Multidimensional assessment of social cognition using non-immersive virtual reality in dementia with Lewy bodies and Alzheimer's disease: an exploratory study.

INTRODUCTION: Few studies have focused on social cognition in dementia with Lewy bodies (DLB), even though some brain structures being well known as underlying social cognitive processes are directly impacted in this disease. Furthermore, social cognition processes have been mostly studied independently using evaluations with poor ecological validity. We aimed at studying the ability of a new naturalistic and multidimensional social cognition task to reveal impairments in DLB patients. We chose to compare the profile of these patients with that of Alzheimer's disease (AD) patients, for which social cognition is better preserved. METHOD: Fifteen patients (DLB: n = 7; AD: n = 8) and 28 healthy controls underwent the REALSoCog task. They encountered several social situations (e.g. control versus transgressions) in a non-immersive virtual city environment allowing the assessment of moral cognition, cognitive and affective theory of mind (ToM), emotional empathy and behavioral intentions. RESULTS: The main results showed (i) a lower ability to detect transgressions in DLB patients, particularly conventional ones, whereas moral cognition seemed better preserved in AD patients; (ii) a cognitive ToM impairment in both DLB and AD patients, while affective ToM is impaired only in DLB patients; (iii) a decreased emotional empathy specifically observed in DLB patients; (iv) more inappropriate behavioral intentions, mainly in DLB patients, but also in some AD patients. CONCLUSIONS: This study suggests the feasibility and potential interest of the REALSoCog task in revealing social cognition deficits, particularly for DLB patients by showing different social patterns as compared to AD patients. These results offer interesting clinical perspectives to develop more naturalistic tasks in such populations and for clinical differential diagnosis. Limitations and future perspectives are discussed.

Considering spatial ability in virtual route learning in early aging.

The aim of this study is to broaden our understanding of the construction and early decline of spatial mental representations in route learning, considering the extent to which spatial ability and age-related differences in environment learning interact. The experiment examines spatial mental representation derived from taking a realistic route acquired using virtual environment and compares individuals different in age but with similar spatial ability. A sample of 34 young (20-30 years) and 30 middle-aged (50-60 years) females with good mental rotation ability were chosen. Participants learned a complex route through its presentation in a virtual environment and then performed a series of tasks (landmark recognition, location of landmarks and verification of spatial relations). Results show that the two participant age groups had similar performance in landmark recognition task and in verification of sentences describing direct spatial relations; instead, the middle-aged group showed a poorer performance than younger in their ability to locate landmarks and to judge the truth of indirect spatial sentences. These results first suggest that spatial abilities have to be seriously considered to avoid any confusion with age, as age-related differences are attenuated when individuals are different in age but similar in spatial ability. Second they confirm a specific difficulty of older participants to handle spatial information in a global configuration.

Using a Computer-Based Virtual Environment to Assess Social Cognition in Aging: An Exploratory Study of the REALSoCog Task.

Although previous studies have suggested that some component processes of social cognition decline in normal aging, several methodological limitations can be pointed out. Traditional sociocognitive tasks assess processes separately and lack ecological validity. In the present study, the main aim was to propose an integrative social cognition assessment in normal aging using an original computer-based task developed in non-immersive virtual reality. Forty-five young adults (YA) and 50 older adults (OA) were asked to navigate in a simulated city environment and to judge several situations that they encountered. These situations investigated social norms by displaying control or (conventional/moral) transgressions. Following each situation, the participants were asked several questions in order to assess their ability to make moral judgments, affective and cognitive theory of mind, emotional reactivity and empathy, and the propensity to act in a socially appropriate or inappropriate way. The main results showed (i) a preserved ability to detect moral and conventional transgressions with advancing age; (ii) participants' preserved cognitive ToM abilities; (iii) an age-related decline in affective ToM, that disappeared when the victim was a senior; (iv) preserved emotional reactivity and emotional empathy in normal aging; (v) an increase in inappropriate behavioral intentions in normal aging. Offering more naturalistic conditions, this new task is an interesting integrative measure of sociocognitive functioning to better reflect social behavior in daily living.

Young and Older Adults Benefit From Sleep, but Not From Active Wakefulness for Memory Consolidation of What-Where-When Naturalistic Events.

