Abstract

The speed and accuracy with which subjects can read words is enhanced or “primed” by a prior presentation of the same words. Moreover, priming effects are generally larger when the physical form of the words is maintained from the first to the second presentation. We investigated the neural basis of format-specific priming in a mirror word-reading task using event-related functional magnetic resonance imaging (fMRI). Participants read words that were presented either in mirror-image (M) orientation or in normal (N) orientation and were repeated either in the same or the alternate orientation, creating 4 study–test conditions, N-N, M-N, N-M, and M-M. Priming of N words resulted in reductions in fMRI signal in multiple brain regions, even though reading times (RTs) were unchanged. Priming of M words showed a pattern of RTs consistent with format-specific priming, with greater reductions when the prime matched the form of the test word. Priming-related reductions in fMRI activity were evident in all regions involved in mirror-image reading, regardless of the orientation of the prime. Importantly, reductions in several posterior regions, including fusiform, superior parietal, and superior temporal regions were also format specific. That is, signal reductions in these regions were greatest when the visual form of the prime and target matched (M-M compared with N-M). The results indicate that, although there are global neural priming effects due to stimulus repetition, it is also possible to identify regional brain changes that are sensitive to the specific perceptual overlap of primes and targets.

Introduction

Previous experiments have indicated that the speed and accuracy with which subjects identify words is enhanced or “primed” by a prior presentation of the same words. Moreover, priming effects are generally larger when the physical form of the word remains the same from the first to the second presentation. This is true for study–test manipulations of sensory modality (e.g., visual vs. auditory; Clarke and Morton 1983; Graf and others 1985; Roediger and Blaxton 1987; Schacter and Graf 1989), symbolic form (pictures vs. words; Weldon and Roediger 1987), script orientation (backwards or upside down vs. normal; Kolers 1975, 1979; Masson 1986; Graf and Ryan 1990), and sometimes type font or case (e.g., upper vs. lower case, handwritten vs. typed; Graf and Ryan 1990; Marsolek and others 1992, 1996; Gibson and others 1993; Curran and others 1996; Wiggs and Martin 1998; but see Scarborough and others 1977; Tardiff and Craik 1989; Rajaram and Roediger 1993, for failures to find type-specific priming).

Graf and Ryan (1990) have used a transfer appropriate processing (TAP) framework (cf., Morris and others 1977) to account for format-specific priming. TAP is based on the notion that remembering is best understood in terms of the cognitive operations that are engaged by different study and test activities (Kolers and Ostry 1974; Kolers 1975, 1979). Reading a word or sentence, for example, requires a particular set of sensory-perceptual and semantic-analyzing operations. Engaging these operations has the same effect as practicing a skill—it increases the fluency and efficiency with which they can be carried out subsequently. Performance on a priming test is facilitated to the extent that it engages the same set of cognitive operations as used on the preceding study task. The greater the overlap in processes from study to test the greater the facilitation. Importantly, priming is also dependent upon how practiced these processes are—cognitive operations that are executed with a high degree of efficiency and skill will show little, if any, priming, whereas uncommon or unskilled operations will show greater facilitation after a single practice episode (Graf and Ryan 1990; Ostergaard 1998, 1999).

Several accounts of priming offer hypotheses as to the brain regions that may mediate these effects. One such account, described by Tulving and Schacter (1990; Schacter 1994), postulates that priming is mediated by changes in the perceptual representation system (PRS). The PRS is described as a collection of domain-specific modules or subsystems that operate on perceptual information about the form and structure, but not the meaning and associative properties, of words and objects. Schacter and others (e.g., Schacter 1994; Schacter and Buckner 1998) argue that priming on most standard tasks such as word identification or fragment completion primarily reflects increased efficiency in the perceptual analysis of the word and, by extension, will be mediated by posterior cortical regions. Recent imaging studies using positron emission tomography and functional magnetic resonance imaging (fMRI) are consistent with this notion. Collectively, these studies have demonstrated that priming is accompanied by blood flow decreases in bilateral posterior perceptual processing areas in extrastriate occipital cortex, using such tasks as word stem completion, visual word-fragment completion, verb generation, and object classification (Buckner and others 1995; Martin and others 1995; Blaxton and others 1996). Interestingly, primary visual regions have not shown subsequent priming-related reductions in blood flow, suggesting that early visual areas as defined by retinotopic organization may not be involved in perceptual priming (Halgren and others 1997; Buckner and others 1998).

It is also clear, however, that frontal regions, particularly left prefrontal cortical areas, are sometimes affected by priming, depending upon the specific demands of the task. Priming-related decreases in blood flow in left prefrontal regions have been demonstrated in various tasks including verb generation (Raichle and others 1994), abstract versus concrete classification of words (Demb and others 1995; Wagner and others 2000), object picture classification (Wagner and others 1997; Buckner and others 1998), and word stem completion (Buckner and others 1995). One possible commonality across these tasks is that they all require some sort of semantic elaboration or conceptual analysis, and conceptually based priming may therefore be mediated by prefrontal regions, especially left inferior prefrontal cortex.

In combination, neuroimaging findings are consistent with a TAP view of priming, suggesting that brain regions showing priming-related reductions in activity are specific to the cognitive requirements of the task, such as perceptual priming mediated by posterior cortical regions, with separate and distinct anterior regions involved in conceptual priming. Few imaging studies, however, have directly manipulated the task demands in a within-subject design. In one such study, Wagner and others (2000) focused on the role of anterior and posterior left prefrontal regions in conceptual priming. Participants initially classified a series of words in a perceptual decision task (upper or lower case) or a conceptual decision task (abstract or concrete). During subsequent scanning, participants made abstract/concrete judgments for words from 3 sources; words that had been previously encountered during the conceptual decision task, words that had been encountered during the perceptual decision task, and words that had not been encountered in either decision task. The results indicated that the left anterior inferior frontal gyrus was activated by the abstract/concrete decision task, and this activity was not reduced as a consequence of prior exposure to the words in the perceptual decision task. By contrast, activation was significantly reduced when the exact same items and task demands were repeated, suggesting that priming and related blood flow reduction in this region depended crucially on the overlap of semantic operations from study to test episodes.

The present study was designed to further illustrate the generality of a TAP view of priming using fMRI. Rather than varying the conceptual component of the task demands as in Wagner and others (2000), we varied the overlap in perceptual operations involved in identifying words presented in 2 visually distinct formats, using a standard word-reading paradigm. Although priming during word reading may be mediated primarily by perceptual processes (Blaxton 1989), according to TAP, both perceptual and semantic processing should play at least some role in priming because both operations are automatically engaged when reading a word. The degree to which conceptual and perceptual processes are the basis for priming will vary depending on the difficulty of the task and—critical to the present study—the overlap of specific perceptual and semantic processes engaged at study and test.

We presented participants with a continuous reading task, in which a list of single words were first presented either in normal orientation (N) or in mirror-image orientation (M) and then were repeated later on in the list either in the same orientation (N-N and M-M) or in different orientations (N-M and M-N). In a similar behavioral paradigm, Graf and Ryan (1990) showed that the reading accuracy with words that were presented mirror image and upside down differed depending on the orientation of the prime. Primes presented in the same unusual orientation produced a greater increase in reading accuracy than primes presented in normal upright orientation. Graf and Ryan (1990) also provided evidence that orientation manipulations of this type induced a letter-by-letter reading strategy, rather than the usual whole word–reading approach (for a discussion of word-reading strategies, see also Shallice 1988). In the case of reading M words, letters must be rotated in order to identify them, and the normal direction of reading is disrupted (words must be read from right to left rather than left to right). When M words are primed with identical words in M orientation, there is considerable overlap in perceptual processes required in order to identify the unique visual form of the word, as well as overlap in the semantic analysis of word meaning. According to TAP, we would expect to see decreases in activation in left prefrontal regions associated with processing word meaning and in posterior regions including temporal, parietal, and fusiform regions that are associated with the perceptual analysis of visual form. In contrast, when M words are primed with words that were presented previously in N orientation, there should be considerably less repetition of perceptual processes carried out during reading. Hence, priming should be mediated to a significantly lesser degree by posterior regions involved in perceptual analysis and should rely instead on frontal regions involved in semantic processing.

