Impaired memory for scenes but not faces in developmental hippocampal amnesia: a case study

Item recognition for unfamiliar faces and scenes was tested in Jon, who has developmental amnesia resulting from bilateral hippocampal pathology. Performance and confidence judgements in healthy adults showed that both tests were equated for difficulty and had similar receiver operating characteristics (ROCs). Jon's performance on the faces test was indistinguishable from the controls, in both sensitivity and the shape of the ROC curve. In contrast his performance on the scenes test was markedly poor, and his ROC was inconsistent with both a standard dual process (DP; recollection and familiarity) model and an unequal variance signal detection model of recognition memory. Jon's data were as well fitted as controls' data by a DP model that included two recollection parameters, but required counter-intuitive parameter values corresponding to normal recollection and impaired familiarity, which likely reflect an idiosyncratic use of confidence judgements when his memory for the material is weak. The results highlight a limitation in using ROCs to estimate recollection and familiarity in patients who may have developed compensatory strategies for material that they have difficulty remembering (scenes, but not faces in this case). Overall, these data are difficult to reconcile with domain-general accounts of the hippocampal role in memory, including dual process models and the declarative model. Instead, the data indicate that the hippocampus plays a preferential role in the processing of topographical memoranda over faces memoranda.     

An fMRI study on memory discriminability for complex visual scenes

The fan effect represents an increase in reaction time for the recognition of an item as a function of the amount of information associated with that item in memory. The present study used fMRI to study the neural correlates of the fan effect for complex visual scenes. We used a test in which landscape pictures were divided vertically into three equal segments. In the high discriminability condition only one segment was presented during encoding, whereas in the low discriminability condition two different segments from the same picture were presented. During a subsequent forced-choice recognition test, reaction times were significantly faster for the high discriminability condition. Increase in brain activity for the low relative to high discriminability condition was observed in the right prefrontal cortex, several regions of parietal cortex bilaterally, and several late visual processing areas, including the occipito-temporal regions, precuneus, and cuneus. These results support the hypothesis that a region of the prefrontal cortex is involved in the control of memory interference at retrieval elicited by the amount of related information in memory, and further suggests that this involvement is right-lateralized for nonverbal material. The high versus low discriminability contrast showed an increase in activity principally in the bilateral medial temporal gyrus, including the enthorinal cortex/hippocampus and in several bilateral prefrontal cortex regions mostly located in BA 10. These activations were associated with a condition, in which the stimuli were more salient in memory and thus could represent the perceptual salience of items in memory.     

Event-related potentials reveal age differences in the encoding and recognition of scenes

The present study used event-related potentials (ERPs) to investigate how the encoding and recognition of complex scenes change with normal aging. Although functional magnetic resonance imaging (fMRI) studies have identified more drastic age impairments at encoding than at recognition, ERP studies accumulate more evidence for age differences at retrieval. However, stimulus type and paradigm differences across the two literatures have made direct comparisons difficult. Here, we collected young and elderly adults' encoding- and recognition-phase ERPs using the same materials and paradigm as a previous fMRI study [Gutchess, A. H., Welsh, R. C., Hedden, T., Bangert, A., Minear, M., Liu, L., et al. Aging and the neural correlates of successful picture encoding: Frontal activations compensate for decreased medial temporal activity. Journal of Cognitive Neuroscience, 17, 84-96, 2005]. Twenty young and 20 elderly adults incidentally encoded and then recognized photographs of outdoor scenes. During encoding, young adults showed a frontocentral subsequent memory effect, with high-confidence hits exhibiting greater positivity than misses. Elderly adults showed a similar subsequent memory effect, which, however, did not differ as a function of confidence. During recognition, young adults elicited a widespread old/new effect, and high-confidence hits were distinct from both low-confidence hits and false alarms. Elderly adults elicited a smaller and later old/new effect, which was unaffected by confidence, and hits and false alarms were indistinguishable in the waveforms. Consistent with prior ERP work, these results point to important age-related changes in recognition-phase brain activity, even when behavioral measures of memory and confidence pattern similarly across groups. We speculate that memory processes with different time signatures contribute to the apparent differences across encoding and retrieval stages, and across methods.     

