and differences in expectancies,
strategies and contrast effects that the different experimental
designs afford. In particular, the similarity across the event-
related and blocked designs demonstrates that the ‘rise-and-fall’
pattern of results we obtained was not due to exposure-related
differences in how subjects allocated their attention. Atten-
tional confounds can be problematic for the results of block
design experiments, because subjects typically know what
condition to expect on every trial. However, there was no
way for subjects in the event-related design to know what
duration to expect for a forthcoming stimulus, because the
presentation orders of the different conditions in these designs
were intermixed. Thus, there was no way to allocate different
levels of attention voluntarily when stimuli appeared for
different exposure durations. The similarity in the results from
the different designs therefore provides strong evidence, not
only that the ‘rise-and-fall’ pattern of repetition reduction and
behavioral priming replicates, but also that these effects are not
an artifact of differences in the top-down allocation of attention.
Findings of repetition-related response reduction have been
speculated to reflect a ‘sharpening’ of the cortical response
(Desimone, 1996). This hypothesis regarding the functional
significance of repetition reduction was later interpreted
(Wiggs and Martin, 1998) to suggest that the reduced response
is a manifestation of a selective representation, in which only
key object features continue to be represented with repeated
experience. These two proposals differ from each other in that
one focuses on a ‘sharpened’, and presumably exhaustive,
representation, whereas the other focuses on a selective, non-
exhaustive representation. Although neither of these proposals
wouldindividuallypredictapatternofexposureeffectssimilarto
that reported here,our findings support thecoexistence of both
mechanisms. As elaborated below, we suggest that these
mechanisms operate separately from each other, and together
create object representations that are both ‘sharpened’ and
selective.
According to the present proposal, visual exposure to
a certain object first recruits a sharpening process during which
the initially broad cortical response becomes fine-tuned and
maximally stimulus-specific. The cortical response to a visual
input is initially driven by coarse information and global aspects
of the image and, in that sense, is not optimal and therefore
requires fine-tuning. Indeed, psychophysical experiments with
stimuli ranging from simple gratings (DeValois and DeValois,
1988) to complex scenes (Schyns and Oliva, 1994) indicate that
observers perceive global components considerably earlier than
they perceive the stimulus-specific detail (Watt, 1987; Bar, 2003;
Loftus and Harley, 2004). Recent neurophysiological studies
(Brown and Xiang, 1998; Sugase et al., 1999; Tamura and
Tanaka, 2001) support this idea by showing that activity in
inferior temporal is initially, at ~130 ms from stimulus onset,
broad and relatively less selective to the specific stimulus,
representing only its global properties (e.g. general orientation
and dimensions). Then, at ~240 ms from stimulus onset, the
representation becomes stimulus-specific, such that only those
neurons that best represent the specific properties of the
stimulus continue to respond (Tamura and Tanaka, 2001).
Figure 4. Behavioral data. Mean magnitude of behavioral priming for correct trials on
the object categorization task (mean RT difference in ms for New -- Repeat conditions;
all items presented for 500 ms) as a function of prior exposure duration (yellow: block
design fMRI; red: event-related fMRI; blue: the behavioral study, intermixed
conditions). Each version of the experiment shows maximal priming for 250 ms of
prior exposure. Error bars represent standard errors of the means.
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Fine-tuning may also benefit from the attentional selectivity of
neurons in inferior-temporal cortex, which follows a compara-
ble timecourse (Chelazzi et al., 1998): While cells initially show
a similar response, regardless of the relevance of a particular
stimulus, this response becomes highly selective in accordance
with attentional demands within 200 ms from stimulus onset.
Taken together, these timecourses are especially compelling in
their similarity to our findings that exposure effects peaked for
objects previously presented for 250 ms, suggesting that
maximal fMRI signal reduction coincides with the completion
of fine-tuning. The outcome of this fine-tuning process is an
efficient but exhaustive representation of the stimulus. The
representation is efficient in that each object’s feature is
represented optimally, but is also redundant because it includes
all of the features in the image. Based on the inverted U-shaped
pattern of exposure effects we observed, it is proposed that
a subsequent selection process eliminates this redundancy.