According to a strict TAP view of priming, the same general hypothesis should hold for N words as well—priming should result in greater reductions in posterior regions when the prime and target are the same, as opposed to when the prime and target differ in physical form. However, Graf and Ryan (1990) found that primes presented in unusual orientations produced greater priming overall than primes in normal orientation, even when the target word was presented in normal orientation. If activation reductions track the magnitude of behavioral priming, we might expect to find greater reductions in activity when N words are preceded by M primes compared with N primes. It is unclear, however, what to expect in terms of cortical regions mediating this enhanced priming effect.

Method

Participants

Volunteers included 12 right-handed individuals, aged 21–30 years, who were paid $40 for their participation. Participants were screened to exclude drug and/or alcohol abuse, neurological disorder and serious head injury, psychiatric illness, and contraindications to undergoing magnetic resonance imaging (MRI).

Materials

Four word lists were created from 800 words, 5–8 letters in length, with medium to high word frequency (20–300 occurrences per million; Kucera and Francis 1967). Words were randomly assigned to 4 lists, ensuring that lists were similar in distribution of word lengths and word frequencies. Within a list, each word was repeated once with varying lags of 8–18 intervening words. Thus, the first 8 words were novel, and then words began to repeat in pseudorandom order, until all words in the list were presented twice. First and second presentations of words were randomly distributed throughout all 4 lists in an event-related design; therefore, any skill learning that may contribute to mirror reading is balanced across all conditions. On the first presentation, half of the words were presented in N orientation, whereas half of the items were presented in M orientation. On the second presentation, words were presented either in the same orientation from first to second presentation or the orientation was reversed from first to second presentation, creating 4 study–test orientation conditions (N-N, M-N, M-M, and N-M). Interspersed randomly throughout all 4 lists were 400 stimuli that provided a visual motor control (!+!+!+!+). Examples of the stimuli are depicted in Figure 1. Thus, each list contained a total of 500 items; 100 control stimuli plus 50 N-N, 50 M-N, 50 N-M, and 50 M-M trials.

Figure 1.

Example of the displays used to present normal and mirror-image text. Screens with arrows were visible for 500 ms and alerted the participant to the orientation of the next word. Text screens were visible until the participant pressed a key or for 2500 ms if they were unable to identify the word. Randomly interspersed with text screens were visual spatial control items (!+!+!+!+) which were preceded equally often by arrows on the right and left side of the screen.

Figure 1.

Example of the displays used to present normal and mirror-image text. Screens with arrows were visible for 500 ms and alerted the participant to the orientation of the next word. Text screens were visible until the participant pressed a key or for 2500 ms if they were unable to identify the word. Randomly interspersed with text screens were visual spatial control items (!+!+!+!+) which were preceded equally often by arrows on the right and left side of the screen.

Procedure

Stimuli were presented in the scanner on magnetic resonance (MR) Vision 2000 goggles (Resonance Technology Inc., Northridge, CA) that were mounted to the head coil so that they rested comfortably over the participant's eyes. All stimuli were presented in lower case letters centered on the screen in bright green 80-point font (MS Word Arial Bold) on a black background. Each list item was visible for up to 2500 ms. Piloting in normal young participants indicated that these parameters resulted in an optimal level of mirror word reading (98% of items were correctly read). Items were preceded by an arrow for 500 ms that oriented participants to the location of the beginning of the word (see Fig. 1). An orienting stimulus was added because pilot data indicated that this substantially increased the number of words that could be successfully read in M orientation. On visual motor control trials, the orienting stimulus was also presented and appeared equally often on the left and right. Presentation rate of the stimuli was self-paced. A button response to an item advanced the presentation to the next list item. If a participant could not identify a word within the 2500-ms time limit, the next item appeared. Response times were collected for all trials using a computer mouse modified for use in the scanner and placed in the participant's right hand. All 4 lists were separated by a 2- to 3-min break.

Prior to scanning, participants were given a short practice run that included words in N orientation, M orientation, and control items. They were instructed that they should read each word as quickly as possible, pressing the mouse button in their hand when they successfully read the word. They were informed that each word would be preceded by an arrow located at the beginning of the word and that moving their eyes to the arrow position would help them to read the words quickly and more accurately. Participants pushed a single mouse button (right hand index finger) when they successfully read a word in either orientation. When the control item appeared, participants were instructed to press another button (right hand ring finger) as quickly as possible. Participants were told that some of the words would be difficult to read in the allotted time and that they should go on to the next item when it appeared. They were also informed that sometimes the words may be repeated, but their primary task was to read each word as quickly as possible.

Imaging Acquisition and Analysis

Images were acquired on a GE Horizon 1.5-T whole-body echo-speed MRI system, using single-shot spiral acquisition (Glover and Lee 1995). Images (17 sections, 5 mm, skip 1 mm) were collected obliquely and aligned on the AC-PC plane covering approximately the whole head (time repetition [TR] = 2000, time echo [TE] = 40, flip angle = 90). The first functional scan was collected with a total of 498 repetitions taking 16 min and 30 s to complete. For subsequent scans, the repetitions were adjusted downward depending on the reading speed of the particular participant. Afterward, T1-weighted images were obtained (256 × 256, TE = 10, TR = 500, field of view [FOV] = 22) using the same slice selection as the functional data set, and a high resolution spoiled gradient recalled (SPGR) series covering the whole brain (1.5-mm sections, 256 × 256, Flip = 30, TE = 6000, TR = 22, FOV = 25 cm) were also collected in order to locate anatomical regions of activation and to overlay functional images for reregistration in standard Talairach and Tournoux (1988) coordinate space.

Regions of Activation

Images were reconstructed offline and then corrected for minor head movement using a 3-dimensional volume registration algorithm (AFNI, Cox 1996). Data were normalized by scaling the whole brain signal intensity to a fixed value of 1000 to allow data to be combined across participants. Then the linear slope was removed on a voxel-by-voxel basis, and spatial filtering was accomplished using a Hanning filter with a 1.5-voxel radius. After normalization, detrending, and filtering, data were analyzed using software developed and validated by Burock and others (1998) for rapid presentation event-related fMRI designs (for details of methods, see Dale and Buckner 1997; Dale 1999). Epochs of 16 s poststimulus onset and 6 s prestimulus baseline were modeled as a linear combination of a time-invariant hemodynamic response (HDR) with Gaussian noise. An estimate of the HDR and variance with the mean signal intensity removed for each condition was modeled using simultaneous least squares fitting of the original MR signal across the epochs. Only words that were successfully read by the individual were included in the event-related analysis.

Regions of activation associated with reading were identified in each individual by contrasting all M words with the control condition and, separately, all N words with the control condition, using a t-statistic weighted for an ideal HDR modeled as a gamma function with 2.25 s onset time and a tau of 1.25 s (Dale and Buckner 1997). Maps of active voxels were created by calculating the covariance between the estimated signal response and the ideal HDR function. The statistical threshold was determined using AlphaSim, which estimates the statistical power for fMRI data by Monte Carlo simulation (AFNI, Cox 1996). This calculation indicated that a 3-voxel cluster size using an individual voxel threshold of P < 0.0001 would result in statistical maps with a corrected significance level of P < 0.05 (corrected for multiple voxel comparisons).

