Attention Stabilizes Representations in the Human Hippocampus

Aly, Mariam; Turk‐Browne, Nicholas B.

doi:10.1093/cercor/bhv041

Cited by 108 publications

(169 citation statements)

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“…Two recent human fMRI studies (16,17) have demonstrated that HPC representations, as evidenced in voxel activation patterns, are distinct for different task states. In these studies, searching through room images for a particular style of wall art evoked distinct HPC patterns relative to searching the same room images for a particular room layout.…”

Section: Discussionmentioning

confidence: 99%

“…First, HPC rapidly learns (13), an ability important for updating conceptual representations in the face of changing goals. Second, HPC has also been shown to activate representations that are goal relevant (14)(15)(16)(17)(18)(19). A critical open question is how the same experiences come to be represented differently in neural terms as a function of changing conceptual knowledge.…”

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confidence: 99%

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Dynamic updating of hippocampal object representations reflects new conceptual knowledge

Mack

Love

Preston

2016

Proc. Natl. Acad. Sci. U.S.A.

206

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Concepts organize the relationship among individual stimuli or events by highlighting shared features. Often, new goals require updating conceptual knowledge to reflect relationships based on different goal-relevant features. Here, our aim is to determine how hippocampal (HPC) object representations are organized and updated to reflect changing conceptual knowledge. Participants learned two classification tasks in which successful learning required attention to different stimulus features, thus providing a means to index how representations of individual stimuli are reorganized according to changing task goals. We used a computational learning model to capture how people attended to goal-relevant features and organized object representations based on those features during learning. Using representational similarity analyses of functional magnetic resonance imaging data, we demonstrate that neural representations in left anterior HPC correspond with model predictions of concept organization. Moreover, we show that during early learning, when concept updating is most consequential, HPC is functionally coupled with prefrontal regions. Based on these findings, we propose that when task goals change, object representations in HPC can be organized in new ways, resulting in updated concepts that highlight the features most critical to the new goal.category learning | attention | computational modeling | hippocampus | fMRI C oncepts are organizing principles that define how items or events are similar to one another. Goals are critical to shaping concepts, by emphasizing some shared features over others. When goals change, previously experienced events may be organized in new ways, resulting in an updated concept that highlights the features most critical to the new goal. For instance, consider purchasing a home. One must learn which features make for the most desirable home. A young couple seeking a cosmopolitan lifestyle may organize potential houses based on trendy features like exposed brick walls, a wet bar, and room for vintage record collections. However, with the news of a baby on the way, the couple's goals are likely to shift. After pouring through parenting books and web forums to learn what makes for a child-friendly home, they may look at those previously seen potential homes in a different light. Instead, family-oriented features such as whether or not a home has a bathtub, is within walking distance to a park, and is in a well-respected school district may matter more resulting in a reorganization of which homes are a good buy. At the core of this example are the fundamental challenges we face in flexible goaldirected learning. When learning new concepts (e.g., child-friendly instead of a trendy house), attention changes focus to different information and items that were conceptually dissimilar (e.g., two houses with and without a wet bar) may become more similar (e.g., they both are close to a park) and vice versa (1). Understanding how conceptual knowledge is created and updated during learning is a cen...

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Dynamic updating of hippocampal object representations reflects new conceptual knowledge

Mack

Love

Preston

2016

Proc. Natl. Acad. Sci. U.S.A.

206

248

View full text Add to dashboard Cite

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“…Such representational stability has been found in the hippocampus more generally, such as for olfactory representations when odor information is task-relevant (19). In humans, attention similarly modulates patterns of hippocampal activity, but over voxels measured with functional magnetic resonance imaging (fMRI); for example, attention to different kinds of information induces distinct activity patterns in all hippocampal subfields (10).…”

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confidence: 96%

“…Specifically, there is growing evidence that attention stabilizes distributed hippocampal representations of task-relevant information (10,13,14). For example, in rodents, distinct ensembles of hippocampal place cells activate when different spatial reference frames are task-relevant (15, 16; see also ref.…”

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confidence: 99%

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Attention promotes episodic encoding by stabilizing hippocampal representations

Aly

Turk‐Browne

2016

Proc. Natl. Acad. Sci. U.S.A.

