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1.
bioRxiv ; 2024 Jun 10.
Article in English | MEDLINE | ID: mdl-38915680

ABSTRACT

Prior studies examining the neural mechanisms underlying retrieval success and precision have yielded inconsistent results. Here, their neural correlates were examined using a memory task that assessed precision for spatial location. A sample of healthy young adults underwent fMRI scanning during a single study-test cycle. At study, participants viewed a series of object images, each placed at a randomly selected location on an imaginary circle. At test, studied images were intermixed with new images and presented to the participants. The requirement was to move a cursor to the location of the studied image, guessing if necessary. Participants then signaled whether the presented image as having been studied. Memory precision was quantified as the angle between the studied location and the location selected by the participant. A precision effect was evident in the left angular gyrus, where BOLD activity covaried across trials with location accuracy. Multi-voxel pattern analysis also revealed a significant item-level reinstatement effect for high-precision trials. There was no evidence of a retrieval success effect in the angular gyrus. BOLD activity in the hippocampus was insensitive to both success and precision. These findings are partially consistent with prior evidence that success and precision are dissociable features of memory retrieval.

2.
Article in English | MEDLINE | ID: mdl-38445641

ABSTRACT

Spatial navigation deficits are often observed among older adults on tasks that require navigating virtual reality (VR) environments on a computer screen. We investigated whether these age differences are attenuated when tested in more naturalistic and ambulatory virtual environments. In Experiment 1, young and older adults navigated a variant of the Morris Water Maze task in each of two VR conditions: a desktop VR condition which required using a mouse and keyboard to navigate, and an ambulatory VR condition which permitted unrestricted locomotion. In Experiment 2, we examined whether age- and VR-related differences in spatial performance were affected by the inclusion of additional spatial cues. In both experiments, older adults navigated to target locations less precisely than younger individuals in the desktop condition. Age differences were significantly attenuated, however, when tested in the ambulatory VR environment. These findings underscore the importance of developing naturalistic assessments of spatial memory and navigation.

3.
Neuron ; 111(7): 1037-1049, 2023 04 05.
Article in English | MEDLINE | ID: mdl-37023709

ABSTRACT

Spatial navigation and memory are often seen as heavily intertwined at the cognitive and neural levels of analysis. We review models that hypothesize a central role for the medial temporal lobes, including the hippocampus, in both navigation and aspects of memory, particularly allocentric navigation and episodic memory. While these models have explanatory power in instances in which they overlap, they are limited in explaining functional and neuroanatomical differences. Focusing on human cognition, we explore the idea of navigation as a dynamically acquired skill and memory as an internally driven process, which may better account for the differences between the two. We also review network models of navigation and memory, which place a greater emphasis on connections rather than the functions of focal brain regions. These models, in turn, may have greater explanatory power for the differences between navigation and memory and the differing effects of brain lesions and age.


Subject(s)
Memory, Episodic , Spatial Navigation , Humans , Brain , Cognition , Temporal Lobe , Hippocampus , Spatial Memory
4.
Elife ; 122023 04 21.
Article in English | MEDLINE | ID: mdl-37083558

ABSTRACT

Including geometric spatial cues in an environment can help reverse the difficulties with spatial navigation experienced by children and older adults.


Subject(s)
Cues , Spatial Navigation , Child , Humans , Aged , Space Perception
5.
bioRxiv ; 2023 Oct 02.
Article in English | MEDLINE | ID: mdl-36747699

ABSTRACT

Spatial navigation deficits in older adults are well documented. These findings are often based on experimental paradigms that require using a joystick or keyboard to navigate a virtual desktop environment. In the present study, we investigated whether age differences in spatial memory are attenuated when tested in a more naturalistic and ambulatory virtual environment. In Experiment 1, cognitively normal young and older adults navigated a virtual variant of the Morris Water Maze task in each of two virtual reality (VR) conditions: a desktop VR condition which required using a mouse and keyboard to navigate and an immersive and ambulatory VR condition which permitted unrestricted locomotion. In Experiment 2, we examined whether age- and VR-related differences in spatial performance were affected by the inclusion of additional spatial cues in an independent sample of young and older adults. In both experiments, older adults navigated to target locations less precisely than did younger individuals in the desktop condition, replicating numerous prior studies. These age differences were significantly attenuated, however, when tested in the fully immersive and ambulatory environment. These findings underscore the importance of developing naturalistic and ecologically valid measures of spatial memory and navigation, especially when performing cross-sectional studies of cognitive aging.