Given sufficient exposure to a specific object, this second
process selects the key features from the fine-tuned, exhaustive
representation of the object in a similar manner as suggested
previously (Wiggs and Martin, 1998). Subsequently, only the key
features continue to be represented, while the neurons repre-
senting redundant features gradually respond less. Signals for
guiding the selection of these key features may be projected
back from the prefrontal cortex, which processes, among other
things, semantic information about objects (Demb et al., 1995;
Wagner et al., 2000), as well as from the amygdala, which
analyzes emotionally relevant information (Hariri et al., 2002).
For the present purpose, key features are defined as either
diagnostic features that distinguish the specific object from
other objects, features that are critical for the specific task at
hand, features that remain invariant under various viewing
conditions, features of outstanding interest, or odd, surprising
and unexpected features. For example, while the shape of the
legs of a certain chair may be considered a key property and will
continue to be represented, maintaining details about all four of
its similarly looking legs is not essential for an economic and
reliable representation. Being selective about which informa-
tion is represented may also serve to emphasize the unique
features of a certain object and thus make it more recognizable,
just as a caricature of a face, eliminating non-distinctive
extraneous information, can be recognized more accurately
than its detailed, veridical version (Rhodes et al., 1987). Thus,
allocating neurons for representing redundant or non-essential
features can be seen as a waste of resources (Lennie, 2003),
and it is predicted that representations are formed to minimize
such cortical commitment whenever optimization is possible.
The selection process that we describe is proposed to help
shape object representations. However, the term selection has
also been associated, in a different context, with a mechanism
that operates in left inferior frontal cortex to select among
multiple lexical/semantic representations that compete for
access to further processes based on their relevance to task
and stimulus demands (Thompson-Schill et al., 1999). Greater
selection in this latter regard refers to the need to select an
appropriate representation from many different representa-
tions. This between-representation process is therefore notably
distinct from the within-representation process that we de-
scribe. Importantly, while selection between different semantic
representations may occur primarily in left inferior frontal
cortex, the shaping of object-related representations by the
selection of which properties should continue to be repre-
sented may occur throughout various cortical regions involved
in object priming and recognition.
The exposure-related fine-tuning and selection processes
described here may overlap in time, but they are completed
consecutively. Fine-tuning is guided by the arrival of gradually
increasing details about the visual stimulus, and is therefore an
inherently bottom-up process that is completed relatively early
(e.g. our results suggest by ~250 ms). The selection process, on
the other hand, depends on high-level information and semantic
knowledge, and is therefore predicted to be guided by top-
down mechanisms and be completed relatively later (i.e.
350 ms and beyond based on our data). While future research
is needed to address whether the precise time course of these
processes depends on task demands or the processing com-
plexity of individual objects, the present findings nevertheless
suggest that the combined outcome of these two processes is
an efficient and selective long-term representation.
How does this two-process model account for the parabolic
pattern of our results? A mask presented after a picture
interrupts further visual processing (Rolls and Tovee, 1994;
Kova ´ cs et al., 1995). If we assume that priming captures the
most developed representation up to this interruption, then
measures of priming can be considered to reflect the latest
outcome of the processes that shape visual representations
(Bar, 2001). When a mask interrupts processing at 250 ms,
a comprehensive fine-tuning process has been completed, but
the selection process has not yet developed. The resulting
primed representation is therefore based on a fine-tuned
representation of all the features. Accordingly, the next time
subjects see that specific object the activation of this complete
and fine-tuned object representation elicits a minimal cortical
response. In other words, presenting the image first for 250 ms
results in maximal repetition reduction relative to novel
controls because all of the object’s features have been stored
in a fine-tuned manner.
When, on the other hand, the mask interrupts visual
processing at 350 ms or longer, after the subset of the relevant
key features has been selected, the resulting stored represen-
tation is partial because it only includes key features. In other
words, key features are primed and represented in their fine-
tuned form, whereas ‘non-key’ features are no longer part of the
object representation and are therefore primed relatively
weakly, if at all. When a subject sees the specific object again,
the primed features elicit a minimal response but the ‘non-key’
features elicit a response comparable to that of a previously
unseen feature. This combination of activating primed and less-
primed features results in a cortical reduction and RT improve-
ment lower than the maximum, but higher than that obtained
for a novel object.