Lifespan age differences in working memory: A two-component framework

We suggest that working memory (WM) performance can be conceptualized as the interplay of low-level feature binding processes and top-down control, relating to posterior and frontal brain regions and their interaction in a distributed neural network. We propose that due to age-differential trajectories of posterior and frontal brain regions top-down control processes are not fully mature until young adulthood and show marked decline with advancing age, whereas binding processes are relatively mature in children, but show senescent decline in older adults. A review of the literature spanning from middle childhood to old age shows that binding and top-down control processes undergo profound changes across the lifespan. We illustrate commonalities and dissimilarities between children, younger adults, and older adults reflecting the change in the two components' relative contribution to visual WM performance across the lifespan using results from our own lab. We conclude that an integrated account of visual WM lifespan changes combining research from behavioral neuroscience and cognitive psychology of child development as well as aging research opens avenues to advance our understanding of cognition in general.     

Hemi-field asymmetries in memory for incongruous scenes

The purpose of the present study was to investigate hemispheric asymmetries of long-term semantic memory in normal subjects. A hemi-field reaction time (RT) and accuracy paradigm was used and the test stimuli consisted of pictures, with different semantic organization. Two separate experiments were conducted. In the first, memory for pictures depicting common scenes or incongruous scenes was measured. In the second, we compared memory for incoherent scenes and the same incongruous scenes. The results showed no difference between the visual half-fields in accuracy scores. However, in both experiments the RT results showed that incongruous scenes were recognized consistently faster in the right visual half-field than in the left half-field. In addition, in the first experiment there was no visual field difference for common scenes. In the second experiment, there was a left visual field advantage for unorganized scenes. The results were interpreted to reflect hemispheric asymmetry in long-term semantic memory, in general, and showing a left hemisphere specialization for uncommon, unusual aspects of otherwise regular percepts, in particular. Applying schemata theory to the results, we discussed the possibility that the left hemisphere uses/stores schemata conducive to "flexible" thinking strategies while the right hemisphere uses/stores schemata that involve "rigid" thinking strategies.     

Working memory deficits in adults with ADHD: is there evidence for subtype differences?

Background  

Working memory performance is important for maintaining functioning in cognitive, academic and social activities. Previous research suggests there are prevalent working memory deficits in children with attention deficit hyperactivity disorder (ADHD). There is now a growing body of literature characterizing working memory functioning according to ADHD subtypes in children. The expression of working memory deficits in adults with ADHD and how they vary according to subtype, however, remains to be more fully documented.     

Italian neuropsychological instruments to assess memory,attention and frontal functions for developmental age

Abstract In this study, a series of tests exploring long-term verbal memory (the Short Story Test), attention (a modified version of Attentional Matrices and the Trail Making Test) and frontal functions (a modified version of the Frontal Assessment Battery) have been standardised on an Italian population of 283 children aged 5–14. Raw scores for each test have been adjusted for a series of variables (child's age, years of parents' education, handedness, gender) and transformed in equivalent scores enabling direct comparison across measures. This study was promoted by LICE (the Italian League Against Epilepsy) in order to provide Italian instruments standardised on the developmental age population and to study some of the most frequently impaired cognitive functions in epilepsy.     

Cultural differences in categorical memory errors persist with age

Objectives: This cross-sectional experiment examined the influence of aging on cross-cultural differences in memory errors. Previous research revealed that Americans committed more categorical memory errors than Turks; we tested whether the cognitive constraints associated with aging impacted the pattern of memory errors across cultures. Furthermore, older adults are vulnerable to memory errors for semantically-related information, and we assessed whether this tendency occurs across cultures.

Methods: Younger and older adults from the US and Turkey studied word pairs, with some pairs sharing a categorical relationship and some unrelated. Participants then completed a cued recall test, generating the word that was paired with the first. These responses were scored for correct responses or different types of errors, including categorical and semantic.

Results: The tendency for Americans to commit more categorical memory errors emerged for both younger and older adults. In addition, older adults across cultures committed more memory errors, and these were for semantically-related information (including both categorical and other types of semantic errors).

Conclusion: Heightened vulnerability to memory errors with age extends across cultural groups, and Americans’ proneness to commit categorical memory errors occurs across ages. The findings indicate some robustness in the ways that age and culture influence memory errors.     