6.
Cereb Cortex ; 33(8): 4542-4552, 2023 04 04.
Article in English | MEDLINE | ID: mdl-36124666

ABSTRACT

Memory retrieval effects in the striatum are well documented and robust across experimental paradigms. However, the functional significance of these effects, and whether they are moderated by age, remains unclear. We used functional magnetic resonance imaging paired with an associative recognition task to examine retrieval effects in the striatum in a sample of healthy young, middle-aged, and older adults. We identified anatomically segregated patterns of enhanced striatal blood oxygen level-dependent (BOLD) activity during recollection- and familiarity-based memory judgments. Successful recollection was associated with enhanced BOLD activity in bilateral putamen and nucleus accumbens, and neither of these effects were reliably moderated by age. Familiarity effects were evident in the head of the caudate nucleus bilaterally, and these effects were attenuated in middle-aged and older adults. Using psychophysiological interaction analyses, we observed a monitoring-related increase in functional connectivity between the caudate and regions of the frontoparietal control network, and between the putamen and bilateral retrosplenial cortex and intraparietal sulcus. In all instances, monitoring-related increases in cortico-striatal connectivity were unmoderated by age. These results suggest that the striatum, and the caudate in particular, couples with the frontoparietal control network to support top-down retrieval-monitoring operations, and that the strength of these inter-regional interactions is preserved in later life.


Subject(s)
Corpus Striatum , Longevity , Corpus Striatum/physiology , Memory/physiology , Recognition, Psychology/physiology , Caudate Nucleus/diagnostic imaging , Magnetic Resonance Imaging , Neural Pathways/physiology , Brain Mapping
7.
J Neurosci ; 42(9): 1765-1776, 2022 03 02.
Article in English | MEDLINE | ID: mdl-35017225

ABSTRACT

Recent research suggests that episodic memory is associated with systematic differences in the localization of neural activity observed during memory encoding and retrieval. The retrieval-related anterior shift is a phenomenon whereby the retrieval of a stimulus event (e.g., a scene image) is associated with a peak neural response which is localized more anteriorly than the response elicited when the stimulus is experienced directly. Here, we examine whether the magnitude of the anterior shift (i.e., the distance between encoding- and retrieval-related response peaks) is moderated by age, and also whether the shift is associated with memory performance. Younger and older human subjects of both sexes underwent fMRI as they completed encoding and retrieval tasks on word-face and word-scene pairs. We localized peak scene and face selectivity for each individual participant within the face-selective precuneus and in three scene-selective (parahippocampal place area [PPA], medial place area, occipital place area) ROIs. In line with recent findings, we identified an anterior shift in the PPA and occipital place area in both age groups and, in older adults only, in the medial place area and precuneus also. Of importance, the magnitude of the anterior shift was larger in older than in younger adults. The shift within the PPA exhibited an age-invariant across-participant negative correlation with source memory performance, such that a smaller displacement between encoding- and retrieval-related neural activity was associated with better performance. These findings provide novel insights into the functional significance of the anterior shift, especially in relation to memory decline in older age.SIGNIFICANCE STATEMENT Cognitive aging is associated with reduced ability to retrieve precise details of previously experienced events. The retrieval-related anterior shift is a phenomenon in which category-selective cortical activity at retrieval is localized anterior to the peak activity at encoding. The shift is thought to reflect a bias at retrieval in favor of semantic and abstract information at the expense of low-level perceptual detail. Here, we report that the anterior shift is exaggerated in older relative to younger adults, and we demonstrate that a larger shift in the parahippocampal place area is associated with poorer memory performance. These findings suggest that the shift is sensitive to increasing age and that it is moderated by the quality and content of the retrieved episode.


