Memory in autism: review and synthesis

Much research about memory in autism concerns the hypothesis that autism is similar to adult-onset amnesia. Initial support for the hypothesis came from post-mortem studies of individuals with autism showing abnormalities in the hippocampus and related brain structures, as well as behavioral studies finding contrasts between intact cued recall and impaired free recall and recognition in autism. The hypothesis was later brought into question by the finding of intact performance in individuals with autism on explicit memory tasks typically impaired in adult-onset amnesia. The present paper proposes a possible reconciliation of these contradictory findings, suggesting that there is selective damage to the limbic-prefrontal episodic memory system, sparing the limbic-only perceptual representation system, and the semantic memory system. This view is consistent with other evidence for early selective damage to other systems involving cooperation between the limbic system and the medial prefrontal cortex in autism.     

A case of amnesia at an early age

A dissociation between short- and long-term memory (LTM) and between the episodic and the semantic component of LTM is reported in a young girl who became amnesic at the age of 6 after an episode of acute encephalopathy resulting in bilateral frontal, insular, thalamic, ponto-mesencephalic, hippocampal and temporal lesions, as documented by MRI. The girl became amnesic a few months after starting school. A follow-up investigation showed that she was able to learn to read, write and acquire number facts and procedures and to improve her semantic knowledge. Our results show that the features of adult amnesia can also be found in children and that new semantic knowledge can be acquired in spite of an anterograde memory deficit. This dissociation does not agree with theories viewing long- term declarative memory as a unitary process mediated by the hippocampal system, but supports recent hypotheses that the acquisition of semantic knowledge is independent from episodic memory processes, and takes place through spared cortical regions subjacent to the hippocampi (Vargha-Khadem et al., 1997).     

“I remember it as if it were yesterday”: Memory for recent events in patients with semantic dementia

Patients with semantic dementia (SD), who have an incontrovertible deficit in semantic memory, are reported to show good day-to-day memory for recent events; but experimental evidence on their anterograde episodic memory/new learning is somewhat sparse and does not always tell a consistent story. We describe the performance of five SD patients, relative to controls, on (a) a range of semantic memory measures that predictably revealed substantial impairment, and (b) a newly designed naturalistic and incidental episodic task, which included information regarding the items and context of the semantic tasks. As a group, the patients’ episodic memory for these natural events was good, even after a 24-h delay, although case-by-case analysis revealed some heterogeneity in performance. These findings are discussed with regard to the neural substrate of episodic memory and psychological models of long-term memory.     

Deeper processing is beneficial during episodic memory encoding for adults with Williams syndrome

Previous research exploring declarative memory in Williams syndrome (WS) has revealed impairment in the processing of episodic information accompanied by a relative strength in semantic ability. The aim of the current study was to extend this literature by examining how relatively spared semantic memory may support episodic remembering. Using a level of processing paradigm, older adults with WS (aged 35–61 years) were compared to typical adults of the same chronological age and typically developing children matched for verbal ability. In the study phase, pictures were encoded using either a deep (decide if a picture belongs to a particular category) or shallow (perceptual based processing) memory strategy. Behavioural indices (reaction time and accuracy) at retrieval were suggestive of an overall difficulty in episodic memory for WS adults. Interestingly, however, semantic support was evident with a greater recall of items encoded with deep compared to shallow processing, indicative of an ability to employ semantic encoding strategies to maximise the strength of the memory trace created. Unlike individuals with autism who find semantic elaboration strategies problematic, the pattern of findings reported here suggests in those domains that are relatively impaired in WS, support can be recruited from relatively spared cognitive processes.     

Exploring the roles of the executive and short-term feature-binding functions in retrieval of retrograde autobiographical memories in severe traumatic brain injury

