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Brain Potentials Reflect Behavioral Differences in True and False Recognition Brain Potentials Reflect Behavioral Differences in True and False Recognition Tim Curran1, Daniel L. Schacter2, Marcia K. Johnson3, and Ruth Spinks1 Abstract & People often falsely recognize nonstudied lures that are showed late (1000±1500 msec), right frontal event-related semantically similar to previously studied words. Behavioral brain potentials (ERPs) that were more positive for targets and research suggests that such false recognition is based on high lures compared with new items. The right frontal differences semantic overlap between studied items and lures that yield a are interpreted as reflecting postretrieval evaluation processes feeling of familiarity, whereas true recognition is more often that were more likely to be engaged by Good than Poor associated with the recollection of details. Despite this performers. Both Good and Poor performers showed a behavioral evidence for differences between true and false parietal ERP old/new effect (400±800 msec), but only Poor recognition, research measuring brain activity (PET, fMRI, performers showed a parietal old/lure difference. These ERP) has not clearly differentiated corresponding differences results are consistent with the view that the parietal and in brain activity. A median split was used to separate subjects frontal ERP old/new effects reflect dissociable processes into Good and Poor performers based on their discrimination related to recollection. & of studied targets from similar lures. Only Good performers INTRODUCTION lap (e.g., Johnson & Raye, 1981). Here, we compare the Understanding of human memory has been advanced by brain activity of individuals who show Good versus Poor the investigation of memory errors, distortions, and discrimination between old items and semantically re- illusions (Schacter, Norman, & Koutstaal, 1998; Roedi- lated new items in order to help identify the brain ger, 1996; Johnson, Hashtroudi, & Lindsay, 1993). Such processes underlying the cognitive processes involved research indicates that memory is often a reconstructive in remembering. process rather than a verbatim record of past events, Many recent studies of false memory have used a and that remembering entails attributions about the procedure reported initially by Deese (1959) and subse- origin of the information that comes to mind. Theore- quently modified by Roediger and McDermott (1995) in tical discussions of these attributional or ``source mon- which subjects falsely remember words that are seman- itoring'' processes emphasize that true and false tically associated to previously studied words (the ``DRM memories arise via powerful but imperfect cognitive procedure''). Roediger and McDermott's subjects heard processes. For example, memory distortions sometimes lists of semantically associated words (e.g., candy, sour, occur because people lack or do not access (``recollect'') sugar, bitter, good, taste, tooth, etc.) that were related critical event details, or because people inappropriately to a nonpresented theme word (e.g., sweet). When the weigh one kind of information (e.g., familiarity) out of theme words were presented as lures on a recognition proportion to its diagnostic value (e.g., Schacter, Israel, memory test, subjects claimed to recognize the critical & Racine, 1999; Johnson et al., 1993; Johnson & Raye, lures as often as actually heard words. These results are 1998; Curran, Schacter, Norman, & Galluccio, 1997). generally consistent with models of memory in which Recent event-related brain potential (ERP) and neuroi- recognition judgments are based on the global similarity maging studies suggest that true and false memories between studied and tested items (e.g., Arndt & Hirsh- sometimes can be distinguished in brain activity (John- man, 1998; Shiffrin & Steyvers, 1997; Clark & Gronlund, son et al., 1997; Schacter, Reiman, et al., 1996), as we 1996; Humphreys, Bain, & Pike, 1989; Hintzman, 1988; would expect based on the assumption that they come Gillund & Shiffrin, 1984; Murdock, 1982). Computation from feature distributions that do not completely over- of global similarity is often thought to underlie the ``familiarity'' component of dual-processes theories of recognition memory, whereas ``recollection'' entails the 1 Case Western Reserve University, 2 Harvard University, 3 Yale retrieval of information about individual items (Brainerd, University Reyna, & Kneer, 1995; Hintzman & Curran, 1994; Yone- D 2001 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 13:2, pp. 201±216 linas, 1994; Jacoby, 1991). Similarly, in the source-moni- Oppy, 1992; Hintzman & Curran, 1994, 1995). ERPs were toring framework, familiarity is proposed to arise from a measured during a recognition test in which subjects