HDR Differences

Image sets were translated into Talairach coordinates (Talairach and Tournoux 1988) using AFNI software. Statistical maps from individuals were then overlaid on an averaged brain image to create a group image, indicating the overlap of significantly active voxels across participants. This group image was then used to determine common regions of interest (ROI) for further analysis. Time series data for all active voxels within each ROI were imported into SPSS for statistical analysis. For each individual, average HDR estimates (0–16 s poststimulus onset) were calculated for each ROI by averaging all significantly active voxels within that region. Because we were interested in the amplitude of the activation, all analyses were conducted on the mean HDR amplitude of signal, which was averaged across time points 2, 4, 6, and 8 s poststimulus onset, and baselined to an average of 4 prestimulus onset points (−6, −4, −2, and 0 s). (To ensure that prestimulus baseline differences could not account for differences in activation amplitudes for the critical test conditions, we compared the averaged baseline values at −6, −4, −2, and 0 s using a 1-way analysis of variance [ANOVA]. Baseline values did not differ between M words, N words, and the control condition [F < 1].)

Results

Behavioral Results

Mean reading times (RTs) were calculated for 6 groups of words: first presentation of N words (N baseline), first presentation of M words (M baseline), and the second presentation of words in the 4 priming conditions (N-N, M-N, M-M, and N-M). Mean RTs, listed in Table 1, were calculated for each individual excluding words for which they did not make a response (approximately 2% of M words, less than 0.5% of N words). Not surprisingly, on first presentation, M words took significantly longer to read than N words, paired t11 = 7.68, P < 0.0001. Priming was assessed for N and M words separately using 2 repeated-measures ANOVAs comparing the 3 conditions (baseline, N primed, and M primed). For words presented in N orientation, there was no measurable priming effect; N baseline, N-N, and M-N conditions did not differ, F < 1. For words presented in M orientation, a previous presentation of a word significantly decreased RTs, F1,11 = 86.77, mean square error (MSe) = 239.34, P < 0.0001. Follow-up paired t-tests indicated significant priming for both N-M and M-M conditions compared with baseline, t11 values = 9.31 and 8.53, respectively, P value < 0.0001. Importantly, there was also a difference in reading speed between N-M and M-M conditions. M-M words were read significantly faster than N-M words, t11 = 4.66, P < 0.001, indicating a format-specific priming effect.

Table 1

Mean RTs and standard deviations (SDs) for words in 2 baseline orientations, mirror image (M) and normal (N), and 4 priming conditions (N-N, M-N, M-M, N-M)

 N orientation M orientation 
 Mean SD  Mean SD 
Baseline 457.67 59.59 Baseline 841.17 203.95 
N-N 450.92 60.52 M-M 727.15 169.44 
M-N 454.00 61.68 N-M 782.33 200.93 
 N orientation M orientation 
 Mean SD  Mean SD 
Baseline 457.67 59.59 Baseline 841.17 203.95 
N-N 450.92 60.52 M-M 727.15 169.44 
M-N 454.00 61.68 N-M 782.33 200.93 

Regions Involved in N and M Reading

Regions showing significant activation during N and M reading compared with the control condition are listed in Table 2. There was considerable overlap in active regions associated with reading N and M words. Areas of activation were present in the M condition (right superior temporal, right middle frontal, and right fusiform gyri) that showed no activation during N reading. In addition, the mean HDR was significantly greater when reading M words compared with N words in bilateral superior parietal and left superior temporal regions.

Table 2

Regions active during the 2 reading conditions, mirror-image (M) and normal (N) orientations, compared with the visual control condition, with mean cluster size (and standard deviations [SDs]), Talairach and Tournoux (1988) coordinates, and corresponding Brodmann areas (BAs)

Anatomical region Mean cluster size in voxels (SD) Regions active during reading M and N words compared with control conditionb Talairach coordinatesa and BAs Regions showing significant reductions in activation level compared with the appropriate baseline condition (N or M) Format-specific primingb
 
  M > N x y z BA N-N M-N N-M M-M M-M > N-M 
L occipital/temporal and fusiform 184 (39) Yes Yes — −41 −7 −1 19 — — <0.0001 <0.0001 Yes 
L superior temporal 28 (5) Yes Yes Yes −52 −35 12 22 <0.01 <0.01 <0.0001 <0.001 — 
L superior parietal 129 (39) Yes Yes Yes −30 −62 47 40/7 — — <0.01 <0.01 Yes 
L anterior inferior frontal 36 (16) Yes Yes — −36 33 45/47 <0.01 — <0.05 <0.05 — 
L posterior prefrontal 88 (22) Yes Yes — −40 10 27 44/6 — — <0.01 <0.0001 — 
R occipital/temporal and fusiform 138 (34) Yes — Yes 41 −68 −1 19 — — <0.001 <0.001 Yes 
R superior temporal 35 (11) Yes — Yes 57 −37 12 22 — — <0.05 <0.05 Yes 
R superior parietal 92 (32) Yes Yes Yes 22 −65 52 40/7 <0.01 <0.05 <0.01 <0.01 Yes 
R anterior inferior frontal 32 (18) Yes Yes — 35 27 45/47 <0.05 — <0.05 <0.01 — 
R middle frontal 40 (13) Yes — Yes 40 27 20 45/46 — — <0.01 <0.01 — 
R superior frontal 82 (39) Yes Yes — 36 27 39 — — <0.01 <0.01 — 
Anatomical region Mean cluster size in voxels (SD) Regions active during reading M and N words compared with control conditionb Talairach coordinatesa and BAs Regions showing significant reductions in activation level compared with the appropriate baseline condition (N or M) Format-specific primingb
 
  M > N x y z BA N-N M-N N-M M-M M-M > N-M 
L occipital/temporal and fusiform 184 (39) Yes Yes — −41 −7 −1 19 — — <0.0001 <0.0001 Yes 
L superior temporal 28 (5) Yes Yes Yes −52 −35 12 22 <0.01 <0.01 <0.0001 <0.001 — 
L superior parietal 129 (39) Yes Yes Yes −30 −62 47 40/7 — — <0.01 <0.01 Yes 
L anterior inferior frontal 36 (16) Yes Yes — −36 33 45/47 <0.01 — <0.05 <0.05 — 
L posterior prefrontal 88 (22) Yes Yes — −40 10 27 44/6 — — <0.01 <0.0001 — 
R occipital/temporal and fusiform 138 (34) Yes — Yes 41 −68 −1 19 — — <0.001 <0.001 Yes 
R superior temporal 35 (11) Yes — Yes 57 −37 12 22 — — <0.05 <0.05 Yes 
R superior parietal 92 (32) Yes Yes Yes 22 −65 52 40/7 <0.01 <0.05 <0.01 <0.01 Yes 
R anterior inferior frontal 32 (18) Yes Yes — 35 27 45/47 <0.05 — <0.05 <0.01 — 
R middle frontal 40 (13) Yes — Yes 40 27 20 45/46 — — <0.01 <0.01 — 
R superior frontal 82 (39) Yes Yes — 36 27 39 — — <0.01 <0.01 — 

Note: Also listed are those regions that showed significantly greater activation during M reading compared with N reading and the P values for regions showing significant signal reductions in the 4 priming conditions. Finally, format-specific priming regions listed are those in which signal reductions were greater when the prime and target were visually identical (M-M) than when they differed (N-M).

a

Coordinates are expressed in millimeters in the Talairach and Tournoux brain atlas (1988): x, Medial–lateral axis (negative is left); y, anterior–posterior axis (negative, posterior); z, dorsal–ventral axis (negative, ventral). BAs correspond to those defined in the Talairach and Tournoux brain atlas.

b

Refer to Results for specifics of analyses and P values.

Activation Reductions Associated with Priming of M Words

ROIs were analyzed separately using a repeated-measures ANOVA comparing the mean HDR amplitude in 3 conditions (M baseline, N-M, and M-M) in order to determine whether there was evidence for priming-related reductions in signal amplitude. Participant was treated as a random factor in all analyses. Significant regions were followed up with paired t-tests comparing baseline with N-primed words and baseline with M-primed words. Alpha for follow-up paired t-tests was P < 0.05. Table 2 lists the results of these analyses identifying regions that showed significant decreases in activation in the 2 priming conditions. Among those ROIs identified as active during the mirror-reading task, there were no repetition related increases revealed. For words presented in M orientation, all brain regions that were active during the first presentation of M words showed significant decreases in activation after repetition, regardless of the orientation of the prime.