Working memory performance in poor outcome schizophrenia: relationship to age and executive functioning

Performance on the Letter-Number Sequencing (LNS) and Wisconsin Card Sorting Tests (WCST) have been shown to be significantly correlated in patients with schizophrenia, a relationship postulated to be due to working memory demands of the two tests (Gold, Carpenter, Randolph, Goldberg, & Weinberger, 1997). An alternative explanation for the association between these two tests is their sorting demands, in that both require sorting of information albeit in slightly different ways. If the latter explanation is valid, then working memory tasks that do not require sorting or other conceptualization demands should be less predictive of WCST performance than LNS. These hypotheses were examined in 34 poor outcome patients with schizophrenia, one-half of whom were over the age of 65. Patients were evaluated on Digit Span Forward, spatial working memory, LNS, and the WCST. It was found that WCST performance was significantly associated with performance on the LNS but no other working memory task. Age related performance differences were greatest on the WCST Categories and floor effects were noted on this test in one-half of the subjects. Analyses predicting WCST Categories in subjects whose scores were greater than zero (n = 16) also demonstrated that LNS, but not Digit Span or spatial working memory (any delay) predicted WCST performance. These findings indicate that LNS may be an index of executive functioning, particularly in patients who cannot perform the WCST.     

Reduced somatosensory activations in swallowing with age

Understanding the neural functional organization of swallowing in healthy elders is essential in diagnosing and treating older adults with swallowing difficulties. The primary aims of this investigation were to identify the neural activation sites of different components of deglutition in healthy elders using functional Magnetic Resonance Imaging (fMRI) and to investigate age differences in the neural control of swallowing. Ten young (age range 19-25 years of age) and nine older (age range 66-77 years of age) right-handed healthy individuals were scanned in a 3-Tesla MRI scanner. Subjects were visually cued for both a "Swallow" task and for component/control tasks ("Prepare to swallow," "Tap your tongue," and "Clear your throat"). Behavioral interleaved gradient (BIG) methodology was used to address movement related artifacts. Between-group comparisons revealed statistically stronger activations in the primary somatosensory cortex of young adults during the motor tasks examined. Both groups showed activations in the major motor areas involved in the initiation and execution of movement; however, areas involved in sensory processing, sensorimotor integration and/or motor coordination and control, showed reduced or limited activity in the elderly. Potential implications of these findings for clinical practice are discussed.     

Decline in verbal memory performance with advancing age: the role of frontal lobe functioning

This study investigated the relationship between measures of frontal lobe functioning (FLF) and verbal memory performance among healthy, community-dwelling older adults (60-85 years old). All were administered measures of FLF, attention, verbal memory, and depression. After controlling for the effects of attention and depression, FLF accounted for significant amounts of the variance in verbal memory scores. Age related to the FLF measure according to the level of organization of verbal material to be recalled. Frontal lobe functioning and performance on an attention measure explained the greatest amount of the variance in the recall of unorganized verbal material, whereas age and attention abilities were the best predictors of the recall of organized verbal material. The data indicate a central role of frontal dysfunction in understanding age-related memory loss.     

Common prefrontal activations during working memory,episodic memory,and semantic memory

Regions of the prefrontal cortex (PFC) are typically activated in many different cognitive functions. In most studies, the focus has been on the role of specific PFC regions in specific cognitive domains, but more recently similarities in PFC activations across cognitive domains have been stressed. Such similarities may suggest that a region mediates a common function across a variety of cognitive tasks. In this study, we compared the activation patterns associated with tests of working memory, semantic memory and episodic memory. The results converged on a general involvement of four regions across memory tests. These were located in left frontopolar cortex, left mid-ventrolateral PFC, left mid-dorsolateral PFC and dorsal anterior cingulate cortex. These findings provide evidence that some PFC regions are engaged during many different memory tests. The findings are discussed in relation to theories about the functional contribution of the PFC regions and the architecture of memory.     

