Joel L. Voss's research while affiliated with University of Chicago and other places
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Publications (149)
Hippocampal-dependent memory is thought to be supported by distinct connectivity states, with strong input to the hippocampus benefitting encoding and weak input benefitting retrieval. Previous research in rodents suggests that the hippocampal theta oscillation orchestrates the transition between these states, with opposite phase angles predicting...
Episodic memory often involves high overlap between the actors, locations, and objects of everyday events. Under some circumstances, it may be beneficial to distinguish, or differentiate, neural representations of similar events to avoid interference at recall. Alternatively, forming overlapping representations of similar events, or integration, ma...
Hippocampal memory function is thought to be supported by distinct connectivity states, with strong extrahippocampal input benefitting encoding and weak extrahippocampal input benefitting retrieval. Previous research in rodents suggests that the hippocampal theta oscillation orchestrates the transition between these states, with opposite phase angl...
Classical lesion studies led to a consensus that episodic and procedural memory arises from segregated networks identified with the hippocampus and the caudate nucleus, respectively. Neuroimaging studies, however, show that competitive and cooperative interactions occur between networks during memory tasks. Furthermore, causal experiments to manipu...
Adjacent regions of parietal cortex are thought to affiliate with distinct large-scale networks and thereby make different contributions to memory formation. We directly tested this putative functional segregation within parietal cortex by perturbing activity of anterior versus posterior parietal areas. We applied noninvasive theta-burst transcrani...
Damage to specific brain circuits can cause specific neuropsychiatric symptoms. Therapeutic stimulation to these same circuits may modulate these symptoms. To determine whether these circuits converge, we studied depression severity after brain lesions (n = 461, five datasets), transcranial magnetic stimulation (n = 151, four datasets) and deep bra...
Memory neuroscientists often measure neural activity during task trials designed to recruit specific memory processes. Behavior is championed as crucial for deciphering brain–memory linkages but is impoverished in typical experiments that rely on summary judgments. We criticize this approach as being blind to the multiple cognitive, neural, and beh...
Episodic memory is supported by hippocampal interactions with a distributed network. Aging is associated with memory decline and network de-differentiation. However, the role of de-differentiation in memory decline has not been directly tested. We reasoned that hippocampal network-targeted stimulation could test these theories, as age-related chang...
The power and precision with which humans link language to cognition is unique to our species. By 3–4 months of age, infants have already established this link: simply listening to human language facilitates infants’ success in fundamental cognitive processes. Initially, this link to cognition is also engaged by a broader set of acoustic stimuli, i...
Although the human hippocampus is necessary for long-term memory, controversial findings suggest that it may also support short-term memory in the service of guiding effective behaviors during learning. We tested the counterintuitive theory that the hippocampus contributes to long-term memory through remarkably short-term processing, as reflected i...
This handbook is currently in development, with individual articles publishing online in advance of print publication. At this time, we cannot add information about unpublished articles in this handbook, however the table of contents will continue to grow as additional articles pass through the review process and are added to the site. Please note...
Substantial evidence implicates the hippocampus and its coordination with a distributed network of interconnected brain areas as being essential for episodic memory, our memory for past events. Motivated by findings that the effects of transcranial magnetic stimulation (TMS) are conducted throughout stimulated networks, recent experiments have succ...
Episodic memory involves the reinstatement of distributed patterns of brain activity present when events were initially experienced. The hippocampus is thought to coordinate reinstatement via its interactions with a network of brain regions, but this hypothesis has not been causally tested in humans. The current study directly tested the involvemen...
During mammalian evolution, primate neocortex expanded, shifting hippocampal functional networks away from primary sensory cortices, towards association cortices. Reflecting this rerouting, whereas rodent resting functional hippocampal networks include primary sensory cortices, those in humans preferentially include higher association cortices. Res...
When direct experience is unavailable, animals and humans can imagine or infer the future to guide decisions. Behavior based on direct experience versus inference may recruit partially distinct brain circuits. In rodents, the orbitofrontal cortex (OFC) contains neural signatures of inferred outcomes, and OFC is necessary for behavior that requires...
Although the human hippocampus is necessary for long-term memory, controversial findings suggest that hippocampal computations support short-term memory in the service of guiding effective behaviors during learning. We tested the counterintuitive theory that the hippocampus contributes to long-term memory through remarkably short-term processing, a...
Memories for episodes are temporally structured. Cognitive models derived from list-learning experiments attribute this structure to the retrieval of temporal context information that indicates when a memory occurred. These models predict key features of memory recall, such as the strong tendency to retrieve studied items in the order in which they...