In order to assess the effect of format-specific priming, HDR “priming” scores were calculated for each region by subtracting the mean HDR amplitude at each time point during the second presentation from the corresponding amplitude during the first presentation. Priming activation scores for fusiform, superior temporal, superior parietal, and anterior inferior frontal regions were then compared using a repeated-measures ANOVA with 2 factors, priming condition (M-M, N-M) and hemisphere (Left, Right). The right middle frontal, right superior frontal, and left posterior prefrontal regions were analyzed using a paired t-test (M-M vs. N-M) because no homologous contralateral hemisphere activation was observed. Regions showing a format-specific effect should show significantly larger priming effects (reductions in activation) in the M-M condition compared with the N-M condition.

Frontal regions (right superior, right middle, bilateral anterior inferior frontal gyri, and left posterior prefrontal cortex) failed to show a format-specific priming effect. Although all these regions showed significant priming, the magnitude of the priming did not differ for primes presented in N or M orientation, and priming was similar in right and left hemispheres (all P values > 0.05). However, 3 regions (fusiform gyrus, superior parietal cortex, and superior temporal lobes) showed format-specific reductions in activity. These regions are depicted in Figure 2. The left and right fusiform gyri showed a significant effect of prime type, F1,11 = 21.29, MSe = 0.106, P < 0.001, with a larger decrease in activation for M-M words compared with N-M words. There was no difference in priming in left and right hemispheres (F < 1), and prime type did not interact with hemisphere (F < 1). Left and right parietal regions also showed a significant effect of prime type, with M-M decreases being larger than N-M decreases, F1,9 = 6.41, MSe = 0.44, P < 0.05. Again, priming did not differ by hemisphere, F1,9 = 1.38, not significant (NS), and there was no interaction between prime type and hemisphere, F1,9 = 1.32, NS. Finally, the superior temporal lobe showed a significant difference between M-M and N-M conditions, but in contrast to the bilateral effects in fusiform and parietal cortices, format-specific priming was found only in the right hemisphere. ANOVA indicated a significant interaction between prime type and hemisphere, F1,8 = 9.94, P < 0.05. Follow-up paired t-tests showed a significant difference between the 2 prime types in the right hemisphere but not in the homologous left hemisphere region. The main effects of prime type and hemisphere did not approach significance, F value < 1.

Figure 2.

Examples of regions showing mean amplitude reductions in the HDR due to repetition of words. y axis refers to the normalized signal with mean removed, averaged across all time points from 2 s postonset of the stimulus to 16 s postonset. Graphs show the mean amplitude response, expressed in percent signal change, for the first presentation of words in mirror-image (M) orientation and the mean amplitude responses for 2 priming conditions. M words were either primed with words in the same orientation (M-M) or primed with words in normal orientation (N-M). The right fusiform, left fusiform, and right superior temporal gyri show a pattern of amplitude reduction consistent with format-specific priming; reduction in the M-M priming condition is significantly greater than the reduction observed in the N-M condition. Other regions showing this pattern but not depicted here were the right and left superior parietal cortices. In contrast, left posterior prefrontal cortex shows similar reductions for both priming conditions compared with the baseline reading condition. This pattern was true for all frontal regions and for the left superior temporal gyrus.

Figure 2.

Examples of regions showing mean amplitude reductions in the HDR due to repetition of words. y axis refers to the normalized signal with mean removed, averaged across all time points from 2 s postonset of the stimulus to 16 s postonset. Graphs show the mean amplitude response, expressed in percent signal change, for the first presentation of words in mirror-image (M) orientation and the mean amplitude responses for 2 priming conditions. M words were either primed with words in the same orientation (M-M) or primed with words in normal orientation (N-M). The right fusiform, left fusiform, and right superior temporal gyri show a pattern of amplitude reduction consistent with format-specific priming; reduction in the M-M priming condition is significantly greater than the reduction observed in the N-M condition. Other regions showing this pattern but not depicted here were the right and left superior parietal cortices. In contrast, left posterior prefrontal cortex shows similar reductions for both priming conditions compared with the baseline reading condition. This pattern was true for all frontal regions and for the left superior temporal gyrus.

Ruling Out Time-On-Screen Effects in Format-Specific Priming

It is important to address one possible confound to the results described above. Because word-reading trials were self-paced, it is possible that differences in signal amplitude were simply reflecting the differences in the time each word remained on the screen and that posterior brain regions are more sensitive to visual presentation times than anterior regions. Previous research has demonstrated that visual presentation time can be an important variable in determining the level of neuroimaging signal in visual cortex. However, it is unclear if presentation time is critical for item differences of 100 ms or less when the items are presented for as long as 1000 ms (Maccotta and others 2001). Nevertheless, we explored this possibility by identifying the 4 subjects with the smallest M-M/N-M differences in RTs (average difference 36 ms). RTs for these subjects were further matched by discarding the longest items in the mirror-reading condition, so that normal and mirror RTs were equated within ±5 ms. Signal amplitude for each condition was then compared with 4 other subjects with the greatest M-M/N-M differences in RTs (average difference 92 ms). Hemodynamic estimates for each subgroup were recalculated and were averaged across the 5 posterior regions showing format-specific priming. Results are displayed in Figure 3. The results of the analysis are inconsistent with the notion that the critical M-M/N-M difference is due merely to differences in viewing time. In fact, the results show that the format-specific effect was numerically greater after response times were matched in the 2 critical conditions.

Figure 3.

The graph shows the percent signal change for format-specific priming, comparing 2 subgroups of subjects: subjects who had a large difference in RTs between M-M and N-M conditions (average 92 ms) and subjects for whom RTs were matched (within ± 5 ms) between M-M and N-M RTs. Signal differences between M-M and M-N conditions are collapsed across all 5 ROIs that exhibited format-specific priming.

Figure 3.

The graph shows the percent signal change for format-specific priming, comparing 2 subgroups of subjects: subjects who had a large difference in RTs between M-M and N-M conditions (average 92 ms) and subjects for whom RTs were matched (within ± 5 ms) between M-M and N-M RTs. Signal differences between M-M and M-N conditions are collapsed across all 5 ROIs that exhibited format-specific priming.

Activation Reductions Associated with Priming of N Words

In spite of the fact that we observed no appreciable RT priming for N words, we analyzed the HDR responses in regions involved in N reading similarly to the analyses described above, in order to determine whether or not activation reductions might provide a more sensitive measure of stimulus repetition than RTs. Results of these analyses are also summarized in Table 2. Several regions showed significant decreases in HDR amplitude corresponding to repeated items. Regions that showed significant reductions in both priming conditions (N baseline compared with N-N, and N baseline compared with M-N) included the left superior temporal gyrus and the right parietal region. In these 2 regions, the magnitude of the priming effect was similar regardless of the orientation of the prime. Two other regions showed significant priming, but only in the N-N condition; these included the left anterior inferior frontal gyrus and the right anterior inferior frontal gyrus.

Discussion

To summarize, the purpose of the present study was to demonstrate that format-specific priming is mediated by regions specifically involved in processing aspects of perceptual features, consistent with a TAP account of priming. In contrast to our predictions, we found that priming for mirror-image reading occurred in all regions associated with the baseline task, regardless of the orientation of the prime, M or N (for a similar result, see Poldrack and Gabrieli 2001). Importantly, however, the priming-related reduction in activation was greater in some brain regions when the visual form of the prime and target matched (M-M condition), compared with when they did not match (N-M condition). Although not specific to the format, those regions showing format sensitivity in the pattern of activation reduction have been implicated in perceptual processing of word form and include bilateral fusiform and right superior temporal gyri and bilateral superior parietal cortex. The results are discussed in detail below in the context of several theoretical views of priming.

