Recognizing identical versus similar categorically related common objects: further evidence for degraded gist representations in amnesia.

Studies have shown lower false recognition of semantically related lure words in patients with global amnesia than in matched controls. This pattern has been interpreted as suggesting that medial temporal and diencephalic structures that are damaged in amnesia and that contribute to veridical memory also contribute to false recognition. It has been argued that whereas controls form and retain a well-organized representation of the semantic gist of studied items, patients with amnesia can retain only a degraded gist representation. However, these studies are subject to an alternative interpretation involving greater source confusions in controls. The authors used a categorized-pictures paradigm to test recognition under conditions in which source confusions were unlikely to occur. Relative to controls, patients with amnesia showed reduced false recognition of categorically related pictorial lures, thereby supporting the notion of degraded gist representations in amnesia.

Perceptual specificity in visual object priming: functional magnetic resonance imaging evidence for a laterality difference in fusiform cortex.

Seeing an object on one occasion may facilitate or prime processing of the same object if it is later again encountered. Such priming may also be found -- but at a reduced level -- for different but perceptually similar objects that are alternative exemplars or 'tokens' of the initially presented object. We explored the neural correlates of this perceptual specificity using event-related functional magnetic resonance imaging (fMRI) procedures, contrasting neural activity when participants made object classification decisions (size judgments) regarding previously presented objects (repeated same), alternative exemplars of previously presented objects (repeated different), or entirely new objects (novel). Many frontal regions (including bilateral frontal operculum, bilateral posterior inferior frontal/precentral, left anterior inferior frontal, and superior frontal cortices) and multiple late visual and posterior regions (including middle occipital, fusiform, fusiform-parahippocampal, precuneus, and posterior cingulate, all bilaterally), demonstrated reduced neural activity for repeated compared to novel objects. Greater repetition-induced reductions were observed for same than for different exemplars in several of these regions (bilateral posterior inferior frontal, right precuneus, bilateral middle occipital, bilateral fusiform, bilateral parahippocampal and bilateral superior parietal). Additionally, right fusiform (occipitotemporal) cortex showed significantly less priming for different versus same exemplars than did left fusiform. These findings converge with behavioral evidence from divided visual field studies and with neuropsychological evidence underscoring the key role of right occipitotemporal cortex in processing specific visual form information; possible differences in the representational-functional role of left fusiform are discussed.

Task-specific repetition priming in left inferior prefrontal cortex.

Previous neuroimaging studies have shown that activation in left inferior prefrontal cortices (LIPC) is reduced during repeated (primed) relative to initial (unprimed) stimulus processing. These reductions in anterior (approximately BA 45/47) and posterior (approximately BA 44/6) LIPC activation have been interpreted as reflecting implicit memory for initial semantic or phonological processing. However, prior studies do not unambiguously indicate that LIPC priming effects are specific to the recapitulation of higher-level (semantic and/or phonological), rather than lower-level (perceptual), processes. Moreover, no prior study has shown that the patterns of priming in anterior and posterior LIPC regions are dissociable. To address these issues, the present fMRI study examined the nature of priming in LIPC by examining the task-specificity of these effects. Participants initially processed words in either a semantic or a nonsemantic manner. Subsequently, participants were scanned while they made semantic decisions about words that had been previously processed in a semantic manner (within-task repetition), words that had been previously processed in a nonsemantic manner (across-task repetition), and words that had not been previously processed (novel words). Behaviorally, task-specific priming was observed: reaction times to make the semantic decision declined following prior semantic processing but not following prior nonsemantic processing of a word. Priming in anterior LIPC paralleled these results with signal reductions being observed following within-task, but not following across-task, repetition. Importantly, neural priming in posterior LIPC demonstrated a different pattern: priming was observed following both within-task and across-task repetition, with the magnitude of priming tending to be greater in the within-task condition. Direct comparison between anterior and posterior LIPC regions revealed a significant interaction. These findings indicate that anterior and posterior LIPC demonstrate distinct patterns of priming, with priming in the anterior region being task-specific, suggesting that this facilitation derives from repeated semantic processing of a stimulus.

Escape from illusion: reducing false memories.