The human cerebellum is thought to interact with distributed brain networks to support cognitive abilities such as episodic memory and semantic prediction. Hippocampal and fronto-temporo-parietal networks that respectively support episodic memory versus semantic prediction have been associated with distinct endogenous oscillatory activity frequency...
Episodic memory involves the reinstatement of distributed patterns of brain activity present when events were initially experienced. The hippocampus is thought to coordinate reinstatement via its interactions with a network of brain regions, but this hypothesis has not been causally tested in humans. The current study directly tested the involvemen...
The hippocampus supports episodic memory via interaction with a distributed brain network. Previous experiments using network-targeted noninvasive brain stimulation have identified episodic memory enhancements and modulation of activity within the hippocampal network. However, mechanistic insights were limited because these effects were measured lo...
Decisions are typically guided by what we have experienced in the past. However, when direct experience is unavailable, animals and humans can imagine or infer the future to make choices. Outcome expectations that are based on direct experience and inference may compete for guiding behavior [1, 2], and they may recruit distinct but overlapping brai...
Episodic memory depends on the hippocampus and its coordination with a distributed network of interconnected brain areas. Recent findings indicate that the function of this network can be altered using network-targeted transcranial magnetic stimulation (TMS). These stimulation experiments have identified increases in episodic memory and the network...
The hippocampus supports episodic memory via interaction with a distributed brain network. Previous experiments using network-targeted noninvasive brain stimulation have identified episodic memory enhancements and modulation of activity within the hippocampal network. However, mechanistic insights were limited because these effects were measured lo...
The cerebellum is thought to interact with distributed brain networks to support cognitive abilities such as episodic memory and language. Episodic memory and language networks have been associated with distinct endogenous oscillatory activity frequency bands: theta (~3-8 Hz) versus beta (~13-30 Hz), respectively. We sought to test whether it is po...
Outcome-guided behavior requires knowledge about the current value of expected outcomes. Such behavior can be isolated in the reinforcer devaluation task, which assesses the ability to infer the current value of specific rewards after devaluation. Animal lesion studies demonstrate that orbitofrontal cortex (OFC) is necessary for normal behavior in...
Introduction:
The distributed cortical network of the human hippocampus is important for episodic memory. In a previous experiment, noninvasive stimulation of the hippocampal-cortical network applied for five consecutive days improved paired-associate learning measured after the stimulation regimen via cued recall (Wang et al., Science, 2014, 345,...
Successful episodic memory involves dynamic increases in activity across distributed hippocampal networks, including the posterior-medial (PMN) and the anterior-temporal (ATN) networks. We tested whether this up-regulation of functional connectivity during memory processing can be enhanced within hippocampal networks by noninvasive stimulation, and...
The striatum and medial temporal lobes (MTL) exhibit dissociable roles during learning. Whereas the striatum and its network of thalamic relays and cortical nodes are necessary for nondeclarative learning, the MTL and associated network are required for declarative learning. Several studies have suggested that these networks are functionally compet...
Wang et al. (2014) found that that five daily sessions of repetitive transcranial magnetic stimulation (rTMS) of the posterior parietal cortex (PPC) significantly increased functional connectivity (FC) in a network centered on the hippocampus, and caused a correlated increase in memory performance. However, this finding has not been reproduced inde...
The processing of emotional facial expressions is important for social functioning and is influenced by environmental factors, including early environmental experiences. Low socio-economic status (SES) is associated with greater exposure to uncontrollable stressors, including violence, as well as deprivation, defined as a lack or decreased complexi...
Outcome-guided behavior requires knowledge about the current value of expected outcomes. Such behavior can be isolated in the reinforcer devaluation task, which assesses the ability to infer the current value of rewards after devaluation. Animal lesion studies demonstrate that orbitofrontal cortex (OFC) is necessary for normal behavior in this task...
Declarative memory is supported by distributed brain networks in which the medial-temporal lobes (MTLs) and pFC serve as important hubs. Identifying the unique and shared contributions of these regions to successful memory performance is an active area of research, and a growing literature suggests that these structures often work together to suppo...
Background:
Focal brain lesions can lend insight into the causal neuroanatomical substrate of depression in the human brain. However, studies of lesion location have led to inconsistent results.
Methods:
Five independent datasets with different lesion etiologies and measures of postlesion depression were collated (N = 461). Each 3-dimensional le...
Successful episodic memory involves dynamic increases in the coordination of activity across distributed hippocampal networks, including the posterior-medial network (PMN) and the anterior-temporal network (ATN). We tested whether this up-regulation of functional connectivity during memory processing can be enhanced within hippocampal networks by n...
[This corrects the article DOI: 10.1371/journal.pone.0210167.].
Objective:
To test whether targeting hippocampal-cortical brain networks with high-frequency transcranial magnetic stimulation in older adults influences behavioral and neural measures characteristic of age-related memory impairment.
