Perceptual Thresholds and Priming in Amnesia
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Neuropsychology In the public domain 1995, Vol. 9, No. 1,3-15 Perceptual Thresholds and Priming in Amnesia Stephan B. Hamann Larry R. Squire University of California, San Diego Veterans Affairs Medical Center, San Diego and University of California, San Diego Daniel L. Schacter Harvard University The widely accepted idea that perceptual priming is intact in amnesia was challenged recently by the suggestion that perceptual identification (PID) thresholds are elevated in amnesia and that this impairment could mask a priming deficit by artificially inflating priming scores. The authors examined the PID thresholds of amnesic patients across a wide range of stimulus conditions and accuracy levels. Baseline thresholds and priming effects were fully intact for all amnesic patients except in a condition using small stimuli (1.1° x 0.25° of visual angle). In that condition, only the patients with Korsakoff's syndrome were impaired. Accordingly, elevated perceptual thresholds are not a necessary consequence of amnesia, and normal priming in amnesia is not an artifact of threshold differences. The results support the conclusion that priming is independent of the brain structures important for declarative memory that are damaged in amnesia. Considerable evidence has accumulated in recent years for medial temporal lobe and diencephalic structures that are distinguishing between different kinds of memory that depend damaged in amnesia (Squire & Zola-Morgan, 1991; Zola- on multiple separate brain systems (Richardson-Klavehn & Morgan & Squire, 1993). Nondeclarative memory is indepen- Bjork, 1988; Schacter, 1987; Squire, 1982; Tulving, 1985; dent of these brain structures. Weiskrantz, 1990). The major distinction is between declara- The conclusion that nondeclarative memory is spared in tive (explicit) memory, which affords conscious recollection of amnesia is based on a considerable body of evidence compar- past facts or episodes, and nondeclarative (implicit) memory, ing normal and memory-impaired subjects. Perhaps the most which is assessed indirectly through performance (cf. Schacter, extensively studied form of nondeclarative memory is priming, 1994; Squire, Knowlton, & Musen, 1993). Although dissocia- the improvement in detecting or identifying a stimulus based tions can be demonstrated in normal subjects between these on its recent exposure (Schacter, Chiu, & Ochsner, 1993; two kinds of memory, amnesic patients provide a particularly Tulving & Schacter, 1990). In both normal subjects and compelling source of evidence for distinguishing between amnesic patients, priming has been demonstrated for familiar kinds of memory. Amnesic patients are severely impaired on and novel stimuli, including words, nonwords, simple line tests of declarative memory, but they perform normally on a patterns, and figures. These results can be summarized by the variety of nondeclarative memory tasks including skill learning statement that amnesic patients and control subjects exhibit (Brooks & Baddeley, 1976; Cohen & Squire, 1980; Musen, equivalent priming across many different tasks and types of Shimamura, & Squire, 1990; Nissen & Bullemer, 1987; Squire materials. & Frambach, 1990), adaptation level effects (Benzing & The notion that priming is intact in amnesic patients was Squire, 1989), artificial grammar learning and prototype learn- challenged recently, based on a study of correlations among ing (Knowlton & Squire, 1993; Knowlton, Ramus, & Squire, measures of priming, measures of recognition memory, and 1992), and priming (Shimamura, 1986; Tulving & Schacter, 1990). Declarative memory depends on the integrity of the quantitative magnetic resonance imaging (MRI) measures of brain damage in 3 groups of neurological patients (Jernigan & Ostergaard, 1993). The subject groups were patients with Stephan B. Hamann, Department of Psychiatry, University of California, San Diego; Larry R. Squire, Veterans Affairs Medical Alzheimer's disease, patients with Huntington's disease, amne- Center, San Diego, California, and Department of Psychiatry and sic patients, and control subjects. Priming was assessed with a Neurosciences, University of California, San Diego; Daniel L. Schacter, perceptual identification task (Cermak, Talbot, Chandler, & Department of Psychology, Harvard University. Wolbarst, 1985) in which previously studied words and new This research was supported by the Medical Research Service of the words were initially presented briefly and then for increasing Department of Veterans Affairs, National Institute of Mental Health durations until subjects could identify each word. (NIMH) Grants MH24600 and MH45398, the Office of Naval Re- Contrary to what might have been expected from previous