Conway’s autobiographical memory (AM) model postulates that memories are not stored in a crystallised form in long-term memory but are reconstructed at time of retrieval via executive and binding processes, to create a temporary multimodal representation from different AM knowledge. Traumatic brain injury (TBI) impairs AM recollection. However, no study has yet considered the distinct roles of executive and short-term feature-binding functions in the retrieval deficits of retrograde AMs after TBI. Examining a group of 33 TBI patients and 33 controls, our study addresses these roles through a first-ever exploration of the links between performance on an AM verbal fluency evaluation that distinguishes four levels of representation, from semantic to episodic (lifetime periods, general events, specific events, specific details of a specific event), and three executive functions (shifting, inhibition and updating) and two short-term feature-binding functions (short-term formation and maintenance of multimodal representations). The results showed that TBI patients were impaired compared to controls in the retrieval of both semantic and episodic retrograde AM representations, but especially for the most episodic level of AM, in the three executive functions and the short-term maintenance of multimodal representations. Regression analyses indicated that the executive predictors (mainly updating) mediated a large proportion (over 70%) of TBI-related deficit on the retrieval of lifetime periods, general events and specific events, in contrast with the main impairment on generation of specific details which were only mildly (just 12%) predicted by the short-term maintenance of multimodal representations. Additional analyses in a subgroup of patients point to episodic memory abilities and time since injury in predicting the retrieval of specific events and details. In summary, the present study mainly emphasizes that the executive deficits in TBI are involved in the disruption of the first levels of AM generative processes that give access to the multiple episodic details recollection.     

Episodic and Semantic Autobiographical Memory in Adults with Autism Spectrum Disorders

Episodic and semantic autobiographical memories were examined in a group of adults with autism spectrum disorders (ASD) and a control group matched for age, gender and IQ. Results demonstrated a personal episodic memory deficit in the ASD group in the absence of a personal semantic memory deficit, suggesting a deficit dissociation between these two components of memory in ASD. Further analysis of memories across different lifetime periods revealed the adolescent and early adult lifetime periods to facilitate memory recall in the control group, but not in the ASD group. These findings suggest a distinctive pattern of remembering in ASD.     

Acquired amnesia in childhood: a single case study

We report the case of C.L., an 8-year-old child who, following the surgical removal of an ependymoma from the left cerebral ventricle at the age of 4 years, developed significant difficulties in retaining day-to-day events and information. A thorough neuropsychological analysis documented in C.L. a severe anterograde amnesic syndrome, characterised by normal short-term memory, but poor performance on episodic long-term memory tests. In particular, C.L. demonstrated virtually no ability to recollect new verbal information several minutes after the presentation. As for semantic memory, C.L. demonstrated general semantic competencies, which, depending on the test, ranged from the level of a 6-year-old girl to a level corresponding to her actual chronological age. Finding a patient who, despite being severely impaired in the ability to recollect new episodic memories, still demonstrates at least partially preserved abilities to acquire new semantic knowledge suggests that neural circuits implicated in the memorisation of autobiographical events and factual information do not overlap completely. This case is examined in the light of growing literature concerned with the dissociation between episodic and semantic memory in childhood amnesia.     

Insights from semantic dementia on the relationship between episodic and semantic memory

An influential theory of long-term memory, in which new episodic learning is dependent upon the integrity of semantic memory, predicts that a double dissociation between episodic and semantic memory is not possible in new learning. Contrary to this view, we found, in two separate experiments, that patients with impaired semantic memory showed relatively preserved performance on tests of recognition memory if the stimuli were perceptually identical between learning and test. A significant effect of semantic memory was only seen when a perceptual manipulation was introduced in the episodic task. To account for these findings, we propose a revision to current models of long-term memory, in which sensory/perceptual information and semantic memory work in concert to support new learning.     

Spatial deficits in an amnesic patient with hippocampal damage: questioning the multiple trace theory

Mediotemporal lobe structures are involved in both spatial processing and long-term memory. Patient M.R. suffers from amnesia, due to bilateral hippocampal lesion and temporoparietal atrophy following carbon monoxide poisoning. We compared his performance in immediate spatial memory tasks with the performance of ten healthy matched participants. Using an immediate reproduction of path, we observed a dissociation between his performance in three allocentric tasks and in five egocentric-updating tasks. His performance was always impaired on tasks requiring the use of an egocentric-updating representation but remained preserved on allocentric tasks. These results fit with the hypothesis that the hippocampus plays a role in spatial memory, but they also suggest that allocentric deficits previously observed in amnesia might actually reflect deficits in egocentric-updating processes. Furthermore, the co-occurrence of deficits in episodic long-term memory and short-term egocentric-updating representation without any short-term allocentric deficit suggests a new link between the mnemonic and navigational roles of the hippocampus. The Cognitive Map theory, the Multiple Trace theory, as well as further models linking spatial and nonspatial functions of the hippocampus are discussed.     

