Stress Disrupts Human Hippocampal-Prefrontal Function during Prospective Spatial Navigation and Hinders Flexible Behavior.

The ability to anticipate and flexibly plan for the future is critical for achieving goal-directed outcomes. Extant data suggest that neural and cognitive stress mechanisms may disrupt memory retrieval and restrict prospective planning, with deleterious impacts on behavior. Here, we examined whether and how acute psychological stress influences goal-directed navigational planning and efficient, flexible behavior. Our methods combined fMRI, neuroendocrinology, and machine learning with a virtual navigation planning task. Human participants were trained to navigate familiar paths in virtual environments and then (concurrent with fMRI) performed a planning and navigation task that could be most efficiently solved by taking novel shortcut paths. Strikingly, relative to non-stressed control participants, participants who performed the planning task under experimentally induced acute psychological stress demonstrated (1) disrupted neural activity critical for mnemonic retrieval and mental simulation and (2) reduced traversal of shortcuts and greater reliance on familiar paths. These neural and behavioral changes under psychological stress were tied to evidence for disrupted neural replay of memory for future locations in the spatial environment, providing mechanistic insight into why and how stress can alter planning and foster inefficient behavior.

Cognitive focus affects spatial decisions under conditions of uncertainty.

Finding one's way to a destination is a common, everyday task that often relies on spatial information provided by humans and/or automatic devices. However, the information can be inaccurate. How we decide which route to take will depend on our thoughts about the available route information, including who or what provided it, and how these sources may be associated with differential accuracy and fallibility. In three experiments (previously reported in Brunyé et al. (Q J Exper Psychol 68(3):585-607, 2015)), we found that when route directions conflicted with the perceived environment, people trusted the landmark information other humans provided, but relied on the turn direction information from an automatic device. But what guides these behavioral results? Here we present a systematic linguistic analysis of retrospective reports that sheds some light on how information about the direction source affects cognitive focus. A focus on direction sources in the instruction triggered a cognitive focus on the direction source throughout. Participants who systematically switched strategies focused more on features of the scenario than those who did not. Non-switching strategies were associated with a higher focus on the participants' own reasoning processes, in particular when relying on turn information. These results highlight how cognitive focus is guided by scenario factors and individual preferences, triggering inferences that influence decisions.

Content Tuning in the Medial Temporal Lobe Cortex: Voxels that Perceive, Retrieve.

How do we recall vivid details from our past based only on sparse cues? Research suggests that the phenomenological reinstatement of past experiences is accompanied by neural reinstatement of the original percept. This process critically depends on the medial temporal lobe (MTL). Within the MTL, perirhinal cortex (PRC) and parahippocampal cortex (PHC) are thought to support encoding and recall of objects and scenes, respectively, with the hippocampus (HC) serving as a content-independent hub. If the fidelity of recall indeed arises from neural reinstatement of perceptual activity, then successful recall should preferentially draw upon those neural populations within content-sensitive MTL cortex that are tuned to the same content during perception. We tested this hypothesis by having eighteen human participants undergo functional MRI (fMRI) while they encoded and recalled objects and scenes paired with words. Critically, recall was cued with the words only. While HC distinguished successful from unsuccessful recall of both objects and scenes, PRC and PHC were preferentially engaged during successful versus unsuccessful object and scene recall, respectively. Importantly, within PRC and PHC, this content-sensitive recall was predicted by content tuning during perception: Across PRC voxels, we observed a positive relationship between object tuning during perception and successful object recall, while across PHC voxels, we observed a positive relationship between scene tuning during perception and successful scene recall. Our results thus highlight content-based roles of MTL cortical regions for episodic memory and reveal a direct mapping between content-specific tuning during perception and successful recall.

Stress Impairs Episodic Retrieval by Disrupting Hippocampal and Cortical Mechanisms of Remembering.

