INTACT PRIMING OF PATTERNS DESPITE IMPAIRED MEMORY* JOHN D. E. GABRIELI,~~ WILLIAM MILBERG,~ MARGARET M. KEANEt and SUZANNE CORKING tDepartment of Brain and Cognitive Sciences and Clinical Research Center, Massachusetts Institute of Technology, Cambridge. MA 02139.U.S.A.; ZDepartment of Psychology. Northwestern University. Evanston. IL, U.S.A.: and $GRECC. West Roxbury VA Center. West Roxbury, MA 02132, U.S.A. (Received 24 Auyust 1989; uccepred 15 November 1989) Abstract-The priming of patterns was examined in normal control subjects (NCS) and in the amnesic patient H.M., whose anterograde amnesia followed bilateral medial temporal-lobe excision 33 years earlier. Despite H.M.‘s impaired recognition of the patterns. he demonstrated a pattern priming effect equivalent in magnitude to that of the NCS. The results demonstrated that intact priming with novel. nonverbal material can occur despite severe amnesia. Pattern priming may reflect adaptive visual processes involved in learning novel perceptual organizations of known visual codes. such as letters, words. shapes, and objects. INTRODUCTION PRIMING refers to the influence of prior processing of stimuli upon later performance with those stimuli. For example, exposure to a word in a study list increases the likelihood that normal and amnesic subjects will complete a 3-letter stem to that word [lo, 11, 20, 451, will produce that word when listing members of a category [15, 18, 223, and will identify that word when it is presented very briefly [2,4, 131 or when it emerges from visual noise [ 11,453. Remarkably, the magnitude of these priming effects is normal (intact) in amnesic patients despite their impaired recall or recognition of the study list words. The presence of intact priming in amnesia indicates that priming can be mediated by memory systems that are separable from those that subserve recall and recognition: a memory system is defined as the minimal neural network required to record, retain, and retrieve a form of knowledge. Priming can be demonstrated on a broad range of tasks and is probably not a unitary phenomenon. Nevertheless, most demonstrations of intact priming in global amnesia have used verbal tasks, such as reading, spelling, or completing letters into words. There are, however, a few examples of priming in amnesia that do not involve words as stimuli. After amnesic patients identified incomplete line drawings of animals and common objects, they demonstrated considerable improvement when reidentifying the incomplete drawings an hour or more later [26,44]. A similar finding was reported in eight amnesic patients (seven of *Presented in part at the Society for Neuroscience meeting in Washington, D.C., November 1986, and in the first author’s doctoral thesis submitted to the Massachusetts Institute of Technology. Korrespondence to be addressed to John D. E. Gabrieli, 102 Swift Hall, Department of Psychology, Northwestern University, Evanston, IL 60208. U.S.A. 417 418 J. D. E. GABRIELI et al whom had closed-head injuries) who reduced greatly their times to detect hidden figures in picture puzzles that they had studied a day earlier [9]. Three amnesic patients also improved their ability to find incongruous features in complex cartoon-type drawings taken from the McGill anomalies task [46]; the improvements were maintained for as long as 4 days. These demonstrations of nonverbal priming in amnesia are intriguing, but their meaning remains elusive for several reasons. First, in no case was the priming demonstrated as being intact in the amnesic patients (i.e. as being equal to that of control subjects). Priming in the amnesic patients was either less than that seen in the control subjects [26, 441 or not compared to that of control subjects [9, 461. Second, no tests of explicit recall and recognition of the nonverbal stimuli were given in those studies, precluding a rigorous dissociation between nonverbal priming and recall/recognition memory. It is possible that given a multiple-choice or yes/no recognition test, the amnesic subjects in the earlier studies would have shown a recognition impairment comparable to their priming impairment. MILNER et al. [26] hypothesized that the small deficit in priming shown by amnesic patients was due to their being restricted to using perceptual memory while normal subjects could consult perceptual memory and explicit verbal memory of the prior testing session. Although Milner’s hypothesis is plausible, it remains unknown whether nonverbal priming can be fully intact in amnesia and can be dissociated rigorously from recall and