Recall and recognition memory in amnesia: patients with hippocampal, medial temporal, temporal lobe or frontal pathology

The relationship between recall and recognition memory impairments was examined in memory-disordered patients with either hippocampal, medial temporal, more widespread temporal lobe or frontal pathology. The Hirst [Hirst, W., Johnson, M. K., Phelps, E. A., & Volpe, B. T. (1988). More on recognition and recall in amnesics. Journal of Experimental Psychology: Learning, Memory, & Cognition, 14, 758-762] technique for titrating exposure times was used to match recognition memory performance as closely as possible before comparing recall memory scores. Data were available from two different control groups given differing exposure times. Each of the patient groups showed poorer recall memory performance than recognition scores, proportionate to the difference seen in healthy participants. When patients' scores were converted to Z-scores, there was no significant difference between mean Z-recall and Z-recognition scores. When plotted on a scatterplot, the majority of the data-points indicating disproportionately low recall memory scores came from healthy controls or patients with pathology extending into the lateral temporal lobes, rather than from patients with pathology confined to the medial temporal lobes. Patients with atrophy extending into the parahippocampal gyrus (H+) performed worse than patients with atrophy confined to the hippocampi (H-); but, when H- patients were given a shorter exposure time (5s) and compared with H+ at a longer exposure (10s), their performance was virtually identical and did not indicate any disproportionate recall memory impairment in the H- group. Parahippocampal volumes on MRI correlated significantly with both recall and recognition memory. The possibility that findings were confounded by inter-stimulus artefacts was examined and rejected. These findings argue against the view that hippocampal amnesia or memory disorders in general are typically characterised by a disproportionate impairment in recall memory. Disproportionate recall memory impairment has been observed in a number of published cases, and the reason for the varying pattern obtained across hippocampal patients requires further examination.     

Age differences in the frontal lateralization of verbal and spatial working memory revealed by PET

Age-related decline in working memory figures prominently in theories of cognitive aging. However, the effects of aging on the neural substrate of working memory are largely unknown. Positron emission tomography (PET) was used to investigate verbal and spatial short-term storage (3 sec) in older and younger adults. Previous investigations with younger subjects performing these same tasks have revealed asymmetries in the lateral organization of verbal and spatial working memory. Using volume of interest (VOI) analyses that specifically compared activation at sites identified with working memory to their homologous twin in the opposite hemisphere, we show pronounced age differences in this organization, particularly in the frontal lobes: In younger adults, activation is predominantly left lateralized for verbal working memory, and right lateralized for spatial working memory, whereas older adults show a global pattern of anterior bilateral activation for both types of memory. Analyses of frontal subregions indicate that several underlying patterns contribute to global bilaterality in older adults: most notably, bilateral activation in areas associated with rehearsal, and paradoxical laterality in dorsolateral prefrontal sites (DLPFC; greater left activation for spatial and greater right activation for verbal). We consider several mechanisms that could account for these age differences including the possibility that bilateral activation reflects recruitment to compensate for neural decline.     

Aging and the neural correlates of successful picture encoding: frontal activations compensate for decreased medial-temporal activity

We investigated the hypothesis that increased prefrontal activations in older adults are compensatory for decreases in medial-temporal activations that occur with age. Because scene encoding engages both hippocampal and prefrontal sites, we examined incidental encoding of scenes by 14 young and 13 older adults in a subsequent memory paradigm using functional magnetic resonance imaging (fMRI). Behavioral results indicated that there were equivalent numbers of remembered and forgotten items, which did not vary as a function of age. In an fMRI analysis subtracting forgotten items from remembered items, younger and older adults both activated inferior frontal and lateral occipital regions bilaterally; however, older adults showed less activation than young adults in the left and right parahippocampus and more activation than young adults in the middle frontal cortex. Moreover, correlations between inferior frontal and parahippocampal activity were significantly negative for old but not young, suggesting that those older adults who showed the least engagement of the parahippocampus activated inferior frontal areas the most. Because the analyses included only the unique activations associated with remembered items, these data suggest that prefrontal regions could serve a compensatory role for declines in medial-temporal activations with age.     