Methods:
Fifteen adults aged 64 to 80 years (mean = 72 years) completed a single-blind, sham-controlled experimen...
Novel approaches to address cognitive aging and to delay or prevent cognitive decline in older individuals will require a better understanding of the biological and environmental factors that contribute to it. Studies in animal models-in particular, animals whose cognitive trajectory across their life span closely tracks that of humans-can provide...
Background
The prefrontal cortex has been implicated in episodic memory and the awareness of memory. Few studies have probed the nature and necessity of its role via brain stimulation. There are uncertainties regarding whether the hemisphere of stimulation predicts effects on memory and whether effects of stimulation are format‐specific, with most...
Connectivity matrix of 30 subjects using simple correlation without mean signal correction.
For some subjects, task-positive and task-negative networks were observed, as apparent by their anti-correlation (i.e., upper-left and lower-right of each graph). However, global BOLD signal fluctuation potentially positively biased correlation between ROIs...
Episodic memory is thought to involve functional interactions of large-scale brain networks that dynamically reconfigure depending on task demands. Although the hippocampus and closely related structures have been implicated, little is known regarding how large-scale and distributed networks support different memory formation demands. We investigat...
Comparison of two methods for identifying modular structure.
The probabilistic method was superior to the conventional averaging method in terms of its ability to identify modules with interactions that were significantly correlated with memory task performance. Modules were also more visually apparent when identified with the probabilistic method...
Activation map of task-positive and task-negative responses.
Supplementary activation map to Fig 3 showing the spatial distribution of the task-positive and the task-negative networks. We used a lenient voxel-wise P < 0.05 for network construction and thus make no statistical significance of this activation map. Brain images with activation maps we...
An example showing how anatomical ROIs were separated into two functional ROIs.
This example frontal region defined by anatomical atlas included both of task-positive (red) and task-negative (blue) voxels. The region in green was discarded because the voxels are neither of task-positive or task-negative i.e., t(29) > 0.05, with the regions that wer...
Connectivity matrix of 30 subjects using partial correlation controlling the mean signal.
The positively biased correlation was reduced by controlling the mean signal. The task-positive and the task-negative networks were more apparent in every subject when partial correlation controlling mean signal was used versus simple correlation (S1 Fig).
(TI...
Distribution of connectivity across all the nodes, conditions (object-scene and object-location tasks), and subjects.
(A) Distribution of simple correlation values. (B) Distribution of the same values but with partial correlation used to control the mean network component signal.
(TIFF)
Episodic memory is thought to rely on interactions of the hippocampus with other regions of the distributed hippocampal‐cortical network (HCN) via interregional activity synchrony in the theta frequency band. We sought to causally test this hypothesis using network‐targeted transcranial magnetic stimulation. Healthy humans participants completed fo...
Successful memory is normally accompanied by explicit awareness of retrieval and confidence in the accuracy of the retrieval product. Prior findings suggest that these features of metamemory can be dissociated from retrieval accuracy in Amnestic Mild Cognitive Impairment (aMCI). However, the literature on this question contains variable and conflic...
Posterior-medial and anterior-temporal cortical networks interact with the hippocampus and are thought to distinctly support episodic memory. We causally tested this putative distinction by determining whether targeted noninvasive stimulation could selectively affect neural signals of memory formation within the posterior-medial network. Stimulatio...
Successful episodic recollection can vary in the precision of the information recalled. The hypothesis that recollection precision requires functional neuroanatomical contributions distinct from those required for recollection success remains controversial. Some findings in individuals with hippocampal lesions have indicated that precision is depen...
Covert scene configuration memory test and stimuli example. (A) Example study block (top) and test block trials (bottom). During the test portion of this task, participants viewed a series of 12 scenes for 8 seconds and were asked to rate how well they thought they learned that scene; ISIs were randomized between scenes. During the test portion, pa...
Nearly three out of four survivors experience Cancer-Related Cognitive Impairment (CRCI) for months or years following treatment. Both clinical and animal studies point to the hippocampus as a likely brain region affected in CRCI, however no previous study has investigated the functional connectivity of the hippocampus in CRCI. We compared hippocam...
Autobiographical memory retrieval is associated with activity of a distributed network that is similar to the default‐mode network (DMN) identified via activity correlations measured during rest. We tested whether activity correlations could be used to identify the autobiographical network during extended bouts of retrieval. Global‐correlativity an...
Dorsolateral prefrontal cortex (DLPFC) is thought to organize items in working memory and this organizational role may also influence long-term memory. To causally test this hypothesized role of DLPFC in long-term memory formation, we used θ-burst noninvasive stimulation (TBS) to modulate DLPFC involvement in a memory task that assessed the influen...