The perceptual richness of complex memory episodes is compromised by medial temporal lobe damage

Perceptual richness, a defining feature of episodic memory, emerges from the reliving of multimodal sensory experiences. Although the importance of the medial temporal lobe (MTL) to episodic memory retrieval is well documented, the features that determine its engagement are not well characterized. The current study assessed the relationship between MTL function and episodic memory's perceptual richness. We designed a laboratory memory task meant to capture the complexity of memory for life episodes, while manipulating memory's perceptual content. Participants encoded laboratory episodes with rich (film clips) and impoverished (written narratives) perceptual content that were matched for other characteristics such as personal significance, emotionality and story content. At retrieval, participants were probed to describe the stories' perceptual features and storyline. Participants also recalled autobiographical memories (AMs) in a comparison condition. We compared the performance of patients with unilateral medial temporal lobe epilepsy (mTLE) and healthy controls to assess how damage to the MTL affects retrieval in these conditions. We observed an overall decrease in detail count in the mTLE group, along with a disproportionate deficit in perceptual details that was most acute in the AM and the perceptually enriched film clip conditions. Our results suggest that the impaired sense of reliving the past that accompanies MTL insult is mediated by a paucity of perceptual episodic memory details. We also introduce a new protocol that successfully mimics naturalistic memories while benefiting from the experimental control provided by using laboratory stimuli. © 2014 Wiley Periodicals, Inc.     

Episodic, semantic and procedural memory in a case of amnesia at an early age

The patient C.C. developed an amnesic syndrome at the age of 10 yr. Like adult amnesics, C.C. demonstrated impaired episodic memory for both verbal and visual materials although immediate memory span was spared. However, striking deficits were also observed on a wide variety of semantic memory tasks, including reading vocabulary and verbal fluency tests, semantic classification and lexical decision tasks and tests of verbal intelligence. On the other hand, C.C. showed normal learning and retention of two procedural tasks. It was argued that this evidence is inconsistent with the view that the amnesic syndrome represents a selective defect of episodic memory that leaves semantic memory relatively unaffected.     

Are faces special in Alzheimer's disease? Cognitive conceptualisation, neural correlates, and diagnostic relevance of impaired memory for faces and names

Memory for faces and names has increasingly become a focus of cognitive assessment and research in Alzheimer's disease (AD). This paper reviews evidence from cognitive and clinical neuroscience regarding the question of whether AD is associated with a specific deficit in face recognition, face-name association, and retrieval of semantic information and names. Cognitive approaches conceptualizing face recognition and face-name association have revealed that, compared to other types of visual stimuli, faces are "special" because of their complexity and high intraclass similarity, and because their association with proper names is arbitrary and unique. Neuroimaging has revealed that due to this particular status, face perception requires a complex interplay of highly specialized secondary visual areas located in the occipitotemporal cortex with a widely distributed system of cortical areas subserving further task-dependent processing. Our review of clinical research suggests that AD-related deficits in face recognition are primarily due to mnestic rather than perceptual deficits. Memory for previously studied or famous faces is closely related to mediotemporal and temporocortical brain regions subserving episodic and semantic memory in general, suggesting that AD-related impairments in this domain are due to neural degeneration in these areas. Despite limited specificity due to the apparent absence of a "genuine" domain-specific deficit of face memory in AD, testing memory for faces and names is useful in clinical contexts, as it provides highly sensitive indices of episodic and semantic memory performance. Therefore, clinical assessment of face memory can usefully contribute to early detection of memory deficits in prodromal and initial stages of AD, and represents a basis for further attempts at rehabilitation. Further advantages, such as ecological validity, high task comprehensibility and, in the case of novel face learning, independence from premorbid intelligence level, render measures of face recognition valuable for clinical assessment in early AD.     

