Oscillatory EEG correlates of episodic trace decay.

Recent studies suggest that human theta oscillations appear to be functionally associated with memory processes. It is less clear, however, to what type of memory sub-processes theta is related. Using a continuous word recognition task with different repetition lags, we investigate whether theta reflects the strength of an episodic memory trace or general processing demands, such as task difficulty. The results favor the episodic trace decay hypothesis and show that during the access of an episodic trace in a time window of approximately 200-400 ms, theta power decreases with increasing lag (between the first and second presentation of an item). LORETA source localization of this early theta lag effect indicates that parietal regions are involved in episodic trace processing, whereas right frontal regions may guide the process of retrieval. We conclude that episodic encoding can be characterized by two different stages: traces are first processed at parietal sites at approximately 300 ms, then further processing takes place in regions of the medial temporal lobe at approximately 500 ms. Only the first stage is related to theta, whereas the second is reflected by a slow wave with a frequency of approximately 2.5 Hz.

Mild hypoxia disrupts recollection, not familiarity.

Yonelinas et al. (2002) found that hypoxic patients exhibited deficits in recollection that left familiarity relatively unaffected. In contrast, Manns, Hopkins, Reed, Kitchener, and Squire (2003) studied a group of hypoxic patients who suffered severe and equivalent deficits in recollection and familiarity. We reexamine those studies and argue that the discrepancy in results is likely due to differences in the hypoxic groups that were tested (i.e., differences in amnestic severity, subject sampling methods, and patient etiology). Yonelinas et al. examined memory in 56 cardiac arrest patients who suffered a brief hypoxic event, whereas Manns et al. examined a group of severely amnesic patients that consisted of 2 cardiac arrest patients, 2 heroin overdose patients, 1 carbon monoxide poisoning patient, and 2 patients with unknown etiologies. We also consider an alternative explanation proposed by Wixted and Squire (2004), who argued that the two patient groups suffered similar deficits, but that statistical or methodological artifacts distorted the results of each of Yonelinas et al.'s experiments. A consideration of those results, however, indicates that such an explanation does not account for the existing data. All of the existing evidence indicates that recollection, but not familiarity, is disrupted in mild hypoxic patients. In more severe cases of hypoxia, or those with more complex etiologies such as heroin overdose, more profound deficits may be observed.

The neural substrates of visual implicit memory: do the two hemispheres play different roles?

Identification of visually presented words is facilitated by implicit memory, or visual priming, for past visual experiences with those words. There is disagreement over the neuro-anatomical substrates of this form of implicit memory. Several studies have suggested that this form of priming relies on a visual word-form system localized in the right occipital lobe, whereas other studies have indicated that both hemispheres are equally involved. The discrepancies may be related to the types of priming tasks that have been used because the former studies have relied primarily on word-stem completion tasks and the latter on tasks like word-fragment completion. The present experiments compared word-fragment and word-stem measurements of visual implicit memory in patients with right occipital lobe lesions and patients with complete callosotomies. The patients showed normal visual implicit memory on fragment completion tests, but essentially no visual priming on standard stem completion tests. However, when we used a set of word stems that had only one correct solution for each test item, as was true of the items in the fragment completion tests, the patients showed normal priming effects. The results indicate that visual implicit memory for words is not solely dependent upon the right hemisphere, rather it reflects changes in processing efficiency in bilateral visual regions involved in the initial processing of the items. However, under conditions of high lexical competition (i.e., multiple completion word stems), the lexical processes, which are dominant in the left hemisphere, overshadow the visual priming supported by the left hemisphere.

Form-specific visual priming in the left and right hemispheres.

Word fragment completion performance was examined for items that were presented in the same or different letter case at study and test. During the study phase words and nonwords were presented at central fixation, then during the test phase a divided visual field technique was used in which word fragments were presented briefly to the right hemisphere (left visual field) or the left hemisphere (right visual field). Previous research using the word stem completion task indicated that only the right hemisphere was sensitive to case changes in words from study to test. In contrast, the current results indicate that in the fragment completion task the priming effects for the test items presented to either hemisphere were greater when the fragments were in the same compared to different letter case at study and test. These results indicate that both hemispheres are capable of supporting form-specific visual implicit memory.

The congruency effect: just what is being learned?