Illusory memories are unsettling, but far from uncommon. Over the past several years, increasing experimental and theoretical attention has focused on misattribution errors that occur when some form of memory is present but attributed to an incorrect time, place or source. Demonstrations of errors and distortions in remembering raise a question with important theoretical and practical implications: how can memory misattributions be reduced or avoided? We consider evidence that documents the occurrence of illusory memories, particularly false recognition responses, and then review three ways in which memory distortion can be minimized.

Functional MRI evidence for a role of frontal and inferior temporal cortex in amodal components of priming.

Changes in human brain activity associated with repetition priming during word generation were characterized across a series of neuroimaging and behavioural studies. Repetition priming was consistently observed behaviourally as a decrease in response latency for repeated items, and was found for both visually and aurally cued word-generation tasks. Brain imaging using whole-brain functional MRI identified neural correlates of these effects. The principal effect of priming was to reduce neural activity within regions that were already being used to perform the word-generation tasks. Repeated word generation in response to visual cues was correlated with anatomically selective reductions in activity within the left frontal cortex along the inferior frontal gyrus and inferior temporal regions and, to a lesser degree, in specific earlier visual regions. These reductions were reversed when new items were presented, indicating that they were item-specific. Repeated word generation in response to aural cues also showed anatomically selective activity reductions within the left frontal and inferior temporal regions, indicating that these activity reductions were not dependent on the perceptual modality of the cue. The auditory cortex showed minimal repetition-related reductions. The presence of activity within left frontal regions that decreases as a function of item repetition for both visual and auditory cues suggests that these reductions may underlie an amodal repetition-priming effect existing at processing stages involving lexical/semantic search and access. The surprising finding that activity reductions in the inferior temporal cortex can be linked to repetition of either visual or auditory cues further suggests that these regions may be modulated in a top-down fashion during repetition priming, independent of (or in parallel with) stimulus-driven perceptual processes. Taken collectively, the data converge on a neural correlate of lexical/semantic priming. Amodal lexical/semantic processes, which may be triggered initially by modality-specific cues, proceed via an interaction between frontal and posterior brain regions. These interdependent regions show activity reductions that correlate with facilitated task performance when items are repeated.

When encoding yields remembering: insights from event-related neuroimaging.

To understand human memory, it is important to determine why some experiences are remembered whereas others are forgotten. Until recently, insights into the neural bases of human memory encoding, the processes by which information is transformed into an enduring memory trace, have primarily been derived from neuropsychological studies of humans with select brain lesions. The advent of functional neuroimaging methods, such as positron emission tomography (PET) and functional magnetic resonance imaging (fMRI), has provided a new opportunity to gain additional understanding of how the brain supports memory formation. Importantly, the recent development of event-related fMRI methods now allows for examination of trial-by-trial differences in neural activity during encoding and of the consequences of these differences for later remembering. In this review, we consider the contributions of PET and fMRI studies to the understanding of memory encoding, placing a particular emphasis on recent event-related fMRI studies of the Dm effect: that is, differences in neural activity during encoding that are related to differences in subsequent memory. We then turn our attention to the rich literature on the Dm effect that has emerged from studies using event-related potentials (ERPs). It is hoped that the integration of findings from ERP studies, which offer higher temporal resolution, with those from event-related fMRI studies, which offer higher spatial resolution, will shed new light on when and why encoding yields subsequent remembering.

Reducing gist-based false recognition in older adults: encoding and retrieval manipulations.

Using a categorized pictures paradigm, Koutstaal and Schacter (1997) reported high levels of false recognition of lures that were categorically related to presented items. Although also shown by younger adults, false recognition was markedly higher for older adults. To probe the factors underlying this age difference, these experiments required participants to engage in more careful scrutiny of the items at retrieval or to notice specific differentiating perceptual features of the objects during encoding. False recognition was reduced with each of these manipulations, but neither manipulation, either separately or together, eliminated the age difference in false recognition. Older adults can considerably reduce false recognition if encouraged to use more stringent decision criteria. Persistent difficulty in opposing familiarity-based responding and comparatively more generic encoding may contribute to residual deficits.

Facilitation and impairment of event memory produced by photograph review.