We have described the operations of the fine-tuning and
selection mechanisms primarily in terms of the formation of
perceptual representations of objects. However, the proposed
fine-tuning and selective processes are also presumed to
operate to shape other types of object-related representations,
such as those involved in the conceptual, linguistic and
response-related components of priming (for a review of
priming specificity, see Schacter et al., 2004). Support for this
comes from the fact that we obtained the same ‘rise-and-fall’
pattern of exposure-related response reductions in several
cortical regions, including anterior temporal and inferior fron-
tal regions that have been implicated in non-perceptual oper-
ations. This possibility underscores the potential generality and
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importance of our proposal, and emphasizes the need for future
research to establish the extent to which the fine-tuning and
selective processes might reflect the general operating charac-
teristics of neural ensembles in shaping different types of
cortical representations.
While our primary focus in this investigation concerns
experience-related reductions in cortical response, our behav-
ioral results also merit consideration. Indeed, despite decades of
research interest in the behavioral manifestations of priming,
evidence regarding the effects of initial exposure duration on
subsequent recognition performance for repeated objects is
lacking. As a result, the ‘rise-and-fall’ pattern of exposure-related
behavioral priming effects that we obtained is itself a novel
finding. Despite the lack of comparable prior object recognition
studies, several studies using visually abstract or linguistic
stimuli have manipulated prime exposure duration and are
therefore relevant to the present results. However, many of
these studies used only very brief prime exposure durations
(<100 ms, e.g. Frost et al., 2003), relatively long exposures
(>1000 ms, e.g. Jacoby and Dallas, 1981; Neill et al., 1990;
Musen, 1991) or only two different exposure durations (e.g.
Hirshman and Mulligan, 1991, Experiment 3; Versace, 1998;
Versace and Nevers, 2003), and none used reaction times to
measure priming. Unfortunately, the absence of multiple prime
durations and/or lack of a similar range of durations as used in
our study impedes proper comparison of these results to our
general ‘rise-and-fall’ pattern of behavioral priming effects.
Of the remaining studies that used relatively more compara-
ble procedures, three provided results that are nominally
consistent with our behavioral findings. Two studies reported
by Crabb and Dark (1999; 2003, Experiment 2), for instance,
together show a similar ‘rise-and-fall’ pattern of priming effects
on identification accuracy for words. In their first study (Crabb
and Dark, 1999), repeated target words that were actively
attended to in prime displays were correctly identified more
often than new, unprimed items. Importantly, for these items
there was a priming-related ‘rise’ in the proportion of identified
repeated items, relative to the proportion of identified new
items, when the prime exposure duration increased from 100
ms (0.095) to 200 ms (0.126), and there was a ‘fall’ in priming
magnitude when the duration increased further to 300 ms
(0.100). Another of their studies that used longer prime
exposure durations (Crabb and Dark, 2003, Experiment 2)
showed additional evidence for the ‘fall’ of priming, with
nominally greater priming for words that were initially pre-
sented individually for 200 ms than for those presented for 600
or 1000 ms. Although the statistical reliability of these prior
trends was not established, the general similarity between these
results and ours supports the potential generality of our
findings. Even more compelling in this regard are the results
of von Hippel and Hawkins (1994, Experiment 1). Prime words
in their study were presented under perceptual study con-
ditionsfor 50, 100,200, 500 or1000 ms. Theproportion of these
prime words that were subsequently used to complete word
fragments (e.g. ma__l_ / marble) showed a ‘rise’ in priming,
with steady increases with prime exposure from 50 ms to the
maximal priming effect at 200 ms. The ‘fall’ of priming was also
clearly evident in these results, with consecutive decreases in
the proportion of primed fragment completions following 200
ms of prime exposure to that following 500 and 1000 ms of
prime exposure, respectively. Furthermore, the quadratic trend
defining this ‘rise-and-fall’ pattern of priming effects was found
to be statistically reliable. Although this pattern was not as clear
in other conditions in von Hippel and Hawkin’s (1994) study,
such as when subjects were required to type the name of
previously primed words that were briefly flashed again for 33
ms, our survey of the behavioral priming literature nevertheless
suggests that our proposal is further supported by previous
reports.