G. H. Bower, S. Thompson-Schill, and E. Tulving (1994) found that when stimulus-response sets in A-B, A-C learning belong to unique categories (congruent-triads), learning appropriate responses appear rapid and memory performance on a modified modified free recall (MMFR) test is enhanced. Bower et al. assumed that category cues protect associations from interpair interference, allowing more rapid learning. However, unlike arbitrary pairs, congruent pairs also allow a reliance on preexperimental associations. As a result, MMFR test performance may not be an unbiased test of what was learned. In the present experiment, free recall (FR) demonstrated that responses were learned approximately equally in all conditions and that the pattern of clustering was compatible with the hypothesis that preexperimental associations continue to play a major role in FR test performance.

Theta synchronization during episodic retrieval: neural correlates of conscious awareness.

The neural correlates of conscious awareness during successful memory retrieval were examined. In a recognition test, subjects indicated whether they consciously recalled the event in which a word was earlier presented (Remembering), or whether they recognized it on the basis that it was familiar in the absence of recollection (Knowing). An early EEG synchronization in the theta band predicted knowing, and a later remembering. Moreover, early and late event-related potentials were also found to predict knowing and remembering, respectively. The results indicate that the temporal dynamics of theta synchronization are related to the particular conscious experiences associated with memory retrieval.

Visual implicit memory in the left hemisphere: evidence from patients with callosotomies and right occipital lobe lesions.

Identification of visually presented objects and words is facilitated by implicit memory for past visual experiences with those items. Several behavioral and neuroimaging studies suggest that this form of memory is dependent on perceptual processes localized in the right occipital lobe. We tested this claim by examining implicit memory in patients with extensive right occipital lobe lesions, using lexical-decision mirror-reading, picture-fragment, and word-fragment-completion tests, and found that these patients exhibited normal levels of priming. We also examined implicit memory in patients with complete callosotomies, using standard and divided-visual-field word-fragment-completion procedures, and found that the isolated left hemisphere exhibited normal priming effects. The results indicate that the right occipital lobe does not play a necessary role in visual implicit memory, and that the isolated left hemisphere can support normal levels of visual priming in a variety of tasks.

Hippocampal, parahippocampal and occipital-temporal contributions to associative and item recognition memory: an fMRI study.

The temporal lobe regions involved in memory retrieval were examined using fMRI. During an associative recognition test, participants made memory judgments about the study color of previously presented drawings of objects, and during item recognition tests they made old/new judgments about previously studied objects or new objects. Associative recognition compared with old item recognition led to activations in bilateral hippocampal and parahippocampal regions, as well as in the left middle occipital gyrus. Old item recognition compared with new item recognition led to activation in the left middle occipital gyrus and the left middle temporal gyrus, and relative deactivations in bilateral hippocampal regions. The results indicate that partially distinct temporal lobe regions are involved during recognition memory for item and associative information.

The contribution of recollection and familiarity to yes-no and forced-choice recognition tests in healthy subjects and amnesics.

Recent reports suggest that some amnesic patients perform relatively normally on forced-choice recognition memory tests. Their preserved performance may reflect the fact that the test relies more heavily on assessments of familiarity, a process that is relatively preserved in these patients, than do other recognition tests such as yes-no tests, which may rely more on recollection. The current study examined recognition memory using yes-no and forced-choice procedures in control and amnesic patients in order to determine whether the two tasks differentially relied on recollection and familiarity, and whether the extent of the recognition memory deficit observed in amnesia was dependent upon the type of recognition test used to measure performance. Results using the remember-know procedure with healthy subjects showed that there were no substantial differences in recognition accuracy or in the contribution of recollection to these two tasks. Moreover, amnesic patients were not found to perform better on a forced-choice test than on a yes-no test, suggesting that familiarity contributed equally to these two types of recognition test.

Predicting individual false alarm rates and signal detection theory: a role for remembering.

The relationships between hit, remember, and false alarm rates were examined across individual subjects in three remember-know experiments in order to determine whether signal detection theory would be consistent with the observed data. The experimental data differed from signal detection predictions in two critical ways. First, remember reports were unrelated, or slightly negatively related, to the commission of false alarms. Second, both response types (remembers and false alarms) were uniquely related to hit rates, which demonstrated that the hit rate cannot be viewed as the result of a single underlying strength process. These results are consistent with the dual-process signal detection model of Yonelinas (1994), in which performance is determined by two independent processes--retrieval of categorical context information (remembering) and discriminations based on continuous item strength. Remember and false alarm rates selectively tap these processes, whereas the hit rate is jointly determined. Monte Carlo simulations in which the dual-process model was used successfully reproduced the pattern in the experimental data, whereas simulations in which a signal detection model, with separate "old" and "remember" criteria, was used, did not. The results demonstrate the utility of examining individual differences in response types when one is evaluating memory models.