Selectively reviewing some items from a larger set of previously learned items increases memory for the items that are reviewed but may also be accompanied by a cost: Memory for the nonreviewed items may be impaired relative to cases where no review occurs at all. This cost to nonreviewed items has primarily been shown in contexts of verbal list learning and in situations where the reviewed and nonreviewed items are categorically or semantically related. Using a more naturalistic impetus to selective review--photographs relating to previously experienced events--we assessed whether the memory of older and younger adults for unrelated complex activities that they themselves had performed was also impaired due to nonreview. Both younger and older adults showed impaired memory for nonreviewed activities when tested with free recall (Experiment 1), but not when tested with recognition or cued recall (Experiment 2). If mitigating retrieval cues are unavailable, selective review may impair memory for nonreviewed everyday events.

Memory, consciousness and neuroimaging.

Neuroimaging techniques that allow the assessment of memory performance in healthy human volunteers while simultaneously obtaining measurements of brain activity in vivo may offer new information on the neural correlates of particular forms of memory retrieval and their association with consciousness and intention. We consider evidence from studies with positron emission tomography and functional magnetic resonance imaging indicating that priming, a form of implicit retrieval, is associated with decreased activity in various cortical regions. We also consider evidence concerning the question of whether two components of explicit retrieval--intentional or effortful search and successful conscious recollection--are preferentially associated with increased activity in prefrontal and medial temporal regions, respectively. Last, we consider recent efforts to probe the relation between the phenomenological character of remembering and neural activity. In this instance we broaden our scope to include studies employing event-related potentials and consider evidence concerning the neural correlates of qualitatively different forms of memory, including memory that is specifically associated with a sense of self, and the recollection of particular temporal or perceptual features that might contribute to a rich and vivid experience of the past.

Building memories: remembering and forgetting of verbal experiences as predicted by brain activity.

A fundamental question about human memory is why some experiences are remembered whereas others are forgotten. Brain activation during word encoding was measured using blocked and event-related functional magnetic resonance imaging to examine how neural activation differs for subsequently remembered and subsequently forgotten experiences. Results revealed that the ability to later remember a verbal experience is predicted by the magnitude of activation in left prefrontal and temporal cortices during that experience. These findings provide direct evidence that left prefrontal and temporal regions jointly promote memory formation for verbalizable events.

Post-event review in older and younger adults: improving memory accessibility of complex everyday events.

Recalling an event at 1 time often increases the likelihood that it will be remembered at a still later time. The authors examined the degree to which older and younger adults' memory for everyday events that they watched on a videotape was improved by later seeing photographs or reading brief verbal descriptions of those events. Both older and younger adults recalled more events, in greater detail, with than without review. Verbal descriptions enhanced later recall to the same degree as reviewing photographs. Younger adults generally gained more from review than older adults on measures of the absolute number of details recalled and when facilitation was assessed relative to a no-review control condition, but not when memory for reviewed events was expressed as a proportion of each individual's total recall. Post-event review has clear potential practical benefits for improving memory of older adults.

Functional-anatomic study of episodic retrieval using fMRI. I. Retrieval effort versus retrieval success.

A number of recent functional imaging studies have identified brain areas activated during tasks involving episodic memory retrieval. The identification of such areas provides a foundation for targeted hypotheses regarding the more specific contributions that these areas make to episodic retrieval. As a beginning effort toward such an endeavor, whole-brain functional magnetic resonance imaging (fMRI) was used to examine 14 subjects during episodic word recognition in a block-designed fMRI experiment. Study conditions were manipulated by presenting either shallow or deep encoding tasks. This manipulation yielded two recognition conditions that differed with regard to retrieval effort and retrieval success: shallow encoding yielded low levels of recognition success with high levels of retrieval effort, and deep encoding yielded high levels of recognition success with low levels of effort. Many brain areas were activated in common by these two recognition conditions compared to a low-level fixation condition, including left and right prefrontal regions often detected during PET episodic retrieval paradigms (e.g., R. L. Buckner et al., 1996, J. Neurosci. 16, 6219-6235) thereby generalizing these findings to fMRI. Characterization of the activated regions in relation to the separate recognition conditions showed (1) bilateral anterior insular regions and a left dorsal prefrontal region were more active after shallow encoding, when retrieval demanded greatest effort, and (2) right anterior prefrontal cortex, which has been implicated in episodic retrieval, was most active during successful retrieval after deep encoding. We discuss these findings in relation to component processes involved in episodic retrieval and in the context of a companion study using event-related fMRI.

