Threat-induced modulation of hippocampal and striatal memory systems during navigation of a virtual environment

Goodman, Jarid; McClay, Mason; Dunsmoor, Joseph E.

doi:10.1016/j.nlm.2020.107160

Cited by 10 publications

(13 citation statements)

References 73 publications

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“…However, learners, compared to non-learners, were significantly more accurate in recalling the location of neutral objects during the task, as measured by object placement distance error and number of object locations recalled during post-task interviews. These findings are consistent with previous research on emotional arousal and impaired spatial memory retrieval (Goodman et al, 2020;Schwabe et al, 2007), where anxiety was found to impair performance in a virtual spatial radial maze task and was associated with reduced use of spatial learning strategies. Additionally, non-learners did not learn the location of the danger zone, further suggesting impaired spatial mapping.…”

Section: Memory Task Performancesupporting

confidence: 92%

Using Virtual Reality to Study Spatial Mapping and Threat Learning

Suarez-Jimenez,

Marino,

Rjabtsenkov

et al. 2024

Preprint

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Using spatial mapping processes to learn about threat and safety in an environment is crucial for survival. Research using conditioning paradigms has explored the effects of state (transient arousal) and trait anxiety (anxiety as an aspect of personality) on threat learning and acquisition. However, results are mixed, and little is known regarding why some individuals do not learn to discriminate between threat and safety during contextual conditioning. We used a virtual reality (VR) contextual threat conditioning paradigm to elucidate the effects of state and trait anxiety on contextual threat learning. 70 healthy participants (46 female) navigated and “picked” flowers in a VR environment. Flowers picked in the dangerous zone (half of the environment) were paired with an electric shock (or “bee sting”) to the hand; flowers picked in the safe zone were never paired with a shock. Participants also collected and returned neutral objects as a measure of spatial memory. Galvanic skin response (GSR) was measured throughout the task and anxiety was assessed via the State Trait Anxiety Inventory (STAI). Participants were categorized as learners if they correctly identified the two zones after the task. Non-learners, compared to learners, performed significantly worse during the spatial memory task and demonstrated significantly higher state anxiety scores and GSR levels throughout the task. Learners showed higher skin conductance response (SCR) in the dangerous zone compared to the safe zone while non-learners showed no SCR differences between zones. These results indicate that state anxiety may impair spatial mapping, disrupting contextual threat learning.

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Section: Memory Task Performancesupporting

confidence: 92%

Using Virtual Reality to Study Spatial Mapping and Threat Learning

Suarez-Jimenez,

Marino,

Rjabtsenkov

et al. 2024

Preprint

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“…Recently, the dorsal striatum which mediates procedural memories based on stimulus–response (S-R) associations was found by several researchers [ 10 ]. Aberrant DLS-dependent S-R memory occurs mainly in obsessive compulsive disorders [ 34 ] and drug addictions [ 35 ], but Goodman et al [ 36 ] proposed a hypothesis that hippocampal damage [ 37 ] could be the key that is critical for the enhancing effects of emotional arousal in charge of the amygdala [ 38 ] on dorsal striatal memory. From the theory above, it is reasonable to deduce that hippocampus dysfunction in the early stages of AD triggers emotional regulation in the amygdala, which further enhances DLS-dependent S-R memory.…”

Section: Discussionmentioning

confidence: 99%

Altered Functional Connectivity of Basal Ganglia in Mild Cognitive Impairment and Alzheimer’s Disease

