Neuroimaging evidence for dissociable forms of repetition priming

Science

Volumn 287, Issue 5456, 2000, Pages 1269-1272

  Henson, R ^a,b   Shallice, T ^b,c   Dolan, R ^a,d  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c SISSA   (Italy)

^d ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BRAIN CORTEX; FACE; HUMAN; HUMAN EXPERIMENT; MEMORY; NEUROPSYCHOLOGY; NORMAL HUMAN; PRIORITY JOURNAL; SYMBOLISM; VISUAL STIMULATION;

EID: 0034681485     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.287.5456.1269     Document Type: Article

References (38)

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9. A 2T VISION system (Siemens, Erlangen, Germany) provided T1 anatomical volume images (1 mm by 1 mm by 1.5 mm voxels) and T2*-weighted echoplanar images (EPIs) (64 by 64 3 mm by 3 mm pixels, TE = 40 ms) with blood oxygenation level-dependent contrast. EPIs comprised 2-mm-thick axial slices that were acquired sequentially every 3 mm and continuously during a single 20-min session. A total of 305 volumes of 46 slices covering the whole brain were acquired in experiments 1 and 2, with a repetition time (TR) of 4.2 s/volume; 667 volumes of 16 slices, angled along the temporal lobe, were acquired in experiments 3 and 4, with a TR of 1.4 s/volume. The first five volumes were discarded to allow for T1 equilibration. Volumes were realigned, resliced using sinc interpolation, and normalized to an EPI template based on the Montreal Neurological Institute reference brain [C. A. Cocosco et al., Neuroimage 5, 425 (1997)] of 3 mm by 3 mm by 3 mm voxels in Talairach space using nonlinear basis functions. T1 structural volumes were coregistered with the mean realigned EPI volumes and normalized with the same deformation parameters. The EPI volumes were smoothed with an 8-mm full width at half maximum (FWHM) isotropic Gaussian kernel and globally scaled to 100. The time series for each voxel were high-pass filtered to 1/240 Hz (experiments 1 and 2) or 1/120 Hz (experiments 3 and 4) and low-pass smoothed by a 4-s FWHM Gaussian kernel.
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11. Data were analyzed with the Statistical Parametric Mapping software [SPM99, Wellcome Department of Cognitive Neurology, London; K. J. Friston, et al., Hum. Brain Mapp. 2, 189 (1995)]. The responses to stimulus onsets for each event type, synchronized with the acquisition of the middle slice, were modeled by a canonical hemodynamic response function (HRF) and its temporal derivative. Five event types were modeled in experiments 1 and 2, and eleven were modeled in experiments 3 and 4 (one for each presentation of familiar and unfamiliar stimuli, plus one for target stimuli). These functions, together with a constant term, were used as participant-specific covariates in a fixed effects, general linear model. Linear contrasts on parameter estimates for the canonical HRF generated statistical parametric maps of the t statistic, which were subsequently transformed to Z values. For experiments 1 and 2, the statistical parametric maps were thresholded at P < 0.001, uncorrected, and masked with the main effect of stimuli versus baseline, thresholded at P < 0.01, uncorrected. Given the prior hypotheses generated from experiments 1 and 2, the statistical parametric maps in experiments 3 and 4 were similarly masked but thresholded at P < 0.005.
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14. V. Bruce and A. W. Young, Br. J. Psychol. 77, 305 (1986). Other regions showed a familiarity effect for faces but did not survive the masking by faces versus baseline, including a left anterior temporal region [x = -63, y = -6, 2 = -24; Brodmann Area (BA) 21; Z score = 3.33] close to that associated with famous versus nonfamous faces in work by M. L. Gorno-Ternpini et al. [Brain 121, 2103 (1998)]. Lesion evidence [A. W. Ellis et al., Brain 112, 1469 (1989)] suggests that anterior temporal regions represent semantic personal knowledge rather than the perceptual information we associate here with fusiform regions and FRUs.
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18. This model included an additional covariate representing the modulation of second presentations of familiar and unfamiliar stimuli by the function exp(-lag/150), where 150 was the maximum possible lag. Contrasts on this lag effect were masked as before and thresholded at P < 0.005 uncorrected. Immediate repetitions (lag = 1), which may represent a special case [S. Bentin and M. Moscovitch, J. Exp. Psychol. Gen. 117, 148 (1988)], were rare, and their removal from analyses had a negligible effect.