Despite decades of science investigating the neural underpinnings of episodic memory retrieval, a critical question remains: how does stress influence remembering and the neural mechanisms of recollection in humans? Here, we used functional magnetic resonance imaging and multivariate pattern analyses to examine the effects of acute stress during retrieval. We report that stress reduced the probability of recollecting the details of past experience, and that this impairment was driven, in part, by a disruption of the relationship between hippocampal activation, cortical reinstatement, and memory performance. Moreover, even memories expressed with high confidence were less accurate under stress, and this stress-induced decline in accuracy was explained by reduced posterior hippocampal engagement despite similar levels of category-level cortical reinstatement. Finally, stress degraded the relationship between the engagement of frontoparietal control networks and retrieval decision uncertainty. Collectively, these findings demonstrate the widespread consequences of acute stress on the neural systems of remembering.

Acute stress and episodic memory retrieval: neurobiological mechanisms and behavioral consequences.

Episodic retrieval allows people to access memories from the past to guide current thoughts and decisions. In many real-world situations, retrieval occurs under conditions of acute stress, either elicited by the retrieval task or driven by other, unrelated concerns. Memory under such conditions may be hindered, as acute stress initiates a cascade of neuromodulatory changes that can impair episodic retrieval. Here, we review emerging evidence showing that dissociable stress systems interact over time, influencing neural function. In addition to the adverse effects of stress on hippocampal-dependent retrieval, we consider how stress biases attention and prefrontal cortical function, which could further affect controlled retrieval processes. Finally, we consider recent data indicating that stress at retrieval increases activity in a network of brain regions that enable reflexive, rapid responding to upcoming threats, while transiently taking offline regions supporting flexible, goal-directed thinking. Given the ubiquity of episodic memory retrieval in everyday life, it is critical to understand the theoretical and applied implications of acute stress. The present review highlights the progress that has been made, along with important open questions.

Where did it come from, where do you go? Direction sources influence navigation decisions during spatial uncertainty.

Previous research on route directions largely considers the case when a knowledgeable route-giver conveys accurate information. In the real world, however, route information is sometimes inaccurate, and directions can lead navigators astray. We explored how participants respond to route directions containing ambiguities between landmarks and turn directions, forcing reliance on one or the other. In three experiments, participants read route directions (e.g., To get to the metro station, take a right at the pharmacy) and then selected from destinations on a map. Critically, in half of the trials the landmark (pharmacy) and turn (right) directions were conflicting, such that the participant had to make a decision under conditions of uncertainty; under these conditions, we measured whether participants preferentially relied upon landmark- versus direction-based strategies. Across the three experiments, participants were either provided no information regarding the source of directions (Experiment 1), or told that the source of directions was a GPS device (Experiment 2), or a human (Experiment 3). Without information regarding the source of directions, participants generally relied on landmarks or turn information under conditions of ambiguity; in contrast, with a GPS source participants relied primarily on turn information, and with a human source on landmark information. Results were robust across gender and individual differences in spatial preference. We discuss these results within the context of spatial decision-making theory and consider implications for the design and development of landmark-inclusive navigation systems.

Acute exercise increases oxygenated and deoxygenated hemoglobin in the prefrontal cortex.

Both acute and chronic exercise is consistently associated with a number of benefits to physical and mental health, including cardiovascular function, body weight, mood, and cognition. Near-infrared spectroscopy is an ideal method to measure changes in oxygenated and deoxygenated hemoglobin (O2Hb and dHb) levels in the prefrontal cortex (PFC) during exercise, to better understand the locus of such changes in affective and cognitive processes. The present study tracked time-dependent changes in O2Hb and dHb levels in the PFC as a function of parametrically manipulated target exercise intensity. Near-infrared spectroscopy was conducted as regular exercisers completed a 30-min bout of exercise with one of three target intensities: 52% (low condition), 68% (moderate condition), or 84% (high condition) of age-adjusted maximum heart rate. Heart rate data confirmed that the participants reached their goal intensities immediately, after 10 min, or after 20 min, respectively. Data showed that O2Hb and dHb levels in the PFC increased as a function of both exercise load and duration. An 84%>68%>52% difference was evident after 18 min of cycling for O2Hb and after 23 min of cycling for dHb. The present results add to the growing body of literature showing that at submaximal levels, increasing exercise intensities reliably promote prefrontal cerebral oxygenation.

