Jared Stokes

Temporal lobe functional activity and connectivity in young adult APOE ɛ4 carriers

We sought to determine if the APOE ε4 allele influences both the functional activation and connectivity of the medial temporal lobes (MTLs) during successful memory encoding in young adults.

Overlapping parietal activity in memory and perception: Evidence for the attention to memory model

The specific role of different parietal regions to episodic retrieval is a topic of intense debate. According to the Attention to Memory (AtoM) model, dorsal parietal cortex (DPC) mediates top–down attention processes guided by retrieval goals, whereas ventral parietal cortex (VPC) mediates bottom–up attention processes captured by the retrieval output or the retrieval cue. This model also hypothesizes that the attentional functions of DPC and VPC are similar for memory and perception. To investigate this last hypothesis, we scanned participants with event-related fMRI whereas they performed memory and perception tasks, each comprising an orienting phase (top–down attention) and a detection phase (bottom–up attention). The study yielded two main findings. First, consistent with the AtoM model, orienting-related activity for memory and perception overlapped in DPC, whereas detection-related activity for memory and perception overlapped in VPC. The DPC overlap was greater in the left intraparietal sulcus, and the VPC overlap in the left TPJ. Around overlapping areas, there were differences in the spatial distribution of memory and perception activations, which were consistent with trends reported in the literature. Second, both DPC and VPC showed stronger connectivity with medial-temporal lobe during the memory task and with visual cortex during the perception task. These findings suggest that, during memory tasks, some parietal regions mediate similar attentional control processes to those involved in perception tasks (orienting in DPC vs. detection in VPC), although on different types of information (mnemonic vs. sensory).

Processing of emotional distraction is both automatic and modulated by attention: Evidence from an event-related fmri investigation

Traditionally, emotional stimuli have been thought to be automatically processed via a bottom–up automatic “capture of attention” mechanism. Recently, this view has been challenged by evidence that emotion processing depends on the availability of attentional resources. Although these two views are not mutually exclusive, direct evidence reconciling them is lacking. One limitation of previous investigations supporting the traditional or competing views is that they have not systematically investigated the impact of emotional charge of task-irrelevant distraction in conjunction with manipulations of attentional demands. Using event-related fMRI, we investigated the nature of emotion–cognition interactions in a perceptual discrimination task with emotional distraction by manipulating both the emotional charge of the distracting information and the demands of the main task. Our findings show that emotion processing is both automatic and modulated by attention, but emotion and attention were only found to interact when finer assessments of emotional charge (comparison of most vs. least emotional conditions) were considered along with an effective manipulation of processing load (high vs. low). The study also identified brain regions reflecting the detrimental impact of emotional distraction on performance as well as regions involved in coping with such distraction. Activity in the dorsomedial pFC and ventrolateral pFC was linked to a detrimental impact of emotional distraction, whereas the dorsal ACC and lateral occipital cortex were involved in helping with emotional distraction. These findings demonstrate that task-irrelevant emotion processing is subjective to both the emotional content of distraction and the level of attentional demand.

Neural correlates of confidence during item recognition and source memory retrieval: Evidence for both dual-process and strength memory theories

Although the medial-temporal lobes (MTL), PFC, and parietal cortex are considered primary nodes in the episodic memory network, there is much debate regarding the contributions of MTL, PFC, and parietal subregions to recollection versus familiarity (dual-process theory) and the feasibility of accounts on the basis of a single memory strength process (strength theory). To investigate these issues, the current fMRI study measured activity during retrieval of memories that differed quantitatively in terms of strength (high vs. low-confidence trials) and qualitatively in terms of recollection versus familiarity (source vs. item memory tasks). Support for each theory varied depending on which node of the episodic memory network was considered. Results from MTL best fit a dual-process account, as a dissociation was found between a right hippocampal region showing high-confidence activity during the source memory task and bilateral rhinal regions showing high-confidence activity during the item memory task. Within PFC, several left-lateralized regions showed greater activity for source than item memory, consistent with recollective orienting, whereas a right-lateralized ventrolateral area showed low-confidence activity in both tasks, consistent with monitoring processes. Parietal findings were generally consistent with strength theory, with dorsal areas showing low-confidence activity and ventral areas showing high-confidence activity in both tasks. This dissociation fits with an attentional account of parietal functions during episodic retrieval. The results suggest that both dual-process and strength theories are partly correct, highlighting the need for an integrated model that links to more general cognitive theories to account for observed neural activity during episodic memory retrieval.