Before turning to the results, the issue of explicit contamination should be addressed briefly. Explicit contamination (participants recognizing some or all of the target items as repeated) is an issue in almost all priming studies. We tried to decrease this likelihood by providing instructions to the participants that emphasized the importance of reading the words aloud, as quickly as possible. We also informed participants that some of the words will be repeated during the long list, but they should ignore this and focus on reading the words quickly. Nevertheless, it is still possible that at least some of the words in the present study were consciously recognized by subjects, at least after gaining access to the meaning of the word through reading. Although the analyses comparing targets with primes showed only decreases in activation across all brain regions, it is premature to assume that fMRI deactivations are synonymous with priming (for discussion, see Henson and Rugg 2003). Because we did not assess explicit recognition for the target words, the present study cannot rule out the possibility that processes mediating recognition are mixed, at least to some degree, with priming effects nor can these influences be separated definitively.

Reading Mirror-Image Text

Compared with N words, reading M words resulted in increased activation in several regions, primarily in the right hemisphere, and recruited additional brain regions that were not evident in normal reading, again in the right hemisphere. These included posterior regions that demonstrate robust activity and repetition effects in studies involving object recognition and priming, including bilateral lateral superior parietal lobe and fusiform gyrus (Wagner and others 1997; Buckner and others 1998; Koutstaal and others 2001). Fusiform cortex has also shown increased activation when participants made subordinate judgments regarding an object (is this a sparrow?) relative to superordinate judgments (is this a bird?), possibly reflecting the additional perceptual processing required to arrive at a more fine-grained classification (Gauthier and others 1997). Reading M words also resulted in increased activity in right hemisphere regions, including the right superior temporal gyrus, right anterior inferior frontal gyrus, and right middle frontal gyrus. The increased activation in right anterior hemisphere regions may be in response to the increased difficulty of reading M words compared with N words, resulting in additional recruitment of regions involved in attention, working memory, and task monitoring. One possible confound contributing to the findings of additional regions involved in mirror reading when compared with normal reading is the fact that mirror words remained on the screen longer than normally oriented words. Although this may contribute to our findings, the presence of additional right hemisphere regions for mirror reading is consistent with at least 2 previous studies (Poldrack and others 1998; Poldrack and Gabrieli 2001). Interestingly, these studies also demonstrated that with practice (skill learning), many of these additional right hemisphere regions dropped away. An obvious limitation of the present study is that, without varying further aspects of the reading task in systematic ways, it is not possible to determine the specific contribution of each of the regions to mirror-image reading.

Priming Effects in Normal and Mirror-Image Reading

Priming, evident both in RTs and in the extent of priming-related reduction in brain activity, was greater overall for words tested in M orientation compared with N orientation. This is consistent with Graf and Ryan (1990; see also Ostergaard 1998, 1999), who showed that tasks that are less practiced benefit most from a single prior presentation. Furthermore, a previous study of repetition priming for mirror presented words found that although the reductions with repetition were widespread across a brain network involved in mirror reading, the extent of this priming effect was reduced after considerable training in mirror reading (Poldrack and Gabrieli 2001). For our purposes, using a task like mirror-image reading without extensive practice slowed RTs and increased overall priming, thereby increasing the sensitivity to more subtle manipulations, in this case, the similarity between the visual form of the prime and target.

For M words, there was a significant reduction in RT following the presentation of primes in both M and N orientations, and primes, regardless of their orientation, resulted in a reduction in activation in all brain regions that were evident in M reading at baseline. In contrast, when words were tested in N orientation, there was no measurable effect of a prior presentation on RTs. Reading words is a highly practiced skill, and when the primes are presented with longer lag times (between 8 and 18 intervening words in the present experiment), it is unlikely to produce a decrease in RT. Most other studies using word identification present target words in some degraded form (Ostergaard 1998, 1999), or at a very fast presentation rate (Masson 1986; Graf and Ryan 1990), or they require the participant to make a decision about the stimulus being presented (Balota and Chumbley 1984), thereby increasing the complexity of the task and, hence, the priming effect. Nevertheless, despite the lack of a behavioral priming effect for N words, we found significant fMRI signal reductions after repeated trials in several regions involved in reading N words, including the left superior temporal gyrus, right superior parietal cortex, and anterior inferior frontal gyri bilaterally. The finding that reductions occurred in some, but not other, brain regions under these conditions may be important, but it may also reflect a lack of sensitivity in this simple reading task. It would be premature to interpret such a finding without replication and without a priori predictions as to why some brain regions, and not others, are affected by priming under these conditions. However, the results indicate that activation reductions may provide a more sensitive priming measure than RTs for some highly practiced tasks such as normal reading, and this warrants further investigation.

Format-Specific Priming Effects

In the mirror-image reading task, the RT data indicated a clear pattern of format-specific priming. RTs decreased an average of 14% for M words that were preceded by a prime in the same (M) orientation, compared with a reduction of 7% for M words that were preceded by a prime in the alternate (N) orientation. Format-specific effects were evident not only in RTs, but in the pattern of brain activity as well. Although all regions associated with mirror-image reading showed reduced activity after repeated trials in both priming conditions (M-M and N-M), in some brain regions, reductions were significantly greater when the orientation of the prime and target matched. There are 2 important points regarding the regions in which format-specific activation reductions were observed.

First, the magnitude of priming-related reductions in left and right frontal regions did not differ between the 2 prime types. This result is consistent with previous studies that suggest that anterior frontal regions mediate nonperceptual processing such as the identification and semantic analysis of format-invariant aspects of words. For example, left anterior inferior frontal cortex has been implicated in access to and evaluation of long-term semantic knowledge (Petersen and others 1988; Demb and others 1995). Alternatively, it may function as the neural substrate for executive control processes involved in working with semantic knowledge (Kapur and others 1994; Gabrieli and others 1998; Poldrack and others 1999; for an alternative view, see Thompson-Schill and others 1998, 1999). In contrast, left posterior prefrontal cortex is reliably activated during tasks that require passive viewing of words, reading words aloud, or making lexical decisions about words and pseudowords (reviewed in Poldrack and others 1999). Based on imaging and neuropsychological findings (Frost 1998), this region may contribute to the transformation of lexical information into phonological codes. However, although one study (Wagner and others 2000) demonstrated that only the anterior left prefrontal region benefited from prior conceptual processing, whereas the posterior region benefited from prior perceptual processing, a number of studies have found that repetition effects produce qualitatively similar effects in both regions (Raichle and others 1994; Buckner and others 1998, 2000). In addition, there is at least one study that provides evidence to suggest that left prefrontal regions are format invariant. Buckner and others (2000) found similar priming-related reductions in activity in the left inferior frontal gyrus during visual-to-visual and auditory-to-auditory priming conditions using a word stem completion task, suggesting that the region is not modality specific. Activity in these regions should therefore be primed by the prior presentation of a word, regardless of the perceptual form of the word.

Second, posterior regions (bilateral fusiform, bilateral superior parietal, and right superior temporal cortices) showed format-specific HDR reductions in response to priming. The signal reduction in response to primes was greatest when the prime was presented in the same visual format as the target. Koutstaal and others (2001) obtained similar results in a recent study of priming using pictures in a size judgment task. They found that both anterior and posterior brain regions showed decreases in fMRI activation for repeated versus novel pictures of common objects. Additionally, when the object was primed with the exact same picture, several posterior cortical regions showed greater activation reductions compared with a condition where the object was primed with a similar but different picture (such as 2 different umbrellas or 2 different coffee mugs). These regions included the right precuneus and bilateral fusiform, parahippocampal, occipital, and superior parietal cortices. Regions sensitive to the format-specific priming in both these studies have been shown to participate in various aspects of visual form analysis of words and objects.