Verbal, visual, and spatio-sequential short-term memory: assessment of the storage capacities of children and teenagers with Down's syndrome

Background   It is recognized that individuals with Down's syndrome have a specific deficit in verbal short-term memory. On the other hand, non-verbal short-term memory seems to be preserved or even be a strong point for these persons. Nevertheless, the extent and specificity of the deficit must be determined. To do so, we carried out a research programme that allowed us to simultaneously assess various short-term memory systems in a developmental perspective, and to compare our participants' performance to that obtained by typically developing individuals of the same mental age.
Method   Three span tasks are used (auditory word span/visual patterns test/Corsi blocks task) with 54 children and teenagers with Down's syndrome and 54 typically developing children as control group. Participants were matched according to their cognitive level.
Results   For the auditory word span task, participants with Down's syndrome obtained performances significantly lower than those of the typically developing participants. On the other hand, compared with typically developing children, children and teenagers with Down's syndrome have a spatio-sequential span significantly higher for the lowest developmental ages. No significant differences were found for visual span.
Conclusions   Individuals with Down's syndrome exhibited a distinctive pattern of memory performance, in addition to their developmental specificities.     

Reduced specificity of autobiographical memory and aging: Do the executive and feature binding functions of working memory have a role?

Autobiographical memory (AM) is built up from various kinds of knowledge, from general to specific, via generative processes. Aging seems to particularly affect the episodic autobiographical information while preserving information that is more semantic. However, the mechanism of this deficit has not yet been thoroughly tested in relation to working memory. This study is designed to investigate, in a group of 100 subjects, the relationships between age, accessibility to different levels of AM specificity, and two main components of working memory: the central executive and the episodic buffer. We used a new task composed of four embedded verbal autobiographical fluencies (VAF) - from low to highest specificity levels - exploring lifetime periods, general events, specific events, and details, plus tasks exploring free recall of episodic AM and updating, shifting, inhibition, and feature binding in working memory. The results demonstrate that age-related difficulties increase with level of specificity of autobiographical knowledge, i.e., from semantic to episodic aspects. Moreover, regression analyses mainly show that increase in age-related deficit with level of specificity of AM is largely mediated by performance on executive functions (updating and inhibition) and to a lesser extent feature binding in working memory. The results confirm in episodic AM the executive/working memory aging hypothesis, and for the first time highlight the role of episodic buffer in associating the various different details of specific events that elicit the conscious recollection.     

Episodic, but not semantic, autobiographical memory is reduced in amnestic mild cognitive impairment

Amnestic mild cognitive impairment (aMCI) is characterized by decline in anterograde memory as measured by the ability to learn and remember new information. We investigated whether retrograde memory for autobiographical information was affected by aMCI. Eighteen control (age 66-84 years) and 17 aMCI (age 66-84 years) participants described a personal event from each of the five periods across the lifespan. These events were transcribed and scored according to procedures that separate episodic (specific happenings) from semantic (general knowledge) elements of autobiographical memory. Although both groups generated protocols of similar length, the composition of autobiographical recall differentiated the groups. The aMCI group protocols were characterized by reduced episodic and increased semantic information relative to the control group. Both groups showed a similar pattern of recall across time periods, with no evidence that the aMCI group had more difficulty recalling recent, rather than remote, life events. These results indicate that episodic and semantic autobiographical memories are differentially affected by the early brain changes associated with aMCI. Reduced autobiographical episodic memories in aMCI may be the result of medial temporal lobe dysfunction, consistent with multiple trace theory, or alternatively, could be related to dysfunction of a wider related network of neocortical structures. In contrast, the preservation of autobiographical semantic memories in aMCI suggests neural systems, such as lateral temporal cortex, that support these memories, may remain relatively intact.     

The influence of semantic encoding on recognition memory in Alzheimer''s disease

Within the framework of the distinction between episodic and semantic memory, it has been argued that these two memory systems are organised in a hierarchical way. The hierarchical hypothesis assumes that episodic memory is a specific subsystem of semantic memory and therefore implies that episodic memory cannot exist without semantic memory. If this hypothesis is correct, it should be expected that patients with impaired semantic memory also have impaired episodic memory. In the present study, two experiments investigated the influence of semantic encoding on recognition memory performance in a population of 20 patients with Alzheimer's disease and 18 normal controls. Both experiments assessed recognition memory for semantically-related items. In Experiment 2, but not in Experiment 1, subjects were explicitly instructed to make a semantic association between the items. Alzheimer's disease patients were impaired, compared to the normal controls, on the recognition memory performance of both experiments. The ability to make a semantic association between two items was significantly and positively correlated with the subjects' performance on the recognition tasks. A further analysis showed that patients who were impaired on the semantic association task did significantly worse on the recognition task of Experiment 2 than normal controls and patients who were unimpaired on the semantic association task. These findings are discussed in the context of memory deficits in Alzheimer's disease, and are interpreted as supporting the view that episodic memory for an item is affected by the level of semantic awareness of that same item.     