Xiong

Chen

et al. 2022

Brain Sciences

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(1) Background: Alzheimer’s disease (AD), an age-progressive neurodegenerative disease that affects cognitive function, causes changes in the functional connectivity of the default-mode network (DMN). However, the question of whether AD-related changes occur in the functional connectivity of the basal ganglia has rarely been specifically analyzed. This study aimed to measure the changes in basal ganglia functional connectivity among patients with AD and mild cognitive impairment (MCI) in their resting state using the functional connectivity density (FCD) value, the functional connectivity (FC) intensity, and the graph theory index, and to confirm their influence on clinical manifestations. (2) Methods: Resting-state functional MRI (rs-fMRI) and neuropsychological data from 48 participants in the Alzheimer’s Disease Neuroimaging Initiative (ADNI) were used for analyses. The 48 ADNI participants comprised 16 patients with AD, 16 patients with MCI, and 16 normal controls (NCs). The functional connectivity of basal ganglia was evaluated by FCDs, FC strength, and graph theory index. We compared voxel-based FCD values between groups to show specific regions with significant variation and significant connectivity from ROI conduction to ROI analysis. Pearson’s correlation analyses between functional connectivity and several simultaneous clinical variables were also conducted. Additionally, receiver operating characteristic (ROC) analyses associated with classification were conducted for both FCD values and graph theory indices. (3) Results: The level of FCD in patients with cognitive impairment showed obvious abnormalities (including short-range and long-range FCD). In addition to DMN-related regions, aberrant functional connectivity was also found to be present in the basal ganglia, especially in the caudate and amygdala. The FCD values of the basal ganglia (involving the caudate and amygdala) were closely related to scores from the Mini-Mental State Examination (MMSE) and the Functional Activities Questionnaire (FAQ); meanwhile, the graph theory indices (involving global efficiency and degree) of the basal ganglia (involving the caudate, amygdala, and putamen) were also found to be closely correlated with MMSE scores. In ROC analyses of both FCD and graph theory, the amygdala was of the utmost importance in the early-stage detection of MCI; additionally, the caudate nucleus was found to be crucial in the progression of cognitive decline and AD diagnosis. (4) Conclusions: It was systematically confirmed that there is a phenomenon of change in the functional connections in the basal ganglia during cognitive decline. The findings of this study could improve our understanding of AD and MCI pathology in the basal ganglia and make it possible to propose new targets for AD treatment in further studies.

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“…We defined the bilateral hippocampus and striatum as regions of interest (ROI) based on prior literature investigating the neural basis of landmark and geometry-based navigation as well as place and response strategy use [7,25,29,35,50]. We observed the hippocampus to be implicated in all conditions, in varying degrees, and the striatum to be engaged solely during the geometry condition.…”

Section: Regions Of Interest Resultsmentioning

confidence: 99%

Selective neural coding of object, feature, and geometry spatial cues in humans

Ramanoël

Durteste

Bizeul

et al. 2021

Preprint

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Orienting in space requires the processing and encoding of visual spatial cues. The dominant hypothesis about the brain structures mediating the coding of spatial cues stipulates the existence of a hippocampal-dependent system for the representation of geometry and a striatal-dependent system for the representation of landmarks. However, this dual-system hypothesis is based on paradigms that presented spatial cues conveying either conflicting or ambiguous spatial information and that amalgamated the concept of landmark into both discrete 3D objects and wall features. These confounded designs introduce difficulties in interpreting the spatial learning process. Here, we test the hypothesis of a complex interaction between the hippocampus and the striatum during landmark and geometry visual coding in humans. We also postulate that object-based and feature-based navigation are not equivalent instances of landmark-based navigation as currently considered in human spatial cognition. We examined the neural networks associated with geometry-, object-, and feature-based spatial navigation in an unbiased, two-choice behavioral paradigm using fMRI. We showed evidence of a synergistic interaction between hippocampal and striatal coding underlying flexible navigation behavior. The hippocampus was involved in all three types of cue-based navigation, whereas the striatum was more strongly recruited in the presence of geometric cues than object or feature cues. We also found that unique, specific neural signatures were associated with each spatial cue. Critically, object-based navigation elicited a widespread pattern of activity in temporal and occipital regions relative to feature-based navigation. These findings challenge and extend the current view of a dual, juxtaposed hippocampal-striatal system for visual spatial coding in humans. They also provide novel insights into the neural networks mediating object vs. feature spatial coding, suggesting a need to distinguish these two types of landmarks in the context of human navigation.

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Threat-induced modulation of hippocampal and striatal memory systems during navigation of a virtual environment

Cited by 10 publications

References 73 publications

Using Virtual Reality to Study Spatial Mapping and Threat Learning

Using Virtual Reality to Study Spatial Mapping and Threat Learning

Altered Functional Connectivity of Basal Ganglia in Mild Cognitive Impairment and Alzheimer’s Disease

Selective neural coding of object, feature, and geometry spatial cues in humans

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