Subject(s)
Memory, Episodic , Aged , Aging/physiology , Brain Mapping , Face , Female , Humans , Magnetic Resonance Imaging , Male , Memory Disorders , Mental Recall/physiology , Parietal Lobe
8.
J Neurosci ; 2021 Jun 15.
Article in English | MEDLINE | ID: mdl-34131036

ABSTRACT

Functional magnetic resonance imaging (fMRI) is among the foremost methods for mapping human brain function but provides only an indirect measure of underlying neural activity. Recent findings suggest that the neurophysiological correlates of the fMRI blood-oxygen-level-dependent (BOLD) signal might be regionally specific. We examined the neurophysiological correlates of the fMRI BOLD signal in the hippocampus and neocortex, where differences in neural architecture might result in a different relationship between the respective signals. Fifteen human neurosurgical patients (10 female, 5 male) implanted with depth electrodes performed a verbal free recall task while electrophysiological activity was recorded simultaneously from hippocampal and neocortical sites. The same patients subsequently performed a similar version of the task during a later fMRI session. Subsequent memory effects (SMEs) were computed for both imaging modalities as patterns of encoding-related brain activity predictive of later free recall. Linear mixed-effects modelling revealed that the relationship between BOLD and gamma-band SMEs was moderated by the lobar location of the recording site. BOLD and high gamma (70-150 Hz) SMEs positively covaried across much of the neocortex. This relationship was reversed in the hippocampus, where a negative correlation between BOLD and high gamma SMEs was evident. We also observed a negative relationship between BOLD and low gamma (30-70 Hz) SMEs in the medial temporal lobe more broadly. These results suggest that the neurophysiological correlates of the BOLD signal in the hippocampus differ from those observed in the neocortex.Significance Statement:The blood-oxygen-level-dependent (BOLD) signal forms the basis of fMRI but provides only an indirect measure of neural activity. Task-related modulation of BOLD signals are typically equated with changes in gamma-band activity; however, relevant empirical evidence comes largely from the neocortex. We examined neurophysiological correlates of the BOLD signal in the hippocampus, where the differing neural architecture might result in a different relationship between the respective signals. We identified a positive relationship between encoding-related changes in BOLD and gamma-band activity in frontal and parietal cortex. This effect was reversed in the hippocampus, where BOLD and gamma-band effects negatively covaried. These results suggest regional variability in the transfer function between neural activity and the BOLD signal in the hippocampus and neocortex.

9.
Neurobiol Aging ; 102: 73-88, 2021 06.
Article in English | MEDLINE | ID: mdl-33765433

ABSTRACT

Retrieval gating refers to the ability to modulate the retrieval of features of a single memory episode according to behavioral goals. Recent findings demonstrate that younger adults engage retrieval gating by attenuating the representation of task-irrelevant features of an episode. Here, we examine whether retrieval gating varies with age. Younger and older adults incidentally encoded words superimposed over scenes or scrambled backgrounds that were displayed in one of three spatial locations. Participants subsequently underwent fMRI as they completed two memory tasks: the background task, which tested memory for the word's background, and the location task, testing memory for the word's location. Employing univariate and multivariate approaches, we demonstrated that younger, but not older adults, exhibited attenuated reinstatement of scene information when it was goal-irrelevant (during the location task). Additionally, in younger adults only, the strength of scene reinstatement in the parahippocampal place area during the background task was related to item and source memory performance. Together, these findings point to an age-related decline in the ability to engage retrieval gating.


Subject(s)
Aging/psychology , Goals , Memory, Episodic , Mental Recall , Adolescent , Adult , Aged , Female , Hippocampus/diagnostic imaging , Hippocampus/physiology , Humans , Magnetic Resonance Imaging , Male , Young Adult
10.
Cereb Cortex ; 31(1): 106-122, 2021 01 01.
Article in English | MEDLINE | ID: mdl-32829396

ABSTRACT

Age-related reductions in neural selectivity have been linked to cognitive decline. We examined whether age differences in the strength of retrieval-related cortical reinstatement could be explained by analogous differences in neural selectivity at encoding, and whether reinstatement was associated with memory performance in an age-dependent or an age-independent manner. Young and older adults underwent fMRI as they encoded words paired with images of faces or scenes. During a subsequent scanned memory test participants judged whether test words were studied or unstudied and, for words judged studied, also made a source memory judgment about the associated image category. Using multi-voxel pattern similarity analyses, we identified robust evidence for reduced scene reinstatement in older relative to younger adults. This decline was however largely explained by age differences in neural differentiation at encoding; moreover, a similar relationship between neural selectivity at encoding and retrieval was evident in young participants. The results suggest that, regardless of age, the selectivity with which events are neurally processed at the time of encoding can determine the strength of retrieval-related cortical reinstatement.