Stepping into a map: initial heading direction influences spatial memory flexibility.

Learning a novel environment involves integrating first-person perceptual and motoric experiences with developing knowledge about the overall structure of the surroundings. The present experiments provide insights into the parallel development of these egocentric and allocentric memories by intentionally conflicting body- and world-centered frames of reference during learning, and measuring outcomes via online and offline measures. Results of two experiments demonstrate faster learning and increased memory flexibility following route perspective reading (Experiment 1) and virtual navigation (Experiment 2) when participants begin exploring the environment on a northward (vs. any other direction) allocentric heading. We suggest that learning advantages due to aligning body-centered (left/right/forward/back) with world-centered (NSEW) reference frames are indicative of three features of spatial memory development and representation. First, memories for egocentric and allocentric information develop in parallel during novel environment learning. Second, cognitive maps have a preferred orientation relative to world-centered coordinates. Finally, this preferred orientation corresponds to traditional orientation of physical maps (i.e., north is upward), suggesting strong associations between daily perceptual and motor experiences and the manner in which we preferentially represent spatial knowledge.

Happiness by association: breadth of free association influences affective states.

Several studies have demonstrated that affective states influence the number of associations formed between remotely related concepts. Someone in a neutral or negative affective state might draw the association between cold and hot, whereas someone in a positive affective state might spontaneously form the more distant association between cold and sneeze. Could the reverse be true, that generating increasingly broad or narrow associations will put someone in a more or less positive affective state? We test this possibility by using verbal free association tasks, and asking whether the breadth of semantic associativity between cue words and generated responses might predict resulting affective states. Two experiments show that generating broader associations, regardless of their valence, changes affect; specifically, broader associations lowered negative affect and marginally increased positive affect over time. These findings carry implications for theories positing interactions between brain areas mediating associative processing and affect, and may hold promise for enhancing affect in clinical contexts.

Abstract spatial concept priming dynamically influences real-world actions.

Experienced regularities in our perceptions and actions play important roles in grounding abstract concepts such as social status, time, and emotion. Might we similarly ground abstract spatial concepts in more experienced-based domains? The present experiment explores this possibility by implicitly priming abstract spatial terms (north, south, east, west) and then measuring participants' hand movement trajectories while they respond to a body-referenced spatial target (up, down, left, right) in a verbal (Exp. 1) or spatial (Exp. 2) format. Results from two experiments demonstrate temporally dynamic and prime biased movement trajectories when the primes are incongruent with the targets (e.g., north - left, west - up). That is, priming abstract coordinate directions influences subsequent actions in response to concrete target directions. These findings provide the first evidence that abstract concepts of world-centered coordinate axes are implicitly understood in the context of concrete body-referenced axes; critically, this abstract-concrete relationship manifests in motor movements, and may have implications for spatial memory organization.

The fabric of thought: priming tactile properties during reading influences direct tactile perception.

The present studies examined whether implied tactile properties during language comprehension influence subsequent direct tactile perception, and the specificity of any such effects. Participants read sentences that implicitly conveyed information regarding tactile properties (e.g., Grace tried on a pair of thick corduroy pants while shopping) that were either related or unrelated to fabrics and varied in implied texture (smooth, medium, rough). After reading each sentence, participants then performed an unrelated rating task during which they felt and rated the texture of a presented fabric. Results demonstrated that the texture properties implied in sentences influence direct tactile perception. Specifically, after reading about a smooth or rough texture, subsequent fabric ratings became notably smoother or rougher, respectively. However, we also show that there was some specificity to these effects: Fabric-related sentences elicited more specific and interactive effects on subsequent ratings. Together, we demonstrate that under certain circumstances, language comprehension can prime tactile representations and affect direct tactile perception. Results are discussed with regard to the nature and scope of multimodal mental simulation during reading.

Up north and down south: implicit associations between topography and cardinal direction.