Memory lost and regained following bilateral hippocampal damage.

We present a longitudinal neuropsychological study (31 examinations over a period of 18 months) of patient DE DF demonstrated bilateral atrophy of the hippocampal formation and globus pallidus resulting from carbon monoxide poisoning. Eighteen months after the event, the volume of the hippocampal formation was reduced by 42% on the left side and 28% on the right. The patient initially presented with a severe global amnesia. Then, he showed a gradual, yet selective recovery of episodic memory function. Verbal free recall and spatial memory performance remained reduced, whereas immediate word recall and recognition memory, as well as picture learning and memory, improved to levels at the lower range of normal performance. Interestingly, nonspatial associative learning was never much impaired and recovered completely by the end of testing. These data are taken as evidence that the human hippocampal formation does not equally support different forms of episodic memory.

Recognition memory for faces: when familiarity supports associative recognition judgments.

Recognition memory for single items can be dissociated from recognition memory for the associations between items. For example, recognition tests for single words produce curvilinear receiver operating characteristics (ROCs), but associative recognition tests for word pairs produce linear ROCs. These dissociations are consistent with dual-process theories of recognition and suggest that associative recognition relies on recollection but that item recognition relies on a combination of recollection and assessments of familiarity. In the present study, we examined associative recognition ROCs for facial stimuli by manipulating the central and external features, in order to determine whether linear ROCs would be observed for stimuli other than arbitrary word pairs. When the faces were presented upright, familiarity estimates were significantly above zero, and the associative ROCs were curvilinear, suggesting that familiarity contributed to associative judgments. However, presenting the faces upside down effectively eliminated the contribution of familiarity to associative recognition, and the ROCs were linear. The results suggest that familiarity can support associative recognition judgments, if the associated components are encoded as a coherent gestalt, as in upright faces.

Confidence-accuracy inversions in scene recognition: a remember-know analysis.

S. E. Clark (1997) offered a modified signal-detection explanation of the confidence-accuracy inversions observed in E. Tulving's (1981) experiments. In addition to replicating E. Tulving (1981), we had participants make "remember-familiar" judgments. Confidence and accuracy dissociated across subjective reports. Response confidence differed only for judgments based on familiarity, whereas accuracy differed only for "remember" responses. S. E. Clark's model does not predict this, nor can it mimic "remember" performance across all conditions. We propose that although "knowing" can be accommodated within an equal variance signal-detection account, "remembering" is governed by contextual constraints that influence the distinctiveness of information upon which participants rely during reports. The current paradigm is a pictorial analogue to H. L. Roediger and K. B. McDermott's paradigm (1995) in that participants claim to explicitly remember thematically related items that were not actually seen during study.

Recollection and familiarity deficits in amnesia: convergence of remember-know, process dissociation, and receiver operating characteristic data.

Previous studies using the process dissociation and the remember-know procedures led to conflicting conclusions regarding the effects of anterograde amnesia on recollection and familiarity. We argue that these apparent contradictions arose because different models were used to interpret the results and because differences in false-alarm rates between groups biased the estimates provided by those models. A reanalysis of those studies with a dual-process signal-detection model that incorporates response bias revealed that amnesia led to a pronounced reduction in recollection and smaller but consistent reduction in familiarity. To test the assumptions of the model and to further assess recognition deficits in amnesics, we examined receiver operating characteristics (ROCs) in amnesics and controls. The ROCs of the controls were curved and asymmetrical, whereas those of the amnesics were curved and symmetrical. The results supported the predictions of the model and indicated that amnesia was associated with deficits in both recollection and familiarity.

Unilateral medial temporal lobe memory impairment: type deficit, function deficit, or both?

Previous research has characterized memory deficits resulting from unilateral hippocampal system damage as 'material specific', suggesting that left damage results in verbal memory impairment with preservation of visuospatial function and the converse with right damage. Implicit within this hypothesis are the assumptions that the systems are independent and memory is lateralized for each type of material. To test the verbal component of this hypothesis, unilateral hippocampal lesion and commissurotomy patients were compared with controls on a multiple-list free-recall task. The material specific hypothesis predicts severe impairment only with left lesions; right lesions and commissurotomy patients should be only minimally impaired. However, secondary memory was compromised at immediate recall for all patient groups, with both unilateral groups showing comparable and severe verbal episodic memory deficits. Final testing across all lists also revealed severe impairment in commissurotomy patients. Finding both unilateral groups to be similarly impaired for verbal material is taken as evidence against a material specific deficit during this verbal episodic memory task. Although previous data suggest that left patients are considerably more impaired during some verbal tasks, this may not be specific to the material, but rather the combination of material and task demands. Implications for the material specific hypothesis are discussed.