Complementary roles of human hippocampal subfields in differentiation and integration of spatial context

The unique circuitry of the hippocampus is thought to support the encoding and retrieval of context-rich episodic memories. Given the neuroanatomical differences between the hippocampal subfields, determining their functional roles during representation of contextual features in humans is an important yet unaddressed research goal. Prior studies suggest that, during the acquisition of information from the environment, the dentate gyrus (DG) and CA3 subfields rapidly differentiate competing contextual representations, whereas CA1, situated downstream from CA3/DG, is believed to process input from both CA3 and neocortical areas via the temporoammonic pathway. To further explore the functionality of these roles, we used high-resolution fMRI to investigate multivariate response patterns within CA3/DG and CA1 during the processing of spatial context. While undergoing functional imaging, participants viewed videos of virtual environments and were asked to discriminate between similar yet geometrically distinct cities. We manipulated a single contextual feature by systematically morphing the city configurations from one common geometric shape to another, resulting in four cities—two distinctively shaped cities and two intermediate “morphed” cities. Pattern similarity within CA3/DG scaled with geometric changes to the environment. In contrast, CA1 pattern similarity, as well as interregional pattern similarity between CA1 and parahippocampal cortex, increased for the regularly shaped configurations compared with the morphs. These results highlight different roles for subfields CA3/DG and CA1 in memory and advance our understanding of how subcomponents of the human hippocampal circuit represent contextual features of memories.

Neural Correlates of Opposing Effects of Emotional Distraction on Working Memory and Episodic Memory: An Event-Related fMRI Investigation

A fundamental question in the emotional memory literature is why emotion enhances memory in some conditions but disrupts memory in other conditions. For example, separate studies have shown that emotional stimuli tend to be better remembered in long-term episodic memory (EM), whereas emotional distracters tend to impair working memory (WM) maintenance. The first goal of this study was to directly compare the neural correlates of EM enhancement (EME) and WM impairing (WMI) effects, and the second goal was to explore individual differences in these mechanisms. During event-related functional magnetic resonance imaging (fMRI), participants maintained faces in WM while being distracted by emotional or neutral pictures presented during the delay period. EM for the distracting pictures was tested after scanning and was used to identify successful encoding activity for the picture distracters. The first goal yielded two findings: (1) emotional pictures that disrupted face WM but enhanced subsequent EM were associated with increased amygdala (AMY) and hippocampal activity (ventral system) coupled with reduced dorsolateral PFC (dlPFC) activity (dorsal system); (2) trials in which emotion enhanced EM without disrupting WM were associated with increased ventrolateral PFC activity. The ventral-dorsal switch can explain EME and WMI, while the ventrolateral PFC effect suggests a coping mechanism. The second goal yielded two additional findings: (3) participants who were more susceptible to WMI showed greater amygdala increases and PFC reductions; (4) AMY activity increased and dlPFC activity decreased with measures of attentional impulsivity. Taken together, these results clarify the mechanisms linking the enhancing and impairing effects of emotion on memory, and provide insights into the role of individual differences in the impact of emotional distraction.

Successful retrieval of competing spatial environments in humans involves hippocampal pattern separation mechanisms

The rodent hippocampus represents different spatial environments distinctly via changes in the pattern of “place cell” firing. It remains unclear, though, how spatial remapping in rodents relates more generally to human memory. Here participants retrieved four virtual reality environments with repeating or novel landmarks and configurations during high-resolution functional magnetic resonance imaging (fMRI). Both neural decoding performance and neural pattern similarity measures revealed environment-specific hippocampal neural codes. Conversely, an interfering spatial environment did not elicit neural codes specific to that environment, with neural activity patterns instead resembling those of competing environments, an effect linked to lower retrieval performance. We find that orthogonalized neural patterns accompany successful disambiguation of spatial environments while erroneous reinstatement of competing patterns characterized interference errors. These results provide the first evidence for environment-specific neural codes in the human hippocampus, suggesting that pattern separation/completion mechanisms play an important role in how we successfully retrieve memories. DOI: http://dx.doi.org/10.7554/eLife.10499.001

A tale of two temporal coding strategies: Common and dissociable brain regions involved in recency versus associative temporal order retrieval strategies