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Attention influences what is later remembered, but little is known about how this occurs in the brain. We hypothesized that behavioral goals modulate the attentional state of the hippocampus to prioritize goal-relevant aspects of experience for encoding. Participants viewed rooms with paintings, attending to room layouts or painting styles on different trials during high-resolution functional MRI. We identified template activity patterns in each hippocampal subfield that corresponded to the attentional state induced by each task. Participants then incidentally encoded new rooms with art while attending to the layout or painting style, and memory was subsequently tested. We found that when task-relevant information was better remembered, the hippocampus was more likely to have been in the correct attentional state during encoding. This effect was specific to the hippocampus, and not found in medial temporal lobe cortex, category-selective areas of the visual system, or elsewhere in the brain. These findings provide mechanistic insight into how attention transforms percepts into memories.long-term memory | selective attention | hippocampal subfields | medial temporal lobe | representational stability W hy do we remember some things and not others? Consider a recent experience, such as the last movie complex you visited, flight you took, or restaurant at which you ate. More information was available to your senses than was stored in memory, such as the theater number of the movie, the faces of other passengers, and the color of the napkins. The selective nature of memory is adaptive, because encoding carries a cost: newly stored memories can interfere with existing ones and with our ability to learn new information in the future. What is the mechanism by which information gets selected for encoding?Attention offers a means of prioritizing information in the environment that is most relevant to behavioral goals. Attended information, in turn, has stronger control over behavior and is represented more robustly in the brain (1, 2). If attention gates which information we perceive and act upon, then it may also determine what information we remember. Indeed, attention during encoding affects both subsequent behavioral expressions of memory (3) and the extent to which activity levels in the brain predict memory formation (4-7). Although these findings suggest that attention modulates processes related to memory, how it does so is unclear.According to biased competition and other theories of attention (1, 8), task-relevant stimuli are more robustly represented in sensory systems, and thus fare better in competition with taskirrelevant stimuli for downstream processing. Indeed, there is extensive evidence that attention enhances overall activity in visual areas that represent attended vs. unattended features and locations (2, 9). Moreover, attention modulates cortical areas of the medial temporal lobe that provide input to the hippocampus (10-12).Attention can also modulate the hippocampus itself. Specifically, there is g...

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Neuronal effects of nicotine during auditory selective attention in schizophrenia

et al. 2015

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Although nicotine has been shown to improve attention deficits in schizophrenia, the neurobiological mechanisms underlying this effect are poorly understood. We hypothesized that nicotine would modulate attention-associated neuronal response in schizophrenia patients in the ventral parietal cortex (VPC), hippocampus, and anterior cingulate based on previous findings in control subjects. To test this hypothesis, the present study examined response in these regions in a cohort of nonsmoking patients and healthy control subjects using an auditory selective attention task with environmental noise distractors during placebo and nicotine administration. In agreement with our hypothesis, significant diagnosis (Control vs. Patient) X drug (Placebo vs. Nicotine) interactions were observed in the VPC and hippocampus. The interaction was driven by task-associated hyperactivity in patients (relative to healthy controls) during placebo administration, and decreased hyperactivity in patients after nicotine administration (relative to placebo). No significant interaction was observed in the anterior cingulate. Task-associated hyperactivity of the VPC predicted poor task performance in patients during placebo. Poor task performance also predicted symptoms in patients as measured by the Brief Psychiatric Rating Scale. These results are the first to suggest that nicotine may modulate brain activity in a selective attention-dependent manner in schizophrenia.

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Attention Stabilizes Representations in the Human Hippocampus

Cited by 108 publications

References 62 publications

Dynamic updating of hippocampal object representations reflects new conceptual knowledge

Dynamic updating of hippocampal object representations reflects new conceptual knowledge

Attention promotes episodic encoding by stabilizing hippocampal representations

Neuronal effects of nicotine during auditory selective attention in schizophrenia

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