less differentiated phenomenal experience than does were told to respond ``yes'' only if the test word was the experience of recollection (Johnson et al., 1993). studied in the same plurality. A left, superior, anterior Several studies have sought to differentiate the phe- N400-like component (300±500 msec) was more nega- nomenal characteristics of true and false recognition tive for new words than lures or studied words, so it with the DRM paradigm. The ``remember±know'' pro- behaved consistently with a familiarity process that was cedure requires subjects to differentiate between items insensitive to the plurality of studied words. This famil- ``remembered'' through detailed recollection and items iarity-sensitive component was dubbed the ``FN400'' merely ``known'' as previously studied based on vague because it was similar to the N400 (e.g., Kutas & Hillyard, feelings of familiarity (Gardiner & Java, 1993; Tulving, 1980; Kutas & Van Petten, 1994), but more frontally 1985). False alarms to critical lures are sometimes asso- distributed (see also, Curran, 1999). Left parietal ERPs ciated with a high rate of ``remember'' responses (Math- (400±800 msec) were more positive for studied words er, Henkel, & Johnson, 1997; Norman & Schacter, 1997; than for lures or new wordsÐsuggesting a specific Roediger & McDermott, 1995), suggesting that subjects recollection process that was sensitive to the plurality are falsely recollecting illusory perceptual details about of studied words. Rugg and colleagues have identified a nonstudied words. However, such responses also may similar, ``left parietal ERP old/new effect'' that they reflect high-confidence judgments based on semantic suggest is related to the recollection of specific informa- familiarity (Curran et al., 1997; Hirshman & Master, 1997; tion (reviewed in, Allan, Wilding, & Rugg, 1998). The Donaldson, 1996). In fact, carefully probing the charac- parietal old/new effect has been associated with source teristics of ``remembering'' has revealed that recollection recollection (Wilding, Doyle, & Rugg, 1995; Wilding & of perceptual details (e.g., auditory attributes of the Rugg, 1996, 1997a, 1997b), recollection of associative studied words) is more prevalent in true than false information (Donaldson & Rugg, 1998, 1999; Tendolkar, recognition (Mather et al., 1997; Norman & Schacter, Doyle, & Rugg, 1997; Rugg, Schloerscheidt, Doyle, Cox, 1997). Such average differences between true and false & Patching, 1996), and discrimination between studied memories are consistent with the proposal that true and words (e.g., BARTER, VALLEY) and nonstudied conjunc- false memories arise from common processes applied to tions (e.g., BARLEY) (Rubin, Van Petten, Glisky, & New- memories that differ in qualitative characteristics de- berg, 1999). Furthermore, the parietal old/new effect is pending on their source (Johnson et al., 1993; Johnson larger when subjects judge recognized items as ``remem- & Raye, 1981). bered'' than ``known'' (Rugg, Schloerscheidt, & Mark, A related line of research with the DRM paradigm has 1998; DuÈzel et al., 1997; Smith, 1993). asked whether true and false recognition are associated Frontal ERP effects have been related to source with different patterns of brain activity as we would recognition in a number of studies. Late frontal ERPs expect based on behavioral evidence such as subjective have been associated with recognition of study-source ratings. A PET study suggested that temporo-parietal attributes such as format (words vs. pictures; Johnson, brain regions involved with auditory/phonological pro- Kounios, & Nolde, 1996), speaker's voice (Wilding & cessing are more active during true recognition of pre- Rugg, 1996, 1997a; Wilding, 1999; Senkfor & Van Petten, viously heard words than false recognition of semantically 1998), encoding task (Wilding, 1999), associative pairing similar lures (Schacter, Reiman, et al., 1996). This pattern (Donaldson & Rugg, 1998), and temporal order (Trott, of activation is consistent with greater retrieval of per- Friedman, Ritter, Fabiani, & Snodgrass, 1999). These ceptual detail for true than false memories, but no effects are often greater over the right hemisphere evidence of temporoparietal activation during true or where late ERPs (600±1900 msec) are more positive in false recognition was observed with fMRI when test response to old than new stimuli (reviewed in Allan conditions were either blocked (as in PET) or mixed et al., 1998). Contradictory reports have indicated that (Schacter, Buckner, Koutstaal, Dale, & Rosen, 1997). the late frontal positivity is greater for old stimuli Overall, small PET and fMRI differences between true associated with correct than incorrect source judge- and false recognition have been dwarfed by similarities in ments
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