Theoretical Accounts of Format-Specific Priming

There is general agreement that repetition priming results in regional fMRI signal reduction. A small number of studies have now added an important qualification to this general finding by demonstrating that the magnitude of the signal reduction is at least partially dependent upon the degree of similarity between the cognitive processes engaged at study and at test (for review, see Schacter and others 2004). For example, in the present study and in Koutstaal and others (2001), when the overlap of perceptual processes from study to test was increased by making the target and prime identical, priming increased behaviorally and was accompanied by greater reductions in activity in posterior cortical regions. These results are at least partially consistent with a PRS system view of priming described by Schacter (1994). However, the fact that anterior regions of the brain also show priming-related signal reductions in a simple visual task such as word identification is not predicted by a strict PRS view. Priming-related signal reductions occur throughout the brain, and it is insufficient to posit that priming on any task is mediated solely by increased efficiency in the perceptual analysis of the stimuli. However, to the extent that priming is enhanced by the overlap of specific perceptual features, this aspect of priming will be mediated by PRS cortical regions involved in perceptual analysis of the form and structure of stimuli. In contrast to the PRS system, TAP provides a more general framework that can account for a broader range of region-specific priming effects, whether they occur in posterior regions that mediate perceptual processing of visual form or in frontal regions mediating conceptual and semantic processes involved in categorization (as in Wagner and others 2000). Depending upon the specific operations required for each task and the overlap across 2 tasks, the specific regions showing format-specific priming may differ significantly from our current results, but the general framework of TAP will apply.

It is important to note, however, that the pattern of signal reductions observed here cannot be explained fully by a purely TAP account of priming. According to a strong TAP view, priming is presumed to occur because of the overlap in processes engaged at study and test, and therefore only those processes that are utilized during the study episode are capable of mediating priming. By this view, we expected that N oriented primes would provide little, if any, facilitation for the perceptual analysis of mirror-image words because there is no requirement in normal reading to engage in letter rotation and the letter-by-letter reading strategy utilized when reading words in this unusual orientation. However, when M words were primed with N words, all regions active during mirror-image reading showed robust signal reductions, even in those regions that were not activated during normal reading including right middle frontal gyrus, right superior temporal gyrus, and right fusiform gyrus. Dale and colleagues (Dale and others 2000) demonstrated that when words are repeated in a size judgment task, priming effects are widespread across the entire cortical network involved in word processing. In addition, they reported that electrocortical repetition effects did not begin until well after the initial perceptual analysis of a stimulus was complete (200–260 ms poststimulus onset). How does one account for such global priming effects? The results of Dale and others (2000), combined with our own, suggest that there are 2 distinct and perhaps interactive bases for priming. Priming may be mediated either by “top down” or “bottom-up” processing of words, depending upon the specific circumstances of the test. We suggest that a recent presentation of a word in any form that fully engages the semantic representation of that word will prime all aspects of a repeated presentation, semantic and perceptual. Increasing the efficiency of semantic processing will serve to disambiguate the perceptual processing of the unfamiliar item as analysis progresses, and this effect will be particularly evident when the task is unfamiliar or difficult. Recent exposure to the identical perceptual processes required for the repeated item will provide an added benefit, but only to specific processes involved in perceptual analysis. Priming, then, may be driven by both semantic and perceptual processes. Importantly, perceptual processes can benefit from a recent exposure to semantic information, without exposure to the specific perceptual processes involved in analyzing the visual form.

One prediction that derives from the above discussion is that the global priming effects we observe might only occur under circumstances where the participant successfully accesses the meaning of the word, regardless of how much time they spend analyzing the visual form. On trials where participants are unsuccessful in identifying the word, no semantic level priming should occur. We were unable to assess this possibility because we specifically designed the study to minimize the number of words that were unsuccessfully read on the first presentation. However, the issue warrants further investigation.

An alternative explanation, and also consistent with the present pattern of results, is that there is a difference between the processes that underlie behavioral priming such as enhanced RTs and accuracy and those that alter the HDR; some neuroimaging signal changes may be directly related to behavioral priming, and some may reflect postprocessing modulations (Dobbins and others 2004). Moreover, effects at this level may have been evident in our normal reading results where, despite the lack of behavioral priming, several brain regions exhibited signal reductions. Tulving and others (Tulving and others 1996) have suggested that reductions in neural activity associated with repetition may be the result of postidentification attentional modulation associated with the detection of nonnovel stimuli. By this account, once perceptual processing is completed, the stimulus is assessed for novelty and then attentional resources are allocated for further analysis depending on the novelty of the item (i.e., more resources are allocated for novel items and less for nonnovel items). The determination that an item is novel must be context dependent; although frequently encountered words are not particularly novel on their own, in the context of a specific episode (the priming experiment), words that are repeated will be deemed less novel than nonrepeated words. The degree of similarity between semantic and perceptual processes across items influences the degree of adjustment to signal levels throughout the currently activated network. Hence, one might expect greater reductions in allocation of resources when the visual form of the word is maintained across repeated presentations. However, it is difficult to explain why such format-specific priming effects should only occur within certain brain regions and not others. The notion that novelty assessment occurs after perceptual analysis is complete is consistent with the findings of late-onset brain changes associated with word identification priming (Dale and others 2000) and may also provide a mechanism that accounts for the nonspecific or global priming effect observed in this and similar studies. At present, however, Tulving's hypothesis is not sufficiently elaborated to account for region-specific priming effects unless one postulates an interaction between global and process-specific priming effects.

Finally, the finding of format-specific signal reductions in right, but not left, superior temporal lobe is consistent with the suggestion that the right hemisphere is engaged in the specific form analysis of a word or object. A further refinement of the PRS account of format-specific priming is provided by Marsolek (Marsolek and others 1992, 1994, 1996). Marsolek suggests that the right and left hemispheres preferentially analyze specific and abstract properties of the visual form, respectively. The abstract visual-form subsystem, associated with posterior left hemisphere regions, supports analysis of abstract categories of forms by processing visual features that are relatively invariant across different instances. In contrast, the specific visual-form (SVF) subsystem, associated with posterior right hemisphere regions, processes distinctive aspects of visual form that would distinguish a specific instance. In word stem completion experiments, for example (Marsolek and others 1992, 1994), greater priming was obtained when prime and target word stems appeared in the same letter case than in different letter cases. More importantly, this effect was greater when stems were presented directly to the right hemisphere via the left visual field than when stems were presented directly to the left hemisphere via the right visual field (see also Vaidya and others 1998).

The specific regions of right posterior cortex mediating these effects may depend on the type of material being tested. In their picture-priming experiment, Koutstaal and others (2001) found one region, the right fusiform gyrus, that showed significantly greater format-specific reduction in activation compared with the homologous left hemisphere region. Although format-specific reductions were also found in other posterior regions, these effects were bilateral. Using words as the critical stimuli, we found a format-specific activation reduction in the right, but not left, superior temporal gyrus, consistent with a recent study using a masked priming paradigm (Dehaene and others 2004). In contrast, both left and right fusiform gyri showed similar degrees of format specificity. Previous research has suggested that visual word forms are processed in regions of fusiform gyrus (Rumsey and others 1997), whereas superior temporal gyrus may be more involved in processing of phonological representations (Majerus and others 2005). Our finding of changes in the right superior temporal lobe suggest that participants utilized phonology as a strategy for identifying mirror orientation words, essentially “sounding out” the words as they read (see also Ryan and others 2001). The results of the 2 studies suggest that the processing of SVFs of stimuli, such as words and pictures, may be dependent on the processing approach taken to identify them, and these approaches are most likely mediated by different brain regions. These findings also warrant further investigation.

In summary, we found that the degree of priming-related signal reduction in brain regions depends at least partially on the degree of overlap of cognitive processes engaged at study and again at test. However, the complete pattern of signal reductions obtained in the present study cannot fully be accounted for by existing views of priming. The results raise interesting and as yet unresolved questions regarding the mechanisms underlying the priming effect. Functional imaging methods clearly provide an important new tool for understanding this phenomenon.