Functional-anatomic study of episodic retrieval. II. Selective averaging of event-related fMRI trials to test the retrieval success hypothesis.

In a companion paper (R. L. Buckner et al., 1998, NeuroImage 7, 151-162) we used fMRI to identify brain areas activated by episodic memory retrieval. Prefrontal areas were shown to differentiate component processes related to retrieval success and retrieval effort in block-designed paradigms. Importantly, a right anterior prefrontal area was most active during task blocks involving greatest retrieval success, consistent with an earlier PET study by M. D. Rugg et al. (1996, Brain 119, 2073-2083). However, manipulation of these variables within the context of blocked trials confounds differences related to varying levels of retrieval success with potential shifts in subjects' strategies due to changes in the probability of target events across blocks. To test more rigorously the hypothesis that certain areas are directly related to retrieval success, we adopted recently developed procedures for event-related fMRI. Fourteen subjects studied words under deep encoding and were then tested in a mixed trial paradigm where old and new words were randomly presented. This recognition testing procedure activated similar areas to the blocked trial paradigm, with all areas showing similar levels of activation across old and new items. Of critical importance, significant activation was detected in right anterior prefrontal cortex for new items when subjects correctly indicated they were new (correct rejections). These findings go against the retrieval success hypothesis as formally proposed and provide an important constraint for interpretation of this region's role in episodic retrieval. Furthermore, anterior prefrontal activation was found to occur late, relative to other brain areas, suggesting that it may be involved in retrieval verification or monitoring processes or perhaps even in anticipation of subsequent trial events (although an alternative possibility, that the late onset is mediated by a late vascular response, cannot be ruled out). These findings and their relation to the results obtained in the companion blocked-trial paradigm are discussed.

Functional-anatomic correlates of object priming in humans revealed by rapid presentation event-related fMRI.

Human functional-anatomic correlates of object repetition were explored in a cohort of 20 subjects using fMRI. Subjects performed an object classification task where the target objects were either novel or repeated. Objects appeared rapidly, one every 2 s, in a randomly intermixed task design similar to traditional behavioral, event-related potential (ERP), and single-unit physiological studies. Recently developed event-related fMRI methods were used to analyze the data. Clear effects of repetition were observed. Brain areas in midlevels of the processing hierarchy, including extrastriate visual cortex extending into inferotemporal cortex and left dorsal prefrontal cortex, showed reductions in the amount of activation after repetition. By contrast, early visual areas and output motor areas were activated equally by both novel and repeated objects and did not show effects of repetition, suggesting that the observed correlates of repetition were anatomically selective. We discuss these findings in relation to previous positron emission tomography (PET) and fMRI studies of item repetition and single-unit physiological studies; we also address the broad impact that rapid event-related fMRI is likely to have on functional neuroimaging.

The cognitive neuroscience of constructive memory.

Numerous empirical and theoretical observations point to the constructive nature of human memory. This paper reviews contemporary research pertaining to two major types of memory distortions that illustrate such constructive processes: (a) false recognition and (b) intrusions and confabulations. A general integrative framework that outlines the types of problems that the human memory system must solve in order to produce mainly accurate representations of past experience is first described. This constructive memory framework (CMF) emphasizes processes that operate at encoding (initially binding distributed features of an episode together as a coherent trace; ensuring sufficient pattern separation of similar episodes) and also at retrieval (formation of a sufficiently focused retrieval description with which to query memory; postretrieval monitoring and verification). The framework is applied to findings from four different areas of research: cognitive studies of young adults, neuropsychological investigations of brain-damaged patients, neuroimaging studies, and studies of cognitive aging.

Functional neuroimaging studies of encoding, priming, and explicit memory retrieval.

Human functional neuroimaging techniques provide a powerful means of linking neural level descriptions of brain function and cognition. The exploration of the functional anatomy underlying human memory comprises a prime example. Three highly reliable findings linking memory-related cognitive processes to brain activity are discussed. First, priming is accompanied by reductions in the amount of neural activation relative to naive or unprimed task performance. These reductions can be shown to be both anatomically and functionally specific and are found for both perceptual and conceptual task components. Second, verbal encoding, allowing subsequent conscious retrieval, is associated with activation of higher order brain regions including areas within the left inferior and dorsal prefrontal cortex. These areas also are activated by working memory and effortful word generation tasks, suggesting that these tasks, often discussed as separable, might rely on interdependent processes. Finally, explicit (intentional) retrieval shares much of the same functional anatomy as the encoding and word generation tasks but is associated with the recruitment of additional brain areas, including the anterior prefrontal cortex (right > left). These findings illustrate how neuroimaging techniques can be used to study memory processes and can both complement and extend data derived through other means. More recently developed methods, such as event-related functional MRI, will continue this progress and may provide additional new directions for research.