recognition memory. The status of nonverbal priming in amnesia is important for theories about the nature of preserved priming capacities. In attempting to elucidate the processes that support verbal priming, investigators have explored the boundary conditions for intact priming effects in amnesia [33, 34, 391. Evidence exists that intact priming can occur across modalities and without physical similarities between the primed word and the stimulus that evokes access of the primed word [19,41]. Amnesic patients, however, have failed to show normal priming for nonwords on some tasks [4, 10, but see 2,11, 131. One explanation for this finding is that the nonwords cannot be known premorbidly by the patients, and that their anterograde memory impairments prevent them from gaining a lexical or semantic representation of newly seen nonwords. If priming depends upon the activation of an established representation (e.g. [27]), it may be hypothesized that amnesic patients can show intact priming only when they have premorbid knowledge of the primed response, i.e. when they possess a normal initial representation of that stimulus. It is easy to identify knowledge of words as being the basis of verbal priming. but is less clear what could constitute a knowledge base for nonverbal priming. The present study sought to discover whether an amnesic patient could show normal priming with stimuli that were patterns and that lacked premorbidly established mental representations of the sort that appear necessary for verbal priming. Dot-pattern stimuli were used that could be organized or parsed perceptually to suggest a variety of figures (Fig. I ). We postulated that the perceptual interpretation of a dot pattern depended upon flexible visual processes that could be influenced by prior experience with a particular figural organization of the dot pattern. If such priming effects were to occur in normal control subjects (NCS), it would be possible to compare their priming effects to those of an amnesic patient who, unlike the NCS, would be unable to remember the figures that were biasing the later perceptual organization of the dot patterns. Priming Study 1 examined whether experience with a figure primed (above a baseline or control condition) the perceptual organization of a dot pattern in NCS and in the amnesic patient H.M. Priming Study 2 was an extension of Study 1 that employed a different method of establishing a baseline. Also, a recognition memory study was conducted in order to NONVERBAL PRIMING IN AMNESIA 419 establish whether H.M. could remember the figures (i.e. the source ofthe priming) at the time that the status of the priming effect was measured. METHOD Subjects The amnesic patient H.M. (aged 61 or 62 years in the several testing sessions, with 12 years ofeducation) and 15 NCS participated in this study. H.M. underwent bilateral medial temporal-lobe resection in 1953. at age 27. in an attempt to alleviate his otherwise intractable epilepsy 1371. The surgical removal was estimated to extend 8 cm back from the tips of the temporal lobes, including the prepyriform gyrus, uncus, amygdala. hippocampus. and parahippocampal gyrus. Temporal neocortex was reported to have been spared. Since the resection. H.M. has had a severe and pervasive anterograde amnesia for verbal and nonverbal materials in all modalities [8. 381. H.M. took part in 4 testing series that were at least 2 months apart: Priming Study 1 in April, 1986: the recognition-memory tests in February, 1987; a replication of Priming Study 1in April. 1987: and Priming Study 2 in November. 1987. In Priming Study 1, five men and six women constituted the NCS group, which had a mean age of 56.8 years (range 49-65) and a mean educational level of 13.9 years (range 1I-18). In Priming Study 2. two men and one woman constituted the NCS group: they had a mean age of 59.7 years (range 5CL74) and a mean educational level of 15.7 (range 14-17). For the test of recognition memory. two women and one man constituted the NCS group: they had a mean age 66.3 years (range 57-82) and a mean educational level of 13.7 (range 12-17). Materials The stimuli, taken from GARNER [ 161. were derived from six dot patterns. each consisting offive dots from the nine possible dots in a 3 x 3 square matrix (Fig. I). For each dot pattern. three target figures were constructed by connecting the five dots with straight lines. Three 6-item priming test forms were made by randomly selecting one target figure for each dot pattern. Explicit recognition memory for the figures was measured using 4-choice recognition tests. There