We have interpreted the ‘rise-and-fall’ patterns of repetition-
related response reduction and behavioral priming that we
obtained as reflections of how cortical representations are
shaped with increasing visual experience. Our account suggests
that a ‘rise-and-fall’ pattern might be expected in any situation
where a repeated stimulus and task-related demands are highly
similaracrossbothpresentations,whereafine-tunedresponseto
redundant and otherwise irrelevant features and information
provides a greater overlap between an object’s cortical repre-
sentation and the corresponding visual input, and where
selection of only ‘key’ features for continued representation
reduces this overlap. Importantly, our account does not suggest
that increase exposure inevitably decreases behavioral perfor-
mance with sufficient visual exposure. Indeed, the effect of
the proposed selection process might often make object iden-
tification more efficient; that is, retaining only the most dis-
tinctive, relevant features and information about an object will
generally make it easier to distinguish from other objects. Thus,
eliminatingtheinfluenceofredundant,lessrelevant information
can aid identification. However, in our task, this normally
redundant and less relevant information is in fact helpful, as it
provides a greater overlap between an object’s cortical repre-
sentation and the corresponding visual input. Maximal priming
should therefore be observed in such situations whenever the
object is most accurately and exhaustively represented (i.e.
following maximal fine-tuning and minimal feature selection).
The reliable correlation and striking similarity in the ‘rise-
and-fall’ pattern of repetition-related response reduction and
behavioral priming we observed suggests that these phenomena
are critically related. If the evolution of an object’s cortical
representation is related to recognition ability, then at least
some level of representational fine-tuning may be required
before recognition of an object is possible. Consequently, if the
representation activated in a second encounter is fine-tuned, RT
is shorter than that observed for a novel stimulus because less
time is required for recognition. Our proposal that fine-tuning is
completed by 250 ms is supported in this regard by the fact that
RTs were indeed fastest for objects shown previously for 250
ms, in addition to priming being maximal in this condition. The
link to behavioral RT improvement is bolstered by the finding
that the cortical response to visual objects is not only reduced
with repeated exposure, but also peaks earlier (Noguchi et al.,
2004). Similarly, in a study of the cell population in IT, activity
there initially distinguished between novel and familiar
objects ~100 ms after the onset of their response (~180 ms
from stimulus onset; Li et al., 1993). The 100 ms delay of this
diagnostic activity, however, was reduced to only 10 ms
following additional presentations. This shortening of response
onset to a familiar stimulus may therefore reflect the efficiency
involved in behavioral RT priming.
Conclusions
Our results demonstrate that visual experience with an object
has a highly similar influence on two important phenomena: the
Cerebral Cortex November 2005, V 15 N 11 1663

Page 10

relatively reduced cortical response to repeated stimuli and
the corresponding behavioral priming. While future research is
required to demonstrate that our findings generalize to differ-
ent experimental designs and cognitive tasks, these findings
converge to improve our understanding of the mechanisms
mediating both. A more important result observed here is our
novel finding of the ‘rise-and-fall’ pattern, in which maximal
repetition-related cortical and behavioral effects were both
obtained at a specific level of visual experience, analogous to
prior exposure of 250 ms, and were reduced at longer exposure
durations. Consequently, we suggest a model in which experi-
ence with a specific visual stimulus recruits two separate
mechanisms that together create cortical representations that
are both efficient and selective.
Notes
We thank R. Henson, A. Martin, C. Tyler and N. Tzourio-Mazoyer for
helpful comments and stimulating discussions; M. Vangel and D. Greve
for statistical advice; B. Quinn and the Imaging Core at the Martinos
Center at MGH for technical assistance; and H. Linz for assistance with
data collection. Supported by the James S. McDonnell Foundation 21st
Century Science Research Award in Bridging Brain, Mind and Behavior
#21002039 (to M.B.), NINDS R01 NS44319 (to M.B.) and the MIND
Institute.
Address correspondence to Moshe Bar, Martinos Imaging Center at
MGH, Harvard Medical School, 149 Thirteenth Street, Charlestown, MA
02129, USA. Email: bar@nmr.mgh.harvard.edu.
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