Neural correlates of recognition memory for emotional faces and scenes

We examined the influence of emotional valence and type of item to be remembered on brain activity during recognition, using faces and scenes. We used multivariate analyses of event-related fMRI data to identify whole-brain patterns, or networks of activity. Participants demonstrated better recognition for scenes vs faces and for negative vs neutral and positive items. Activity was increased in extrastriate cortex and inferior frontal gyri for emotional scenes, relative to neutral scenes and all face types. Increased activity in these regions also was seen for negative faces relative to positive faces. Correct recognition of negative faces and scenes (hits vs correct rejections) was associated with increased activity in amygdala, hippocampus, extrastriate, frontal and parietal cortices. Activity specific to correctly recognized emotional faces, but not scenes, was found in sensorimotor areas and rostral prefrontal cortex. These results suggest that emotional valence and type of visual stimulus both modulate brain activity at recognition, and influence multiple networks mediating visual, memory and emotion processing. The contextual information in emotional scenes may facilitate memory via additional visual processing, whereas memory for emotional faces may rely more on cognitive control mediated by rostrolateral prefrontal regions.     

Adult age differences in the functional neuroanatomy of verbal recognition memory

Adult age differences are frequently observed in the performance of memory tasks, but the changes in neural function mediating these differences are largely unknown. We used H₂¹⁵O positron emission tomography (PET) to measure changes in regional cerebral blood flow (rCBF) during Encoding, Baseline, and Retrieval conditions of a recognition memory task. Twelve young adults (20–29 years) and 12 older adults (62–79 years) participated. During each task condition, participants made a two‐choice manual response to each of 64 words. Analyses of the performance data yielded evidence of age‐related slowing of encoding and retrieval processes, and an age‐related decline in the accuracy of yes/no recognition (d'). The rCBF activation associated with both encoding and retrieval was greater for older adults than for young adults, but this pattern was more clearly evident for memory retrieval. For young adults, rCBF activation during retrieval occurred primarily in right prefrontal cortex, whereas older adults exhibited a more bilateral pattern of prefrontal activation. Regression analyses predicting reaction time in the memory task from regional PET counts confirmed that the neural system mediating memory retrieval is more widely distributed for older adults than for young adults. Both age groups exhibited some decrease in rCBF activation in the second half of the test session, relative to the first half. The practice‐related decrease in rCBF activation was more prominent for young adults, suggesting that the older adults' recruitment of additional neural systems reflects a more continual allocation of attention to support task performance. Hum. Brain Mapping 7:115–135, 1999. © 1999 Wiley‐Liss, Inc.     

Working memory and schizophrenia: evidence for slowed encoding

Previous studies have found impairments in working memory in individuals with schizophrenia, but have not identified the underlying information processing deficit. Because schizophrenia is associated with slowed cognitive processing, deficits on working memory tests may be due to decreased speed of encoding rather than an inability to maintain information over time. This hypothesis was examined using a Delayed Match to Sample (DMTS) Test. Task difficulty under 0-delay conditions was equated by individually establishing the stimulus presentation time needed to reach approximately 80% accuracy. Schizophrenia participants required longer presentation durations, but there were no group differences under delay conditions when performance was equated in the 0-delay condition. These results suggest that poor working memory performance in schizophrenia results from slowed encoding processes.     

Event-related nociceptive arousal enhances memory consolidation for neutral scenes

The superior memory for emotional events has been attributed to the beneficial effects of noradrenaline released into the amygdala attributable to arousal. Noradrenaline mediates the effects of different hormones and neurotransmitters, including adrenal stress hormones on consolidation (McGaugh, 2004; Roozendaal et al., 2009). The majority of human fMRI studies of the enhancement of emotional memories contrasted successful encoding of emotionally arousing and neutral stimuli (LaBar and Cabeza, 2006; Murty et al., 2010). Recently, it was highlighted that emotional stimuli elicit not only arousal but also intensify cognitive processes that contribute to the enhanced memory. In particular, the enhanced use of selective attention as well as the greater distinctiveness and semantic relatedness of emotional stimuli influence memory formation (Talmi et al., 2007a). The present study aimed to explore the effects of arousal on memory formation independent of these cognitive factors in an event-related manner. Arousal was induced by the application of a nociceptive stimulus briefly after the presentation of neutral scenes. The results show a purely arousal-driven memory enhancement for the neutral scenes that differs in critical aspects from the superior memory for emotional stimuli. In particular, the enhancement was only evident after consolidation and exclusively based on an increase in item familiarity but not recollection. Moreover, successful memory formation for stimuli followed by arousal was correlated with activity in the parahippocampal cortex but not the amygdala, as is the case for emotional stimuli.