Wilma Koutstaal

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.

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.

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.

Neural mechanisms of visual object priming: Evidence for perceptual and semantic distinctions in fusiform cortex

Previous functional imaging studies have shown that facilitated processing of a visual object on repeated, relative to initial, presentation (i.e., repetition priming) is associated with reductions in neural activity in multiple regions, including fusiform/lateral occipital cortex. Moreover, activity reductions have been found, at diminished levels, when a different exemplar of an object is presented on repetition. In one previous study, the magnitude of diminished priming across exemplars was greater in the right relative to the left fusiform, suggesting greater exemplar specificity in the right. Another previous study, however, observed fusiform lateralization modulated by object viewpoint, but not object exemplar. The present fMRI study sought to determine whether the result of differential fusiform responses for perceptually different exemplars could be replicated. Furthermore, the role of the left fusiform cortex in object recognition was investigated via the inclusion of a lexical/semantic manipulation. Right fusiform cortex showed a significantly greater effect of exemplar change than left fusiform, replicating the previous result of exemplar-specific fusiform lateralization. Right fusiform and lateral occipital cortex were not differentially engaged by the lexical/semantic manipulation, suggesting that their role in visual object recognition is predominantly in the visual discrimination of specific objects. Activation in left fusiform cortex, but not left lateral occipital cortex, was modulated by both exemplar change and lexical/semantic manipulation, with further analysis suggesting a posterior-to-anterior progression between regions involved in processing visuoperceptual and lexical/semantic information about objects. The results are consistent with the view that the right fusiform plays a greater role in processing specific visual form information about objects, whereas the left fusiform is also involved in lexical/semantic processing.

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.

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.

Older Adults Encode—But Do Not Always Use—Perceptual Details Intentional Versus Unintentional Effects of Detail on Memory Judgments

Investigations of memory deficits in older individuals have concentrated on their increased likelihood of forgetting events or details of events that were actually encountered (errors of omission). However, mounting evidence demonstrates that normal cognitive aging also is associated with an increased propensity for errors of commission—shown in false alarms or false recognition. The present study examined the origins of this age difference. Older and younger adults each performed three types of memory tasks in which details of encountered items might influence performance. Although older adults showed greater false recognition of related lures on a standard (identical) old/new episodic recognition task, older and younger adults showed parallel effects of detail on repetition priming and meaning-based episodic recognition (decreased priming and decreased meaning-based recognition for different relative to same exemplars). The results suggest that the older adults encoded details but used them less effectively than the younger adults in the recognition context requiring their deliberate, controlled use.

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 thenonreviewed 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.

False recognition of abstract versus common objects in older and younger adults: testing the semantic categorization account.

Older adults often demonstrate higher levels of false recognition than do younger adults. However, in experiments using novel shapes without preexisting semantic representations, this age-related elevation in false recognition was found to be greatly attenuated. Two experiments tested a semantic categorization account of these findings, examining whether older adults show especially heightened false recognition if the stimuli have preexisting semantic representations, such that semantic category information attenuates or truncates the encoding or retrieval of item-specific perceptual information. In Experiment 1, ambiguous shapes were presented with or without disambiguating semantic labels. Older adults showed higher false recognition when labels were present but not when labels were never presented. In Experiment 2, older adults showed higher false recognition for concrete but not abstract objects. The semantic categorization account was supported.

PERCEPTUALLY BASED FALSE RECOGNITION OF NOVEL OBJECTS IN AMNESIA: EFFECTS OF CATEGORY SIZE AND SIMILARITY TO CATEGORY PROTOTYPES

Previous research suggests that amnesics may show impaired semantically based false recognition under conditions where control participants show high levels of gist-based errors, but little or no impairment when controls show less robust false recognition. Using abstract novel objects, we examined perceptually based false recognition in amnesics under conditions designed to induce differing levels of false recognition in controls. Whereas amnesics showed significantly impaired false recognition for category prototypes, and numerically impaired false recognition when many perceptually similar exemplars were studied-conditions where controls showed high rates of illusory recognition-amnesics and controls showed lower, and comparable, levels of false recognition when few related exemplars were studied, or lures were at a far transformational distance from the prototype. Although amnesics may be able to extract some information regarding the perceptual “gist” of studied items, they appear to do so less effici...