Route planners show a reliable tendency to select south- relative to north-going routes between two horizontally (east/west) aligned landmarks, suggesting the application of a north-is-up heuristic (Brunyé, Mahoney, Gardony, & Taylor, 2010). The source of this north-is-up bias remains unknown, and there is no strong evidence to suggest that it is due to explicit strategy use. In four experiments, we attempt to further elucidate the source of this effect by testing whether it can be attributed to implicit associations between cardinal direction (north/south) and topography (mountainous/level terrain). Experiments 1 and 2 used an adapted Implicit Association Test and demonstrate automatically activated judgements that associate north with mountainous and south with relatively level terrain. Experiment 3 rules out the possibility that this effect is due to the local topography of New England by replicating in participants from the topographically dissimilar Midwestern United States. Finally, Experiment 4 tests the relative contribution of implicit versus explicit associations between cardinal direction and topography in predicting route-planning asymmetries; we show that implicit associations are a stronger predictor of southern route biases than explicit processes. Overall, results demonstrate that the conceptualization of space can be driven by physically unfounded implicit associations between cardinal directions and topographical features, and these associations are at least partially responsible for southern route preferences.

Mouse cursor movement and eye tracking data as an indicator of pathologists' attention when viewing digital whole slide images.

CONTEXT: Digital pathology has the potential to dramatically alter the way pathologists work, yet little is known about pathologists' viewing behavior while interpreting digital whole slide images. While tracking pathologist eye movements when viewing digital slides may be the most direct method of capturing pathologists' viewing strategies, this technique is cumbersome and technically challenging to use in remote settings. Tracking pathologist mouse cursor movements may serve as a practical method of studying digital slide interpretation, and mouse cursor data may illuminate pathologists' viewing strategies and time expenditures in their interpretive workflow. AIMS: To evaluate the utility of mouse cursor movement data, in addition to eye-tracking data, in studying pathologists' attention and viewing behavior. SETTINGS AND DESIGN: Pathologists (N = 7) viewed 10 digital whole slide images of breast tissue that were selected using a random stratified sampling technique to include a range of breast pathology diagnoses (benign/atypia, carcinoma in situ, and invasive breast cancer). A panel of three expert breast pathologists established a consensus diagnosis for each case using a modified Delphi approach. MATERIALS AND METHODS: Participants' foveal vision was tracked using SensoMotoric Instruments RED 60 Hz eye-tracking system. Mouse cursor movement was tracked using a custom MATLAB script. STATISTICAL ANALYSIS USED: Data on eye-gaze and mouse cursor position were gathered at fixed intervals and analyzed using distance comparisons and regression analyses by slide diagnosis and pathologist expertise. Pathologists' accuracy (defined as percent agreement with the expert consensus diagnoses) and efficiency (accuracy and speed) were also analyzed. RESULTS: Mean viewing time per slide was 75.2 seconds (SD = 38.42). Accuracy (percent agreement with expert consensus) by diagnosis type was: 83% (benign/atypia); 48% (carcinoma in situ); and 93% (invasive). Spatial coupling was close between eye-gaze and mouse cursor positions (highest frequency ∆x was 4.00px (SD = 16.10), and ∆y was 37.50px (SD = 28.08)). Mouse cursor position moderately predicted eye gaze patterns (Rx = 0.33 and Ry = 0.21). CONCLUSIONS: Data detailing mouse cursor movements may be a useful addition to future studies of pathologists' accuracy and efficiency when using digital pathology.

High and Mighty: Implicit Associations between Space and Social Status.

Figurative language and our perceptuo-motor experiences frequently associate social status with physical space. In three experiments we examine the source and extent of these associations by testing whether people implicitly associate abstract social status indicators with concrete representations of spatial topography (level versus mountainous land) and relatively abstract representations of cardinal direction (south and north). Experiment 1 demonstrates speeded performance during an implicit association test (Greenwald et al., 1998) when average social status is paired with level topography and high status with mountainous topography. Experiments 2 and 3 demonstrate a similar effect but with relatively abstract representations of cardinal direction (south and north), with speeded performance when average and powerful social status are paired with south and north coordinate space, respectively. Abstract concepts of social status are perceived and understood in an inherently spatial world, resulting in powerful associations between abstract social concepts and concrete and abstract notions of physical axes. These associations may prove influential in guiding daily judgments and actions.