An extensive psychological literature shows that sleep actively promotes human episodic memory (EM) consolidation in younger adults. However, evidence for the benefit of sleep for EM consolidation in aging is still elusive. In addition, most of the previous studies used EM assessments that are very different from everyday life conditions and are far from considering all the hallmarks of this memory system. In this study, the effect of an extended period of sleep was compared to the effect of an extended period of active wakefulness on the EM consolidation of naturalistic events, using a novel (What-Where-When) EM task, rich in perceptual details and spatio-temporal context, presented in a virtual environment. We investigated the long-term What-Where-When and Details binding performances of young and elderly people before and after an interval of sleep or active wakefulness. Although we found a noticeable age-related decline in EM, both age groups benefited from sleep, but not from active wakefulness. In younger adults, only the period of sleep significantly enhanced the capacity to associate different components of EM (binding performance) and more specifically the free recall of what-when information. Interestingly, in the elderly, sleep significantly enhanced not only the recall of factual elements but also associated details and contextual information as well as the amount of high feature binding (i.e., What-Where-When and Details). Thus, this study evidences the benefit of sleep, and the detrimental effect of active wakefulness, on long-term feature binding, which is one of the core characteristics of EM, and its effectiveness in normal aging. However, further research should investigate whether this benefit is specific to sleep or more generally results from the effect of a post-learning period of reduced interference, which could also concern quiet wakefulness.

An Impairment of Prospective Memory in Mild Alzheimer's Disease: A Ride in a Virtual Town.

Objective: Research suggests that prospective memory (PM) is impaired from the very early stages of Alzheimer's disease (AD). We sought to further characterize this impairment in patients with mild AD, using a virtual reality (VR) task to provide ecological assessment of PM. Methods: Fifteen cognitively normal older individuals (76.47 years old ± 4.14, MMSE: 28.80 ± 1.21), and 17 patients with mild AD (79.29 years old ± 4.45, MMSE: 22.82 ± 2.83) were asked to recall the prospective and retrospective components of seven intentions in a virtual town task. Six intentions were event-based, where the prospective cue was either highly (three intentions) or weakly (three intentions) associated with the retrospective component. The remaining intention was time-based. All participants completed a neuropsychological assessment of episodic memory, semantic memory and executive functioning. Non-parametric tests were used to compare the two groups on the different intentions types and components. Correlations between cognition and PM scores were then realized to further understand the cognitive correlates of the PM impairment in patients with AD. Results: Overall, patients with Alzheimer disease recalled fewer intentions than controls, with the retrospective component and time-based intentions being the most challenging for them. The strength of the association between the prospective and retrospective components, however, had no effect on their performance. Event-based PM impairment, as well as deficit in the recall of prospective component correlated with memory and executive functions performance. Conclusion: PM is impaired in AD. Both automatic and controlled processes of PM retrieval are disturbed. This study also confirms the reliability of VR for assessing complex cognitive functions such as PM.

Saccade dynamics before, during, and after saccadic adaptation in humans.

PURPOSE: When saccade amplitude is systematically inadequate relative to the desired target position, the saccadic system adaptively modifies the amplitude of subsequent saccades so as to recover precise targeting capabilities. The effect of saccadic adaptation on saccade metrics (amplitude, direction) is well documented, but the effect on dynamics (velocity, duration, acceleration, deceleration) remains to be fully elucidated. METHODS: The dynamics of adapted saccades were compared with that of baseline saccades of similar amplitudes. RESULTS: The peak deceleration and skewness (duration of the acceleration period/duration of the deceleration period) were modified by adaptation. CONCLUSIONS: The results point toward involvement of the cerebellum rather than the brain stem saccade generator in human saccadic adaptation.

Is binding decline the main source of the ageing effect on prospective memory? A ride in a virtual town.