Numerous studies indicate the importance of the hippocampus to temporal order retrieval. However, behavioral studies suggest that there are different ways to retrieve temporal order information from encoded sequences, one involving an associative strategy (retrieving associations using neighboring items in a list) and another involving a recency strategy (determining which of two items came first). It remains unresolved, however, whether both strategies recruit the hippocampus or only associative strategies, consistent with the hippocampuss role in relational processing. To address this, we developed a paradigm in which we dissociated associative versus recency-based retrieval, involving the same stimulus presentation during retrieval. Associative retrieval involved an increase in RT (and decrease in performance) with greater distances between intervals, consistent with the need to retrieve intervening associations. Recency-based retrieval involved an increase in RT (and decrease in performance) with shorter distances between intervals, suggesting the use of a strength-based coding mechanism to retrieve information. We employed fMRI to determine the neural basis of the different strategies. Both strategies showed significant levels of hippocampal activation and connectivity that did not differ between tasks. In contrast, both univariate and connectivity pattern analyses revealed differences in extrahippocampal areas such as parietal and frontal cortices. A covariate analysis suggested that differences could not be explained by task difficulty alone. Together, these findings suggest that the hippocampus plays a role in both forms of temporal order retrieval, with neocortical networks mediating the different cognitive demands for associative versus recency-based temporal order retrieval.

Search and recovery of autobiographical and laboratory memories: Shared and distinct neural components

ABSTRACT Functional neuroimaging evidence suggests that there are differences in the neural correlates of episodic memory for laboratory stimuli (laboratory memory) and for events from ones own life (autobiographical memory). However, this evidence is scarce and often confounded with differences in memory testing procedures. Here, we directly compared the neural mechanisms underlying the search and recovery of autobiographical and laboratory memories while minimizing testing differences. Before scanning, participants completed a laboratory memory encoding task in which they studied four‐word “chains” spread across three word pairs. During scanning, participants completed a laboratory memory retrieval task, in which they recalled the word chains, and an autobiographical memory retrieval task, in which they recalled specific personal events associated with word cues. Importantly, response times were similar in the two tasks, allowing for a direct comparison of the activation time courses. We found that during memory search (searching for the memory target), similar brain regions were activated during both the autobiographical and laboratory tasks, whereas during memory recovery (accessing the memory traces; i.e., ecphory), clear differences emerged: regions of the default mode network (DMN) were activated greater during autobiographical than laboratory memory, whereas the bilateral superior parietal lobules were activated greater during laboratory than autobiographical memory. Also, multivariate functional connectivity analyses revealed that regardless of memory stage, the DMN and ventral attention network exhibited a more integrated topology in the functional network underlying autobiographical (vs. laboratory) memory retrieval, whereas the fronto‐parietal task control network exhibited a more integrated topology in the functional network underlying laboratory (vs. autobiographical) memory retrieval. These findings further characterize the shared and distinct neural components underlying autobiographical and laboratory memories, and suggest that differences in autobiographical vs. laboratory memory brain activation previously reported in the literature reflect memory recovery rather than search differences. Graphical abstract Figure. No caption available. HighlightsWe compared autobiographical (AM) vs. laboratory (LM) memory retrieval.Task brain activation differences occurred during memory recovery but not search.The default mode network was more strongly activated during AM recovery.The superior parietal lobules were more strongly activated during LM recovery.The default mode network exhibited a more integrated topology during AM.

Learning-dependent evolution of spatial representations in large-scale virtual environments.

An important question regards how we use environmental boundaries to anchor spatial representations during navigation. Behavioral and neurophysiological models appear to provide conflicting predictions, and this question has been difficult to answer because of technical challenges with testing navigation in novel, large-scale, realistic spatial environments. We conducted an experiment in which participants freely ambulated on an omnidirectional treadmill while viewing novel, town-sized environments in virtual reality on a head-mounted display. Participants performed interspersed judgments of relative direction (JRD) to assay their spatial knowledge and to determine when during learning they employed environmental boundaries to anchor their spatial representations. We designed JRD questions that assayed directions aligned and misaligned with the axes of the surrounding rectangular boundaries and employed structural equation modeling to better understand the learning-dependent dynamics for aligned versus misaligned pointing. Pointing accuracy showed no initial directional bias to boundaries, although such “alignment effects” did emerge after the fourth block of learning. Preexposure to a map in Experiment 2 led to similar overall findings. A control experiment in which participants studied a map but did not navigate the environment, however, demonstrated alignment effects after a brief, initial learning experience. Our results help to bridge the gap between neurophysiological models of location-specific firing in rodents and human behavioral models of spatial navigation by emphasizing the experience-dependent accumulation of route-specific knowledge. In particular, our results suggest that the use of spatial boundaries as an organizing schema during navigation of large-scale space occurs in an experience-dependent fashion.