search, and the McKnight Foundation. work, a multiple regression analysis found an association We thank Nicole Champagne, Brent Kronenberg, {Camilla Willoughby, and Joyce Zouzounis for research assistance. between priming and damage to "temporolimbic" structures Correspondence concerning this article should be addressed to (this region was reported to include the hippocampus, amyg- Larry R. Squire, Veterans Affairs Medical Center, 3350 La Jolla dala, and adjacent gray matter in the medial temporal lobe). Village Drive, San Diego, California 92161. Electronic mail may be The association between priming and temporolimbic damage sent to [email protected]. was not apparent in a simple correlational measure but S. HAMANN, L. SQUIRE, AND D. SCHACTER became significant in the multiple regression analysis, when comprehensive studies have not been conducted to investigate volume loss in the caudate nucleus was also taken into account. baseline performance levels of amnesic patients in priming The finding across subject groups was that loss of caudate tasks. nucleus volume was associated with improved priming scores, The finding of intact baseline performance scores in amnesic and temporolimbic damage was associated with poorer prim- patients in earlier studies, which were not designed specifically ing scores. These two influences (caudate nucleus damage and to assess baseline performance, is not sufficient to decide the temporolimbic damage) exerted opposing effects of similar issue. These studies commonly assessed baseline performance magnitude on priming. Accordingly, the two effects canceled under only one experimental condition, not across a wide each other and would have gone undetected unless they had range of performance. For example, in a recent study of been considered together in a multiple regression analysis. perceptual priming for words and nonwords (Haist, Musen, & On the basis of these results, Jernigan and Ostergaard Squire, 1991), amnesic patients exhibited fully intact baseline (1993) proposed that previous findings of intact priming in word identification performance in a condition that yielded amnesic patients may have been complicated by the presence approximately 50% correct identification accuracy. Yet, it is of undetected striatal damage. Specifically, it was proposed possible that at some other difficulty level a deficit in baseline that striatal damage should impair baseline performance performance would have been detected in the amnesic pa- scores in priming studies. As a result, priming scores would be tients. spuriously inflated, and any deficit in priming would thereby be In four experiments, we examined the possibility that masked. amnesic patients have a deficit in baseline performance that It is well known that baseline performance differences can could affect their scores on tests of priming. We assessed pose problems when comparing subject groups (Cermak et al., baseline and primed performance in amnesic patients and 1985; Cermak, Verfaellie, Milberg, & Letourneau, 1991; Chap- control subjects, using a perceptual identification task that man, Chapman, Curran, & Miller, 1994; Ellis & Young, 1988, sampled a wide range of difficulty levels from near 0% to near p. 284; Loftus, 1985; Snodgrass, 1989). If one group initially 100% performance accuracy. The logic behind this approach is performs more poorly than another, it may be easier for the simple. If normal baseline performance and normal priming poorer group to improve than the group that initially performs can be demonstrated for amnesic patients across a wide range well. For example, in one report (Heindel, Salmon, & Butters, of difficulty levels, then preserved priming in amnesic patients 1990), patients with Huntington's disease (HD) were impaired cannot be attributed to a deficit in baseline performance. relative to control subjects on a task of identifying fragmented In Experiment 1, we compared baseline perceptual identifi- pictures. Following a study phase, the HD patients exhibited cation ability in amnesic patients and control subjects, testing greater priming than control subjects. This result was ex- across a wide range of performance levels. We used an plained by noting that the HD patients were initially slower unusually small stimulus size to ensure that performance and less efficient than control subjects at the baseline task of would reach very low levels with brief exposure durations. In identifying the fragmented pictures. Accordingly, it was easier Experiment 2, the procedure for assessing baseline perfor- for their performance to improve. Although this example and mance was modified to conform to the procedure used in a the study by Jernigan and Ostergaard (1993) focus on the previous study that had found normal perceptual identification importance of striatal pathology