Conflict of Interest: None declared.

References

Balota
DA
Chumbley
JI
Are lexical decisions a good measure of lexical access? The role of word frequency in the neglected decision stage
J Exp Psychol Hum Percept Perform
 , 
1984
, vol. 
10
 (pg. 
340
-
357
)
Blaxton
TA
Investigating dissociations among memory measures: support for a transfer-appropriate processing framework
J Exp Psychol Learn Mem Cogn
 , 
1989
, vol. 
15
 (pg. 
657
-
668
)
Blaxton
TA
Bookheimer
SY
Zeffiro
TA
Figlozzi
CM
Gaillard
WD
Theodore
WH
Functional mapping of human memory using PET: comparisons of conceptual and perceptual tasks
Can J Exp Psychol
 , 
1996
, vol. 
50
 (pg. 
42
-
56
)
Buckner
RL
Goodman
J
Burock
M
Rotte
M
Koutstaal
W
Schacter
DL
Rosen
B
Dale
AM
Functional-anatomical correlates of object priming in humans revealed by rapid presentation event-related fMRI
Neuron
 , 
1998
, vol. 
20
 (pg. 
285
-
196
)
Buckner
RL
Koutstaal
W
Schacter
DL
Rosen
BR
fMRI evidence for a role of frontal and inferior temporal cortex in conceptual priming
Brain
 , 
2000
, vol. 
123
 (pg. 
620
-
640
)
Buckner
RL
Petersen
SE
Ojemann
JG
Miezin
FM
Squire
LR
Raichle
ME
Functional anatomical studies of explicit and implicit memory retrieval tasks
J Neurosci
 , 
1995
, vol. 
15
 (pg. 
12
-
29
)
Burock
MA
Buckner
RL
Woldorff
MG
Rosen
BR
Dale
AM
Randomized event-related experimental design allows for extremely rapid presentation rates using functional MRI
Neuroreport
 , 
1998
, vol. 
9
 (pg. 
3735
-
3739
)
Clarke
R
Morton
J
Cross modality facilitation in tachistoscopic word recognition
Q J Exp Psychol
 , 
1983
, vol. 
104
 (pg. 
268
-
294
)
Cox
RW
AFNI: software for analysis and visualization of functional magnetic resonance neuroimages
Comput Biomed Res
 , 
1996
, vol. 
29
 (pg. 
162
-
173
)
Curran
T
Schacter
DL
Bessenoff
G
Visual specificity effects on word stem completion: beyond transfer appropriate processing?
Can J Exp Psychol
 , 
1996
, vol. 
50
 (pg. 
22
-
33
)
Dale
AM
Optimal experimental design for event-related fMRI
Hum Brain Mapp
 , 
1999
, vol. 
8
 (pg. 
109
-
114
)
Dale
AM
Buckner
RL
Selective averaging of rapidly presented individual trials using fMRI
Hum Brain Mapp
 , 
1997
, vol. 
5
 (pg. 
329
-
340
)
Dale
AM
Liu
AK
Fischl
BR
Buckner
RL
Belliveau
JW
Lewine
JD
Halgren
E
Dynamic statistical parametric mapping: combining fMRI and MEG for high-resolution imaging of cortical activity
Neuron
 , 
2000
, vol. 
26
 (pg. 
55
-
67
)
Dehaene
S
Jobert
A
Naccache
L
Ciuciu
P
Poline
JB
Le Bihan
D
Cohen
L
Letter binding and invariant recognition of masked words: behavioral and neuroimaging evidence
Psychol Sci
 , 
2004
, vol. 
15
 (pg. 
307
-
313
)
Demb
JB
Desmond
JE
Wagner
AD
Vaidya
CJ
Glover
GH
Gabrieli
JDE
Semantic encoding and retrieval in the left inferior prefrontal cortex: a functional MRI study of task difficulty and process specificity
J Neurosci
 , 
1995
, vol. 
15
 (pg. 
5870
-
5878
)
Dobbins
IG
Schnyer
DM
Verfaellie
M
Schacter
DL
Cortical activity reductions during repetition priming can result from rapid response learning
Nature
 , 
2004
, vol. 
428
 (pg. 
316
-
319
)
Frost
R
Toward a strong phonological theory of visual word recognition: true issues and false trails
Psychol Bull
 , 
1998
, vol. 
123
 (pg. 
71
-
99
)
Gabrieli
JDE
Poldrack
RA
Desmond
JE
The role of left prefrontal cortex in language and memory
Proc Natl Acad Sci USA
 , 
1998
, vol. 
95
 (pg. 
906
-
913
)
Gauthier
I
Anderson
AW
Tarr
MJ
Skudlarski
P
Gore
JC
Levels of categorization in visual recognition studies using functional magnetic resonance imaging
Curr Biol
 , 
1997
, vol. 
7
 (pg. 
645
-
651
)
Gibson
JM
Brooks
JO
Friedman
L
Yesavage
JA
Typography manipulations can affect priming of word stem completion in older and younger adults
Psychol Aging
 , 
1993
, vol. 
8
 (pg. 
481
-
489
)
Glover
GH
Lee
AT
Motion artifacts in fMRI: comparison of 2DFT with PR and spiral scan methods
Magn Reson Med
 , 
1995
, vol. 
33
 (pg. 
624
-
635
)
Graf
P
Ryan
L
Transfer-appropriate processing for implicit and explicit memory
J Exp Psychol Learn Mem Cogn
 , 
1990
, vol. 
16
 (pg. 
978
-
992
)
Graf
P
Shimamura
AP
Squire
LR
Priming across modalities and priming across category levels: extending the domain of preserved function in amnesia
J Exp Psychol Learn Mem Cogn
 , 
1985
, vol. 
11
 (pg. 
386
-
396
)
Halgren
E
Buckner
RL
Marinkovic
K
Rosen
BR
Dale
AM
Cortical localization of word repetition effects
Cogn Neurosci Soc Annu Meet
 , 
1997
, vol. 
4
 pg. 
34
 
Henson
RN
Rugg
MD
Neural suppression, hemodynamic repetition effects and behavioural priming
Neuropsychologia
 , 
2003
, vol. 
41
 (pg. 
263
-
270
)
Kapur
S
Rose
R
Liddle
PF
Zipursky
RB
Brown
GM
Stuss
D
Houle
S
Tulving
E
The role of the left prefrontal cortex in verbal processing: semantic processing or willed actions
Neuroreport
 , 
1994
, vol. 
5
 (pg. 
2193
-
2196
)
Kolers
PA
Memorial consequences of automatized encoding
J Exp Psychol Hum Learn Mem
 , 
1975
, vol. 
1
 (pg. 
689
-
701
)
Kolers
PA
Cermak
LS
Craik
FIM
A pattern-analyzing basis of recognition
Levels of processing in human memory
 , 
1979
Hillsdale, NJ
Erlbaum
(pg. 
363
-
384
)
Kolers
PA
Ostry
DJ
Time course of loss of information regarding pattern analyzing operations
J Verb Learn Verb Behav
 , 
1974
, vol. 
13
 (pg. 
599
-
612
)
Koutstaal
W
Wagner
AD
Rotte
M
Maril
A
Buckner
RL
Schacter
DL
Perceptual specificity in visual object priming: functional magnetic resonance imaging evidence for a laterality difference in fusiform cortex
Neuropsychologia
 , 
2001
, vol. 
39
 (pg. 
184
-
199
)
Kucera
M
Francis
W
Computational analysis of present-day American English
 , 
1967
RI: Brown University Press
Providence
Maccotta
L
Zachs
JM
Buckner
RL
Rapid self-paced event-related functional MRI: feasibility and implications of stimulus- versus response-locked timing
Neuroimage
 , 
2001
, vol. 
14
 (pg. 
1105
-
1121
)
Majerus
S
Van der Linden
M
Collette
F
Laureys
S
Poncelet
M
Degueldre
C
Delfiore
G
Luxen
A
Salmon
E
Modulation of brain activity during phonological familiarization
Brain Lang
 , 
2005
, vol. 
92
 (pg. 
320
-
331
)
Marsolek
CJ
Kosslyn
SM
Squire
LR
Form-specific visual priming in the right cerebral hemisphere
J Exp Psychol Learn Mem Cogn
 , 
1992
, vol. 
18
 (pg. 
492
-
508
)
Marsolek
CJ
Schacter
DL
Nicholas
CD
Form-specific visual priming for new associations in the right cerebral hemisphere
Mem Cogn
 , 
1996
, vol. 
24
 (pg. 
539
-
556
)
Marsolek
CJ
Squire
LR
Kosslyn
SM
Lulenski
ME
Form-specific explicit and implicit memory in the right cerebral hemisphere
Neuropsychology
 , 
1994
, vol. 
8
 (pg. 
588
-
597
)
Martin
A
LaLonde
FM
Wiggs
CL
Weisberg
J
Ungerleider
LG
Haxby
JV
Repeated presentation of objects reduces activity in ventral occipitotemporal cortex: a fMRI study of repetition priming
Soc Neurosci Abstr
 , 
1995
, vol. 
21
 pg. 
1497
 