Subject(s)
Aging/pathology , Cell Differentiation , Cognitive Dysfunction/pathology , Neurons/pathology , Adolescent , Adult , Aged , Cerebral Cortex , Cognitive Dysfunction/diagnostic imaging , Cognitive Dysfunction/psychology , Face , Female , Humans , Magnetic Resonance Imaging , Male , Memory , Memory Disorders/pathology , Memory Disorders/psychology , Mental Recall , Neuropsychological Tests , Psychomotor Performance , Recognition, Psychology , Young Adult
11.
Neuroimage Rep ; 1(3)2021 Sep.
Article in English | MEDLINE | ID: mdl-35434691

ABSTRACT

We examined whether post-retrieval monitoring processes supporting memory performance are more resource limited in older adults than younger individuals. We predicted that older adults would be more susceptible to an experimental manipulation that reduced the neurocognitive resources available to support post-retrieval monitoring. Young and older adults received transcranial magnetic stimulation (TMS) to the right dorsolateral prefrontal cortex (DLPFC) or a vertex control site during an associative recognition task. The right DLPFC was selected as a TMS target because the region is held to be a key member of a network of regions engaged during retrieval monitoring and is readily accessible to administration of TMS. We predicted that TMS to the right DLPFC would lead to reduced associative recognition accuracy, and that this effect would be more prominent in older adults. The results did not support this prediction. Recognition accuracy was significantly reduced in older adults relative to their younger counterparts, but the magnitude of this age difference was unaffected following TMS to the right DLPFC or vertex. These findings suggest that TMS to the right DLPFC was insufficient to deplete the neurocognitive resources necessary to support post-retrieval monitoring.

12.
eNeuro ; 7(3)2020.
Article in English | MEDLINE | ID: mdl-32341120

ABSTRACT

The aging brain is characterized by neural dedifferentiation, an apparent decrease in the functional selectivity of category-selective cortical regions. Age-related reductions in neural differentiation have been proposed to play a causal role in cognitive aging. Recent findings suggest, however, that age-related dedifferentiation is not equally evident for all stimulus categories and, additionally, that the relationship between neural differentiation and cognitive performance is not moderated by age. In light of these findings, in the present experiment, younger and older human adults (males and females) underwent fMRI as they studied words paired with images of scenes or faces before a subsequent memory task. Neural selectivity was measured in two scene-selective (parahippocampal place area (PPA) and retrosplenial cortex (RSC)] and two face-selective [fusiform face area (FFA) and occipital face area (OFA)] regions using both a univariate differentiation index and multivoxel pattern similarity analysis. Both methods provided highly convergent results, which revealed evidence of age-related reductions in neural dedifferentiation in scene-selective but not face-selective cortical regions. Additionally, neural differentiation in the PPA demonstrated a positive, age-invariant relationship with subsequent source memory performance (recall of the image category paired with each recognized test word). These findings extend prior findings suggesting that age-related neural dedifferentiation is not a ubiquitous phenomenon, and that the specificity of neural responses to scenes is predictive of subsequent memory performance independently of age.


Subject(s)
Brain Mapping , Occipital Lobe , Adult , Brain , Female , Humans , Magnetic Resonance Imaging , Male , Memory , Pattern Recognition, Visual , Photic Stimulation
13.
Neuroimage ; 207: 116397, 2020 02 15.
Article in English | MEDLINE | ID: mdl-31770638

ABSTRACT

Intra-cranial electroencephalographic brain recordings (iEEG) provide a powerful tool for investigating the neural processes supporting episodic memory encoding and form the basis of experimental therapies aimed at improving memory dysfunction. However, given the invasiveness of iEEG, investigations are constrained to patients with drug-resistant epilepsy for whom such recordings are clinically indicated. Particularly in the case of temporal lobe epilepsy (TLE), neuropathology and the possibility of functional reorganization are potential constraints on the generalizability of intra-cerebral findings and pose challenges to the development of therapies for memory disorders stemming from other etiologies. Here, samples of TLE (N â€‹= â€‹16; all of whom had undergone iEEG) and age-matched healthy control (N â€‹= â€‹19) participants underwent fMRI as they studied lists of concrete nouns. fMRI BOLD responses elicited by the study words were segregated according to subsequent performance on tests of delayed free recall and recognition memory. Subsequent memory effects predictive of both successful recall and recognition memory were evident in several neural regions, most prominently in the left inferior frontal gyrus, and did not demonstrate any group differences. Behaviorally, the groups did not differ in overall recall performance or in the strength of temporal contiguity effects. However, group differences in serial position effects and false alarm rates were evident during the free recall and recognition memory tasks, respectively. Despite these behavioral differences, neuropathology associated with temporal lobe epilepsy was apparently insufficient to give rise to detectable differences in the functional neuroanatomy of episodic memory encoding relative to neurologically healthy controls. The findings provide reassurance that iEEG findings derived from experimental paradigms similar to those employed here generalize to the neurotypical population.