Retrieval of old memories: the temporofrontal hypothesis.

Extensive neuropsychological testing is reported on two chronic patients with combined temporopolar and prefrontal damage, dominantly left-hemispheric, and, as control, one chronic patient with bi-hemispheric prefrontal damage. The principal finding is that combined temporofrontal damage, but not substantial prefrontal damage alone, results in marked retrograde memory deficits while leaving intelligence and new learning relatively unimpaired. Although their general world knowledge was good, the temporopolar patients demonstrated retrograde memory impairments on several tests of past events and faces of previously famous people. With respect to retrograde autobiographical memory, one of the temporopolar patients was severely impaired and the other was judged to be moderately impaired. The control patient appeared to be normal. These results, together with corresponding data from related single case and dynamic imaging studies, strongly support a crucial role of the temporofrontal junction area in the ecphory of old memories.

Memory encoding following complete callosotomy.

Three patients with complete resection of the corpus callosum were tested in a series of memory tasks to determine the effects of callosotomy on the encoding and retrieval of information in memory. Verbal and pictorial conjunction tests were administered to measure patients' ability to consolidate the elements of a stimulus into an accurate composite memory. Patients were also tested in a paired-associate learning task to determine the consequences of callosotomy on the encoding and retrieval of associations between stimuli. Although callosotomy patients were unimpaired in the verbal conjunction task, results from both the pictorial conjunction task and the paired-associate learning task suggest that the absence of callosal cross-talk impairs encoding in these patients. In addition, the pattern of results in the paired-associate learning task suggests that callosotomy impairs retrieval processes. The role of the callosum in the formation of memory traces for nonverbal material and associations between verbal stimuli is discussed.

Semantic memory: complexity or connectivity?

The complexity hypothesis predicts that concept-feature verification times should be directly related to the number of features associated with a concept (the fan effect). Conversely, the connectivity hypothesis predicts that for interconnected semantic relationships, this verification time should be inversely related to the number of closely associated features (the reversed fan effect). In the present experiments, although the time required for episodic recognition memory decisions tended to be directly related to the number of features associated with a concept, semantic verification times were inversely related to the complexity of the concept. In addition, the concept's complexity was at least as good a predictor of performance in semantic tasks as was the strength of association between the concept and feature. Both of these results are interpreted in terms of the connectivity hypothesis.

Visual priming effects as a measure of short-term visual memory.

On each trial, subjects classified one of four letters as belonging to one of two categories. Visual priming occurs when the classification response is faster to a stimulus visually identical to a previous stimulus than to one identical only in name. Earlier experiments found no visual priming effects between stimuli separated by a stimulus of the same task but from the opposite classification category. Two of the five conditions in the present experiment varied the stimulus-response (S-R) contingencies in such a way that the penultimate but not the immediately preceding trial had the same contingencies. Only these two conditions gave evidence of the above type of visual priming. Visual priming was found, however, in almost all conditions when the intervening stimulus was from the same task and the same classification category. It is argued that a similarity of S-R contingency, and not simply stimulus similarity, is an important component of the visual priming effect.

Visual memory as measured by classification and comparison tasks.

One measure often used to indicate the existence of visual memory is visual priming, that is, faster responding to a stimulus physically identical to its predecessor than to one identical in name only. Walker and Marshall (1982) used visual priming within speeded classification tasks to demonstrate a visual memory effect that does not seem to require active visualization to prevent decay or to prevent being over-written by succeeding stimuli. This article presents six experiments with classification tasks that not only replicate Walker and Marshall's finding of a strong visual memory in the absence of visualization but also--contrary to their results--show visual priming even after an unpredictable intervening visual pattern. Four additional experiments with comparison tasks show visual priming effects only when stimulus-response contingencies remain consistent. Although this result seems to favor an explanation of the visual priming effect based on stimulus-response contingencies, it does not totally rule out explanations based on stimulus-identification processes, assuming that inconsistent stimulus-response contingencies interfere with the benefits that stimulus repetition may have on stimulus identification.