Masson
MEJ
Identification of typographically transformed words: instance-based skill acquisition
J Exp Psychol Learn Mem Cogn
 , 
1986
, vol. 
12
 (pg. 
479
-
488
)
Morris
CD
Bransford
JE
Franks
JJ
Levels of processing versus transfer appropriate processing
J Verb Learn Verb Behav
 , 
1977
, vol. 
16
 (pg. 
519
-
533
)
Ostergaard
A
The effects on priming of word frequency, number of repetitions, and delay depend on the magnitude of priming
Mem Cogn
 , 
1998
, vol. 
26
 (pg. 
40
-
60
)
Ostergaard
A
Priming deficits in amnesia: now you see them, now you don't
J Int Neuropsychol Soc
 , 
1999
, vol. 
5
 (pg. 
175
-
190
)
Petersen
SE
Fox
PT
Posner
MI
Mintun
M
Raichle
ME
Positron emission tomographic studies of the cortical anatomy of single-word processing
Nature
 , 
1988
, vol. 
331
 (pg. 
585
-
589
)
Poldrack
RA
Desmond
JE
Glover
GH
Gabrieli
JDE
The neural basis of visual skill learning: an fMRI study of mirror reading
Cereb Cortex
 , 
1998
, vol. 
8
 (pg. 
1
-
10
)
Poldrack
RA
Gabrieli
JDE
Characterizing the neural mechanisms of skill learning and repetition priming: evidence from mirror reading
Brain
 , 
2001
, vol. 
125
 
67
pg. 
82
 
Poldrack
RA
Wagner
AD
Prull
MW
Desmond
JE
Gover
GH
Gabrieli
JDE
Distinguishing semantic and phonological processing in the left inferior prefrontal cortex
Neuroimage
 , 
1999
, vol. 
10
 (pg. 
15
-
35
)
Raichle
ME
Fiez
JA
Videen
TO
MacLeod
AM
Pardo
JV
Fox
PT
Petersen
SE
Practice-related changes in human brain functional anatomy during nonmotor learning
Cereb Cortex
 , 
1994
, vol. 
4
 (pg. 
8
-
26
)
Rajaram
S
Roediger
HL
Direct comparison of four implicit memory tests
J Exp Psychol Learn Mem Cogn
 , 
1993
, vol. 
19
 (pg. 
765
-
776
)
Roediger
HL
Blaxton
TA
Effects of varying modality, surface features, and retention interval on priming in word-fragment completion
Mem Cogn
 , 
1987
, vol. 
15
 (pg. 
379
-
388
)
Rumsey
J
Horwitz
B
Donohue
B
Nace
K
Maisog
J
Andreason
P
Phonological and orthographic components of word recognition
Brain
 , 
1997
, vol. 
120
 (pg. 
739
-
759
)
Ryan
L
Ostergaard
A
Norton
L
Johnson
J
Explicit and implicit word stem completion: declines in performance across the lifespan and the role of search processes and familiarity
Mem Cogn
 , 
2001
, vol. 
29
 (pg. 
678
-
690
)
Scarborough
DL
Cortese
C
Scarborough
HS
Frequency and repetition effects in lexical memory
J Exp Psychol Hum Percept Perform
 , 
1977
, vol. 
3
 (pg. 
1
-
17
)
Schacter
DL
Schacter
DL
Tulving
E
Priming and multiple memory systems: perceptual mechanisms of implicit memory
Memory systems 1994
 , 
1994
Cambridge, MA
MIT Press
(pg. 
233
-
268
)
Schacter
DL
Buckner
RL
Priming and the brain
Neuron
 , 
1998
, vol. 
20
 (pg. 
185
-
195
)
Schacter
DL
Dobbins
IG
Schnyer
DM
Specificity of priming: a cognitive neuroscience perspective
Nat Neurosci Rev
 , 
2004
, vol. 
5
 
11
(pg. 
853
-
862
)
Schacter
DL
Graf
P
Modality specificity of implicit memory for new associations
J Exp Psychol Learn Mem Cogn
 , 
1989
, vol. 
15
 (pg. 
3
-
12
)
Shallice
T
From neuropsychology to mental structure
 , 
1988
MA: Cambridge University Press
Cambridge
Talairach
J
Tournoux
P
Co-planar stereotaxic atlas of the human brain
1988
New York
Thieme
Tardiff
T
Craik
FIM
Reading a week later: perceptual and conceptual factors
J Mem Lang
 , 
1989
, vol. 
28
 (pg. 
107
-
125
)
Thompson-Schill
SI
D'Esposito
M
Kan
IP
Effects of repetition and competition on activity in left prefrontal cortex during word generation
Neuron
 , 
1999
, vol. 
23
 (pg. 
513
-
522
)
Thompson-Schill
SI
Swick
D
Farah
MJ
D'Esposito
M
Kan
IP
Knight
RT
Verb generation in patients with focal frontal lesions: a neuropsychological test of neuroimaging findings
Proc Natl Acad Sci USA
 , 
1998
, vol. 
95
 (pg. 
15855
-
15860
)
Tulving
E
Markowitsch
HJ
Craik
FIM
Habib
R
Houle
S
Novelty and familiarity activations in PET studies of memory encoding and retrieval
Cereb Cortex
 , 
1996
, vol. 
6
 (pg. 
71
-
79
)
Tulving
E
Schacter
DL
Priming and human memory systems
Science
 , 
1990
, vol. 
247
 (pg. 
301
-
306
)
Vaidya
CJ
Gabrieli
JDE
Verfaellie
M
Fleischman
D
Askari
N
Font-specific priming following global amnesia and occipital lobe damage
Neuropsychology
 , 
1998
, vol. 
12
 (pg. 
183
-
192
)
Wagner
AD
Desmond
JE
Demb
JB
Glover
GH
Gabrieli
JDE
Semantic repetition priming for verbal and pictorial knowledge: a functional MRI study of left inferior prefrontal cortex
J Cogn Neurosci
 , 
1997
, vol. 
9
 (pg. 
714
-
726
)
Wagner
AD
Koutstaal
W
Maril
A
Schacter
DL
Buckner
RL
Task-specific repetition priming in left inferior prefrontal cortex
Cereb Cortex
 , 
2000
, vol. 
10
 (pg. 
1176
-
1184
)
Weldon
MS
Roediger
HL
Altering retrieval demands reverses the picture superiority effect
Mem Cogn
 , 
1987
, vol. 
15
 (pg. 
269
-
280
)
Wiggs
CL
Martin
A
Properties and mechanisms of perceptual priming
Curr Opin Neurobiol
 , 
1998
, vol. 
8
 (pg. 
227
-
233
)