Relationship of Age at Onset, Chronologic Age, and Adequacy of Preoperative Performance to Verbal Memory Change After Anterior Temporal Lobectomy

Summary We examined the relationship of age of onset of epilepsy, chronological age at time of operation, and adequacy of preoperative memory performance to pre- to postoperative verbal memory decline. Patients who underwent left (n = 50) or right (n = 51) anterior temporal lobectomy (ATL) were administered tests of verbal episodic (list learning, paragraph recall) and semantic memory (visual naming, vocabulary), both preoperatively and 6 months postoperatively. As a group, left ATL patients showed the classic selective decrease on measures of episodic but not semantic memory. However, examination of episodic memory outcome showed considerable individual variability. Stepwise regression analyses indicated that both later age at onset and older chronologic age were significant and selective predictors of episodic memory decrease for left ATL patients. Adequacy of preoperative memory performance was a nonspecific predictor, associated with decrease in postoperative memory performance for both left and right ATL patients and for multiple types of memory indices. The clinical and theoretical implications are discussed.     

Nature of personal semantic memory: evidence from Alzheimer's disease

Personal semantic memory is factual knowledge about a person's own past. Although personal semantic memory is assumed to have features of both semantic memory and episodic memory, the relationship to episodic memory and to semantic memory have not been well documented. In patients with Alzheimer's disease, episodic memory, semantic memory, and personal semantic memory are all defective. In this study, the hypothesis that defective personal semantic memory is related to both semantic and episodic memory dysfunction was tested in patients with Alzheimer's disease. Functions of episodic, semantic, and personal semantic memory were examined by using the Wechsler Memory Scale-Revised (WMS-R), subtests of the WAIS-R (Information, Vocabulary, Comprehension and Similarities), and the Family Line Test (FLT) in 62 patients who met the NINCDS/ADRDA criteria for probable Alzheimer's disease. Specific effects of episodic and semantic memory on personal semantic memory were examined by using multiple linear regression analysis with the total score of the FLT as the dependent variable and the WMS-R Delayed Recall weighted sum score and the WAIS-R Semantic Memory score (a composite of standardized scores of the four subtests) as the independent variables. Personal semantic memory function was significantly correlated with both the episodic and semantic memory functions, after controlling age, sex, educational attainment, and severity of dementia. This result supports the hypotheses that personal semantic memory has features of both episodic and semantic memory, and that semantic memory is transformed from episodic memory.     

How do Korsakoff patients learn new concepts?

The goal of the present investigation was to assess semantic learning in Korsakoff patients (KS), compared with uncomplicated alcoholics (AL) and control subjects (CS), taking the nature of the information to-be-learned and the episodic memory profiles of the three groups into account.Ten new complex concepts, each illustrated by a photo and composed of a label, a category and three features, were taught to 13 KS, 23 AL and 45 CS. When examined independently of the main experimental task, the two patients’ groups presented episodic memory, working memory and executive impairments but episodic memory was more severely impaired in KS.Both AL and KS exhibited label learning deficits but KS were more severely impaired than AL. The episodic memory results were the main factor accounting for label learning performance when the three groups were pooled together. When examined within each group, the correlation was significant in CS and AL but not in KS. Only KS exhibited impaired category and feature learning results. Episodic memory did not account for category and feature learning performance.New label learning may be equivalent to that of proper names, requiring the involvement of episodic memory notably to arbitrarily associate a meaningless word with a specific identity. However, when episodic memory is severely impaired like in KS, an alternative neocortical learning route, bypassing episodic memory, may be invoked. Category and feature seem to be acquired independently of episodic memory. The specific impairment in category and feature learning in KS may therefore reflect a genuine deficit of semantic memory in Korsakoff's syndrome.