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23. The same right fusiform region was revealed when the linear interaction contrast across all five presentations was orthogonalized with respect to the pairwise interaction across the first two presentations, for both faces and symbols. Further tests of quadratic trends did not reveal any right fusiform regions, contrary to an expectation that repetition enhancement for unfamiliar stimuli might asymptote, or switch to repetition suppression, after five presentations (as expected if a number of presentations were sufficient to make unfamiliar stimuli functionally equivalent to familiar stimuli).
24. Parametric effects of presentation number (1 through 5), exponentiated lag (72), and the interaction between presentation and lag were modeled separately for familiar and unfamiliar stimuli. Differential lag effects for familiar and unfamiliar stimuli were found in right fusiform regions for faces (x = 48, y = -57, z = -18; BA 37; Z score = 2.79) and symbols (x = 45, y = -42, z = -21; BA 37; Z score = 3.78). A right fusiform region also showed an interaction between familiarity, presentation number, and lag for symbols (x = 36, y = -60, z = -31; BA 37; Z score = 3.32). 19. Images of parameter estimates for the familiarity and familiarity-by-repetition contrasts for each participant were entered into a second-level, one-tailed t test. Some more posterior occipitotemporal regions also showed effects of familiarity, repetition, or lag (compare Figs. 2 through 4), but these regions were less consistent across the four separate analyses, and we concentrate on the middle fusiform cortex because of its prior association with visual object (particularly face) recognition (8, 70).
25. The spatial variability of these regions was further quantified by testing each participant separately (thresholded at P < 0.01, uncorrected). Taking the maxima from each participant that was closest to the group maxima, we found that the mean and standard deviation of Talairach coordinates (x, y, z) were (-36.5 ± 13.3, -51.5 ± 13.1, -15.0 ± 4.7), (-41.5 ± 3.5, -50.5 ± 4.8, -7.5 ± 10.7), (-38.5 ± 16.7, -49.5 ± 7.8, -17.0 ± 9.8), and (-49.5 ±8.8, -44.5 ± 15.5, -12.0 ± 10.6) for the familiarity effect and (42 ± 6.8, -55.5 ± 7.3, -20.5 ± 7.7), (40.5 ± 7.7, -55.5 ± 9.4, -26 ± 9.3), (34.5 ± 11.5, -48 ± 12.4, -24.5 ± 6.9), and (36.5 ± 12.5, -44.5 ± 21.7, -19.0 ± 7.9) for the familiarity-by-repetition interaction, across experiments 1 through 4, respectively. Although a trend is evident for a more medial location of the familiarity effect for faces relative to symbols, no reliable differences were detected in the x, y, or z coordinates for either the familiarity effect or the familiarity-by-repetition interaction in comparison of experiments 1 and 3 versus experiments 2 and 4 [t (12) < 1.69, P > 0.05].
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30. Our experimental design cannot distinguish the relative influence of explicit versus implicit memory [D. L. Schacter, J. Exp. Psychol. 13, 501 (1987)], and the repetition-related increases may reflect explicit recognition processes [P. J. Reber, C. E. Stark, L. R. Squire, Learn Mem. 5, 420 (1998)].
31. Our experimental design cannot distinguish the relative influence of explicit versus implicit memory [D. L. Schacter, J. Exp. Psychol. 13, 501 (1987)], and the repetition-related increases may reflect explicit recognition processes [P. J. Reber, C. E. Stark, L. R. Squire, Learn Mem. 5, 420 (1998)].
32. Prior presentation of intact images of unfamiliar faces may [R. J. Dolan et al., Nature 389, 596 (1997)] or may not (24) be sufficient for subsequent recognition of degraded versions. In situations where recognition is not achieved, repetition suppression would be expected (24).
33. One exception is when task-relevant repetitions must be distinguished from task-irrelevant repetitions [E. Miller and R. Desimone, Science 263, 520 (1994)]. Thus, the pattern of increased versus decreased responses is also likely to depend on the specific task performed.
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36. Probabilistic presentation maintains sensitivity to the main effect of stimuli versus baseline at short SOAs [A. M. Dale and R. L. Buckner, Hum. Brain Mapp. 5, 329 (1997); O. Josephs and R. N. A. Henson, Philos. Trans. R. Soc. London Ser. B 354, 1215 (1999)].
37. Probabilistic presentation maintains sensitivity to the main effect of stimuli versus baseline at short SOAs [A. M. Dale and R. L. Buckner, Hum. Brain Mapp. 5, 329 (1997); O. Josephs and R. N. A. Henson, Philos. Trans. R. Soc. London Ser. B 354, 1215 (1999)].
38. This work was supported by Wellcome Trust grant 051028/Z. R.D. is supported by the Wellcome Trust. We thank J. Andersson, C. Buechel, K. Friston, M. Gorno-Ternpini, O. Josephs, and an anonymous referee for their assistance.