A comprehensive understanding of human memory requires both cognitive and neural descriptions of memory processes along with theories of how memory processing drives behavioral responses and subjective experiences. The electrophysiological approaches described here are highly suitable for progressing toward these goals. In particular, event-related...
BACKGROUND
Patients with brain tumors often suffer from memory impairment, a symptom that results in a significant decrement to quality of life. However, unlike sensorimotor and language functions, memory is not mapped during awake craniotomies. Following on research showing that long-term memory processes are operative and can be measured over com...
Current interpretations of hippocampal memory function are blind to the fact that viewing behaviors are pervasive and complicate the relationships among perception, behavior, memory, and brain activity. For example, hippocampal activity and associative memory demands increase with stimulus complexity. Stimulus complexity also strongly modulates vie...
Memory can profoundly influence new learning, presumably because memory optimizes exploration of to-be-learned material. Although hippocampus and frontoparietal networks have been implicated in memory-guided exploration, their specific and interactive roles have not been identified. We examined eye movements during fMRI scanning to identify neural...
Primary progressive aphasia (PPA) is clinically defined by an initial loss of language function and preservation of other cognitive abilities, including episodic memory. While PPA primarily affects the left-lateralized perisylvian language network, some clinical neuropsychological tests suggest concurrent initial memory loss. The goal of this study...
Cancer survivors have lingering cognitive problems, however the anatomical basis for these problems has yet to be fully elucidated. Clinical studies as well as animal models of chemotherapy have pinpointed cell and volume loss to the hippocampus, however, few studies have performed shape analysis of the hippocampus on cancer survivors. This study u...
The hippocampus is crucial for long-term memory; its involvement in short-term or immediate expressions of memory is more controversial. Rodent hippocampus has been implicated in an expression of memory that occurs on-line during exploration termed "vicarious trial-and-error" (VTE) behavior. VTE occurs when rodents iteratively explore options durin...
Episodic memory is thought to critically depend on interaction of the hippocampus with distributed brain regions [1-3]. Specific contributions of distinct networks have been hypothesized, with the hippocampal posterior-medial (HPM) network implicated in the recollection of highly precise contextual and spatial information [3-6]. Current evidence fo...
Background:
Threat-related attention bias relates to anxiety and posttraumatic stress symptoms in adults and adolescents, but few longitudinal studies examine such associations in young children. This study examines prospective relations among attention bias, trauma exposure, and anxiety and trauma symptoms in a sample previously reported to manif...
Early-life stress (ELS) exposure is associated with adverse outcomes across the lifespan. We examined the relation of ELS exposure to resting-state fMRI in children ages 4 to 7 years. ELS in the first years of life, but not concurrent, was associated with higher regional homogeneity of resting-state fMRI in the left lateral frontal cortex. Resting-...
Introduction:
Callous-unemotional (CU) traits in the presence of conduct problems are associated with increased risk of severe antisocial behavior. Developmentally sensitive methods of assessing CU traits have recently been generated, but their construct validity in relation to neurocognitive underpinnings of CU has not been demonstrated. The curr...
Expression of learned stimulus-reward associations based on context is essential for regulation of behavior to meet situational demands. Contextual regulation improves during development, although the developmental progression of relevant neural and cognitive processes is not fully specified. We therefore measured neural correlates of flexible, con...
Background:
Delirium symptoms are associated with later worse functional outcomes and long-term cognitive impairments, but the neuroanatomical basis for delirium symptoms in patients with acute brain injury is currently uncertain. We tested the hypothesis that hematoma location is predictive of delirium symptoms in patients with intracerebral hemo...
Background:
Patients who receive adjuvant chemotherapy have reported cognitive impairments that may last for years after the completion of treatment. Working memory-related and long-term memory-related changes in this population are not well understood. The objective of this study was to demonstrate that cancer-related cognitive impairments are as...
Of the many elements that comprise an episode, are any disproportionately bound to the others? We tested whether active short-term retrieval selectively increases binding. Individual objects from multiobject displays were retrieved after brief delays. Memory was later tested for the other objects. Cueing with actively retrieved objects facilitated...
The importance of dimensional approaches is widely recognized, but an empirical base for clinical application is lacking. This is particularly true for irritability, a dimensional phenotype that cuts across many areas of psychopathology and manifests early in life. We examine longitudinal, dimensional patterns of irritability and their clinical imp...
Eye movement trajectories during a verbally cued object search task were used as probes of lexico-semantic associations in an anomic patient with primary progressive aphasia. Visual search was normal on trials where the target object could be named but became lengthy and inefficient on trials where the object failed to be named. The abnormality was...