Objective: This study was designed to improve our understanding of prospective memory (PM) changes in ageing, and to identify the cognitive correlates of PM decline, using a virtual environment, to provide a more realistic assessment than traditional laboratory tasks. Design: Thirty-five young and 29 older individuals exposed to a virtual town were asked to recall three event-based intentions with a strong link between prospective and retrospective components, three event-based intentions with a weak link, and three time-based intentions. They also underwent retrospective episodic memory, executive functions, binding in working memory, processing speed, and time estimation assessments. Results: Older individuals recalled fewer intentions than young adults. While age-related PM decline affected the recall of both prospective and retrospective components, the recall of the latter seemed more challenging for older individuals when the link was weak. This PM decline was linked to an age-related decline in the binding process in working memory, as well as in processing speed, executive functioning, and episodic memory, depending on the nature of intentions. Conclusion: PM appears to be sensitive to ageing, even when the device is thought to be ecological. This decline is particularly pronounced when controlled processes are needed.

A Serious Game to Improve Cognitive Functions in Schizophrenia: A Pilot Study.

Cognitive deficits in schizophrenia impair everyday functioning and instrumental daily living activities. These disabilities can be partly responsible for chronicity and institutionalization. We present here a virtual reality (VR) tool in which patients with schizophrenia performed a virtual game in an imaginary town during a 3-month program. In a pilot study, seven patients with schizophrenia (DSM-5), institutionalized for many years, attended weekly 1-h-and-a-half sessions organized by two clinicians. During the first sessions, they listed together the difficulties they experienced in everyday organization and planning. After being familiarized with the joystick and the VR environment, they navigated in the town, and planned actions that were difficult for them to carry out in their usual life (e.g., shopping, memorizing the way to the supermarket or being on time at a meeting point). They had to look for alternative routes and practice a switch from a 2D Map to the 3D Map. They also gathered their efforts to share strategies for each action, or discussed the action plan they could generate to solve concrete problems. The pre/post-neuropsychological evaluations showed attention, working memory, prospective, and retrospective memory benefits, but no improvement in planning as assessed by the Zoo map test and the action program subtest of Behavioral Assessment of the Dysexecutive Syndrome. Patients also clinically and functionally improved, gaining autonomy. Pragmatically, they reported a strong energy to elaborate concrete plans to search for jobs, or return to activities in the community. Qualitative assessments showed a benefit in sparing time, planning better, enriched relatedness, and better management of their housework. This VR game opens avenue to rehabilitation for patients with schizophrenia experiencing chronicity in their life, less attendance in daycare units, and a better community living. This program might reduce neurocognitive difficulties and might evolve into a true method for cognitive remediation (trial n° 2011-A00988-33).

Intermittent theta burst stimulation over left BA10 enhances virtual reality-based prospective memory in healthy aged subjects.

Prospective memory (PM) refers to a complex cognitive ability that underpins the delayed execution of previously formulated intentions. PM performance declines early in normal aging and this process is accentuated in Alzheimer's disease. The left frontopolar cortex (BA10) has been consistently assigned a major role in PM functioning, but whether it can be noninvasively modulated to enhance PM performance in aged people has not been addressed so far. Here, we investigated the effects of modulating left BA10 by means of theta burst stimulation (TBS), using either excitatory (intermittent TBS), inhibitory (continuous TBS) or control (vertex) TBS in healthy aged subjects. The behavioral effects were assessed using a reliable and ecological virtual reality PM task that included both event- and time-based retrievals. As compared with vertex stimulation, event-based PM performance significantly improved after excitatory stimulation, whereas inhibitory stimulation had no significant effect. Additionally, and across the different types of stimulation, performance for congruent links between the event-based PM cue and the action to be performed was significantly better as compared with incongruent links. In conclusion, intermittent TBS might provide a relevant interventional strategy to counteract the decline of cognitive functions and memory abilities in normal aging.

Landmark and route knowledge in children's spatial representation of a virtual environment.

This study investigates the development of landmark and route knowledge in complex wayfinding situations. It focuses on how children (aged 6, 8, and 10 years) and young adults (n = 79) indicate, recognize, and bind landmarks and directions in both verbal and visuo-spatial tasks after learning a virtual route. Performance in these tasks is also related to general verbal and visuo-spatial abilities as assessed by independent standardized tests (attention, working memory, perception of direction, production and comprehension of spatial terms, sentences and stories). The results first show that the quantity and quality of landmarks and directions produced and recognized by participants in both verbal and visuo-spatial tasks increased with age. In addition, an increase with age was observed in participants' selection of decisional landmarks (i.e., landmarks associated with a change of direction), as well as in their capacity to bind landmarks and directions. Our results support the view that children first acquire landmark knowledge, then route knowledge, as shown by their late developing ability to bind knowledge of directions and landmarks. Overall, the quality of verbal and visuo-spatial information in participants' spatial representations was found to vary mostly with their visuo-spatial abilities (attention and perception of directions) and not with their verbal abilities. Interestingly, however, when asked to recognize landmarks encountered during the route, participants show an increasing bias with age toward choosing a related landmark of the same category, regardless of its visual characteristics, i.e., they incorrectly choose the picture of another fountain. The discussion highlights the need for further studies to determine more precisely the role of verbal and visuo-spatial knowledge and the nature of how children learn to represent and memorize routes.