False recollection induced by photographs: a comparison of older and younger adults.

Looking at photographs constitutes an important everyday memory activity for older adults. The authors found that reviewing photographs of events seen earlier in a videotape increases the likelihood that both older and younger adults remember specific details from the reviewed event (W. Koutstaal, D. L. Schacter, M. K. Johnson, K. E. Angell, & M. S. Gross, 1977). In the present study, the authors report 2 experiments demonstrating that photo review can also produce false recollection in elderly adults: After reviewing photos of events that had not been shown earlier in a videotape, older but not younger adults were later more likely to "remember" that those events had been shown in the videotape. False recollection induced by photo review appears to reflect an age-related deficit in source-monitoring abilities.

False memories and aging.

Although memory processes and systems usually operate reliably, they are sometimes prone to distortions and illusions. Here we review evidence indicating that cognitive aging is often associated with increased susceptibility to various kinds of false recollections. Accumulating data indicate that older adults frequently have special difficulties recollecting the source of information, which in turn renders them vulnerable to confusing perceived and imagined experiences, and to related kinds of memory distortions. Evidence from studies of false recall and recognition indicate that older adults are sometimes more likely than younger adults to remember events that never happened, reflecting the influence of indistinct encoding of events and the use of lenient criteria during retrieval. Neuroimaging studies suggest that age-related changes in medial temporal and frontal regions may play a role in the altered functioning of specific encoding and retrieval processes that give rise to memory distortions. Future studies of aging and false memories are likely to provide a promising avenue for illuminating basic mechanisms of memory distortion.

Late onset of anterior prefrontal activity during true and false recognition: an event-related fMRI study.

Previous studies using PET and fMRI to examine memory retrieval have been limited by the requirement to test different types of items in separate blocks and to average data across items and response types within blocks. We used recently developed procedures for analyzing event-related mixed trial data from fMRI experiments to compare brain activity during true recognition of previously studied words and false recognition of semantic associates. A previous PET study using blocked testing procedures reported similarities and differences in rCBF patterns associated with true and false recognition (Schacter et al., 1996a). We examined brain activity during blocked testing of studied words and nonstudied semantic associates (similar to PET), and also during event-related mixed trials, where studied words and nonstudied semantic associates are intermixed. Six subjects initially heard lists of semantically related words and were later tested for old/new recognition with studied words and nonstudied semantic associates, either in separate blocks or intermixed randomly for the event-related analysis. Compared to a fixation control condition, a variety of regions previously reported in the PET study showed significant activation for both true and false recognition, including anterior prefrontal, frontal opercular, medial parietal, and visual cortex extending into hippocampal/parahippocampal regions. Differences across trial types were not clearly present. Event-related analyses of time course data show a relatively late onset and sustained duration for anterior prefrontal signal changes compared to signal changes in other activated regions. Further study is needed to resolve whether this late onset originates from variance in hemodynamic response properties or is attributable to delayed neural activity. The delayed onset is consistent with the idea that anterior prefrontal regions participate in postretrieval monitoring processes.

Can cognitive neuroscience illuminate the nature of traumatic childhood memories?

Recent findings from cognitive neuroscience and cognitive psychology may help explain why recovered memories of trauma are sometimes illusory. In particular, the notion of defective source monitoring has been used to explain a wide range of recently established memory distortions and illusions. Conversely, the results of a number of studies may potentially be relevant to forgetting and recovery of accurate memories, including studies demonstrating reduced hippocampal volume in survivors of sexual abuse, and recovery from functional and organic retrograde amnesia. Other recent findings of interest include the possibility that state-dependent memory could be induced by stress-related hormones, new pharmacological models of dissociative states, and evidence for 'repression' in patients with right parietal brain damage.