were three recognition memory tests, each ofwhich was paired to one of the priming tests in that the same target figures were used for the corresponding priming and recognition tests, For each recognition item. a dot pattern was shown at the top of the page and four figures that connected the dots were shown at the bottom. One figure was the target and three were foils. Procedure For Priming Study 1, there were four test sessions. In Session I, subjects were asked to draw any figure onto each dot pattern that connected all the dots with straight lines. The figures that subjects drew constituted their baseline figures. In Session 2, which always occurred at least 6 hr later, subjects were asked to copy six target figures from one form onto corresponding dot patterns (each figure was above the corresponding pattern on an 8; x 11 in. piece of paper). Then, the materials were removed. and subjects were asked to write down the names of as many famous entertainers from the 20th~century as they could: this interference task was done for 3 min. Next. subjects were given the dot patterns (without any lines) and asked to draw any figure that connected the dots in each pattern with straight lines. In Session 3. the same procedure was followed except that a second. different set of target figures were copied onto the same dot patterns. and subjects were asked to write down the names of as many famous political figures from the ZOth-century as they could for the interference task. In Session 4, the third set of target ligures were copied onto the dot patterns. and subjects were asked to write down the names of as many athletes from the ZOthcentury as they could for the 3-min interference task. Unlike Sessions 2 and 3, subjects were then asked to draw the same figures they had just copied onto the dot patterns. Thus, Session 4 provided a measure of cued recall (the dot patterns being the cues) of incidentally encoded figures. The three test forms were administered in the same order for all subjects, with a day between Sessions 2. 3 and 4. H.M. participated in all four sessions on each of two separate occasions, a year apart. The protocol was modified for Priming Study 2, which was conducted 6 months after Study 1. As before, subjects drew the first figure that came to mind on each of the dot patterns. These figures served as baseline ligures. Then, at least 6 hr later, subjects copied target fgures (from the same set used in Priming Study I )that had been selected on the basis of their not being drawn in the baseline session. This procedure ensured that none ofthe target figures were an individual subject’s primary, or spontaneous, perceptual organization of the dot patterns. The rest of the test (copy figures, the interference task, and drawing figures onto dot patterns) was administered as described above. For the separate test of recognition memory. subjects copied one set of target figures onto dot patterns. Following the same 3-min delay task used in the priming test, subjects were asked to indicate which one of the four figures on the bottom of each page they had copied earlier onto the dot pattern displayed at the top of each page. Each of the NCS did this task once with six target figures; H.M. did this task with IX target figures, 6 per session in each of 3 sessions. TARGET J. D. E. GABRIELI et ul. SOME OTHER POSSIBLE COMPLETIONS Fig. I. Dot patterns are shown in column one. Examples of target figures copied onto dot patterns (i.e. primed figures) are shown in column two. Some other figures that could be drawn onto dot patterns are shown In the remaining columns. RESULTS In order to determine whether the control subjects demonstrated priming in Study 1, paired comparisons were made between the number of target figures drawn in the baseline condition and the number drawn in the primed (post-copying) condition. In baseline Session 1, the control subjects drew randomly a mean of 0.27 (SD, 0.47) target figures used in Session 2 compared to mean of 1.27 (SD, 0.64) target figures following the copying in Session 2. This difference was significant (r = 5.24, d.f. = 10, P~0.01. one-tailed), indicating NONVERBAL PRIMING IN AMPU’ESIA JZI that copying a target figure onto a dot pattern increased the probability of its subsequently being drawn freely onto the same dot pattern. In baseline Session 1. the control subjects drew randomly a mean of 1.18 (SD, 0.75) target figures used in Session 3 compared to a mean of 1.91 (SD, 1.04) target figures following the copying in Session 3. This difference also was significant (r = 1.90, d.f. = 10, P