Effects of enactment in episodic memory: a pilot virtual reality study with young and elderly adults.

None of the previous studies on aging have tested the influence of action with respect to the degree of interaction with the environment (active or passive navigation) and the source of itinerary choice (self or externally imposed), on episodic memory (EM) encoding. The aim of this pilot study was to explore the influence of these factors on feature binding (the association between what, where, and when) in EM and on the subjective sense of remembering. Navigation in a virtual city was performed by 64 young and 64 older adults in one of four modes of exploration: (1) passive condition where participants were immersed as passengers of a virtual car [no interaction, no itinerary control (IC)], (2) IC (the subject chose the itinerary, but did not drive the car), (3) low, or (4) high navigation control (the subject just moved the car on rails or drove the car with a steering-wheel and a gas pedal on a fixed itinerary, respectively). The task was to memorize as many events encountered in the virtual environment as possible along with their factual (what), spatial (where), and temporal (when) details, and then to perform immediate and delayed memory tests. An age-related decline was evidenced for immediate and delayed feature binding. Compared to passive and high navigation conditions, and regardless of age-groups, feature binding was enhanced by low navigation and IC conditions. The subjective sense of remembering was boosted by the IC in older adults. Memory performance following high navigation was specifically linked to variability in executive functions. The present findings suggest that the decision of the itinerary is beneficial to boost EM in aging, although it does not eliminate age-related deficits. Active navigation can also enhance EM when it is not too demanding for subjects' cognitive resources.

The influence of action on episodic memory: a virtual reality study.

A range of empirical findings suggest that active learning is important for memory. However, few studies have focused on the mechanisms underlying this enactment effect in episodic memory using complex environments. Research using virtual reality has yielded inconsistent results. We postulated that the effect of action depends on the degree of interaction with the environment and freedom in the planning of an itinerary. To test these hypotheses, we disentangled the interaction and planning components of action to investigate whether each enhances factual and spatial memory. Seventy-two participants (36 male and 36 female) explored a virtual town in one of three experimental conditions: (a) a passive condition where participants were immersed as passenger of the car (no interaction, no planning); (b) a planning-only condition (the subject chose the itinerary but did not drive the car); (c) an interaction-only condition (the subject drove the car but the itinerary was fixed). We found that itinerary choice and motor control both enhanced spatial memory, while factual memory was impaired by online motor control. The role of action in memory is discussed.

The planning of a sequence of saccades in pro- and antisaccade tasks: influence of visual integration time and concurrent motor processing.

Previous studies have shown that a saccade is coded in a specific reference frame according to its goal: to aim for a new object or to explore an object which has already been fixated. In a two saccade sequence, the second saccade aiming for a new object is programmed in a retinocentric reference frame in which the spatial location of the second object is stored in spatial memory before the first saccade and updated after its execution. The second saccade exploring the same object is coded in an oculocentric reference frame in which object size is directly transformed into a fixed motor vector, encoded in motor memory before the first saccade and simply applied after its execution. The integration of parafoveal visual information appears to be crucial in the selection of the appropriate reference frame. The two experiments presented here investigate how and when the saccadic system integrates visual information to plan a sequence of saccades. In separate blocks, subjects were asked to execute a sequence of prosaccades directed toward a single object or two short objects, or to execute a sequence of antisaccades in the opposite direction of the stimuli. The latency of the initial saccade was modulated by using the Gap-200, Gap-0 and Overlap-600 ms paradigms. The results show that the time available for segmenting the visual stimulation into discrete objects and application of a specific reference frame according to this segmentation is critical for saccadic planning.