Subject(s)
Epilepsy, Temporal Lobe/physiopathology , Memory Disorders/physiopathology , Memory, Episodic , Recognition, Psychology/physiology , Adolescent , Adult , Drug Resistant Epilepsy/physiopathology , Epilepsy, Temporal Lobe/pathology , Female , Humans , Magnetic Resonance Imaging/adverse effects , Male , Mental Recall/physiology , Prefrontal Cortex/physiopathology , Temporal Lobe/physiopathology
14.
Neuroimage ; 162: 186-198, 2017 11 15.
Article in English | MEDLINE | ID: mdl-28877515

ABSTRACT

Behavioral studies using delay and social discounting as indices of self-control and altruism, respectively, have revealed functional similarities between farsighted and social decisions. However, neural evidence for this functional link is lacking. Twenty-five young adults completed a delay and social discounting task during fMRI scanning. A spatiotemporal partial least squares analysis revealed that both forms of discounting were well characterized by a pattern of brain activity in areas comprising frontoparietal control, default, and mesolimbic reward networks. Both forms of discounting appear to draw on common neurocognitive mechanisms, regardless of whether choices involve intertemporal or interpersonal outcomes. We also observed neural profiles differentiating between high and low discounters. High discounters were well characterized by increased medial temporal lobe and limbic activity. In contrast, low discount rates were associated with activity in the medial prefrontal cortex and right temporoparietal junction. This pattern may reflect biological mechanisms underlying behavioral heterogeneity in discount rates.


Subject(s)
Altruism , Brain/physiology , Delay Discounting/physiology , Self-Control , Brain Mapping , Female , Humans , Magnetic Resonance Imaging , Male , Reward , Young Adult
15.
Conscious Cogn ; 22(3): 677-83, 2013 Sep.
Article in English | MEDLINE | ID: mdl-23681207

ABSTRACT

The ability to imagine hypothetical events in one's personal future is thought to involve a number of constituent cognitive processes. We investigated the extent to which individual differences in working memory capacity contribute to facets of episodic future thought. College students completed simple and complex measures of working memory and were cued to recall autobiographical memories and imagine future autobiographical events consisting of varying levels of specificity (i.e., ranging from generic to increasingly specific and detailed events). Consistent with previous findings, future thought was related to analogous measures of autobiographical memory, likely reflecting overlapping cognitive factors supporting both past and future thought. Additionally, after controlling for autobiographical memory, residual working memory variance independently predicted future episodic specificity. We suggest that when imagining future events, working memory contributes to the construction of a single, coherent, future event depiction, but not to the retrieval or elaboration of event details.


Subject(s)
Imagination/physiology , Memory, Short-Term/physiology , Adolescent , Adult , Female , Humans , Individuality , Male , Memory, Episodic , Thinking/physiology , Young Adult
16.
Biol Psychiatry ; 69(3): 260-5, 2011 Feb 01.
Article in English | MEDLINE | ID: mdl-20965498

ABSTRACT

BACKGROUND: Excessive discounting of future rewards has been observed in a variety of disorders and has been linked both to valuation of the past and to memory of past events. METHODS: To explore the functionality of discounting and memory, we examined whether training of working memory would result in less discounting of future rewards. In this study, 27 adults in treatment for stimulant use were randomly assigned to receive either working memory training or control training according to a yoked experimental design. Measures of delay discounting and several other cognitive behaviors were assessed pre- and posttraining. RESULTS: Rates of discounting of delayed rewards were significantly reduced among those who received memory training but were unchanged among those who received control training; other cognitive assessments were not affected by memory training. Discount rates were positively correlated with memory training performance measures. CONCLUSIONS: To our knowledge, this is the first study demonstrating that neurocognitive training on working memory decreases delay discounting. These results offer further evidence of a functional relationship between delay discounting and working memory.


Subject(s)
Amphetamine-Related Disorders/psychology , Education/methods , Impulsive Behavior/psychology , Memory, Short-Term , Adult , Cognition , Decision Making , Female , Humans , Male , Reward
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