Working memory (WM) is critical to many aspects of cognition, but it frequently fails. Much WM research has focused on capacity limits, but even for single, simple features, the fidelity of individual representations is limited. Why is this? One possibility is that, because of neural noise and interference, neural representations do not remain stable across a WM delay, nor do they simply decay, but instead, they may “drift” over time to a new, less accurate state. We tested this hypothesis in a functional magnetic resonance imaging study of a match/nonmatch WM recognition task for a single item with a single critical feature: orientation. We developed a novel pattern-based index of “representational drift” to characterize ongoing changes in brain activity patterns throughout the WM maintenance period, and we were successfully able to predict performance on the match/nonmatch recognition task using this representational drift index. Specifically, in trials where the target and probe stimuli matched, participants incorrectly reported more nonmatches when their activity patterns drifted away from the target. In trials where the target and probe did not match, participants incorrectly reported more matches when their activity patterns drifted toward the probe. On the basis of these results, we contend that neural noise does not cause WM errors merely by degrading representations and increasing random guessing; instead, one means by which noise introduces errors is by pushing WM representations away from the target and toward other meaningful (yet incorrect) configurations. Thus, we demonstrate that behaviorally meaningful drift within representation space can be indexed by neuroimaging.
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The Dynamic-Processing Model of Working Memory
Recent shifts in the understanding of how the mind and brain retain information in working memory (WM) call for revision to traditional theories. Evidence of dynamic, “activity-silent,” short-term retention processes diverges from conventional models positing that information is always retained in WM by sustained neural activity in buffers. Such evidence comes from machine-learning methods that can decode patterns of brain activity and the simultaneous administration of transcranial magnetic stimulation (TMS) to causally manipulate brain activity in specific areas and time points. TMS can “ping” brain areas to both reactivate latent representations retained in WM and affect memory performance. On the basis of these findings, I argue for a supplement to sustained retention mechanisms. Brain-decoding methods also reveal that dynamic levels of representational codes are retained in WM, and these vary according to task context, from perceptual (sensory) codes in posterior areas to abstract, recoded representations distributed across frontoparietal regions. A dynamic-processing model of WM is advanced to account for the overall pattern of results.
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- Award ID(s):
- 1848440
- NSF-PAR ID:
- 10180799
- Date Published:
- Journal Name:
- Current Directions in Psychological Science
- Volume:
- 29
- Issue:
- 4
- ISSN:
- 0963-7214
- Page Range / eLocation ID:
- 378 to 387
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract The emergence of distributed patterns of neural activity supporting brain functions and behavior can be understood by study of the brain’s low-dimensional topology. Functional neuroimaging demonstrates that brain activity linked to adaptive behavior is constrained to low-dimensional manifolds. In human participants, we tested whether these low-dimensional constraints preserve working memory performance following local neuronal perturbations. We combined multi-session functional magnetic resonance imaging, non-invasive transcranial magnetic stimulation (TMS), and methods translated from the fields of complex systems and computational biology to assess the functional link between changes in local neural activity and the reshaping of task-related low dimensional trajectories of brain activity. We show that specific reconfigurations of low-dimensional trajectories of brain activity sustain effective working memory performance following TMS manipulation of local activity on, but not off, the space traversed by these trajectories. We highlight an association between the multi-scale changes in brain activity underpinning cognitive function.
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null (Ed.)Relational integration is required when multiple explicit representations of relations between entities must be jointly considered to make inferences. We provide an overview of the neural substrate of relational integration in humans and the processes that support it, focusing on work on analogical and deductive reasoning. In addition to neural evidence, we consider behavioral and computational work that has informed neural investigations of the representations of individual relations and of relational integration. In very general terms, evidence from neuroimaging, neuropsychological, and neuromodulatory studies points to a small set of regions (generally left lateralized) that appear to constitute key substrates for component processes of relational integration. These include posterior parietal cortex, implicated in the representation of first-order relations (e.g., A:B); rostrolateral pFC, apparently central in integrating first-order relations so as to generate and/or evaluate higher-order relations (e.g., A:B::C:D); dorsolateral pFC, involved in maintaining relations in working memory; and ventrolateral pFC, implicated in interference control (e.g., inhibiting salient information that competes with relevant relations). Recent work has begun to link computational models of relational representation and reasoning with patterns of neural activity within these brain areas.more » « less
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Abstract Study Objectives Synchronization of neural activity within local networks and between brain regions is a major contributor to rhythmic field potentials such as the EEG. On the other hand, dynamic changes in microstructure and activity are reflected in the EEG, for instance slow oscillation (SO) slope can reflect synaptic strength. SO-spindle coupling is a measure for neural communication. It was previously associated with memory consolidation, but also shown to reveal strong interindividual differences. In studies, weak electric current stimulation has modulated brain rhythms and memory retention. Here, we investigate whether SO-spindle coupling and SO slope during baseline sleep are associated with (predictive of) stimulation efficacy on retention performance. Methods Twenty-five healthy subjects participated in three experimental sessions. Sleep-associated memory consolidation was measured in two sessions, in one anodal transcranial direct current stimulation oscillating at subjects individual SO frequency (so-tDCS) was applied during nocturnal sleep. The third session was without a learning task (baseline sleep). The dependence on SO-spindle coupling and SO-slope during baseline sleep of so-tDCS efficacy on retention performance were investigated. Results Stimulation efficacy on overnight retention of declarative memories was associated with nesting of slow spindles to SO trough in deep nonrapid eye movement baseline sleep. Steepness and direction of SO slope in baseline sleep were features indicative for stimulation efficacy. Conclusions Findings underscore a functional relevance of activity during the SO up-to-down state transition for memory consolidation and provide support for distinct consolidation mechanisms for types of declarative memories.more » « less
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Many daily activities and psychophysical experiments involve keeping multiple items in working memory. When items take continuous values (e.g., orientation, contrast, length, loudness) they must be stored in a continuous structure of appropriate dimensions. We investigate how this structure is represented in neural circuits by training recurrent networks to report two previously shown stimulus orientations. We find the activity manifold for the two orientations resembles a Clifford torus. Although a Clifford and standard torus (the surface of a donut) are topologically equivalent, they have important functional differences. A Clifford torus treats the two orientations equally and keeps them in orthogonal subspaces, as demanded by the task, whereas a standard torus does not. We find and characterize the connectivity patterns that support the Clifford torus. Moreover, in addition to attractors that store information via persistent activity, our networks also use a dynamic code where units change their tuning to prevent new sensory input from overwriting the previously stored one. We argue that such dynamic codes are generally required whenever multiple inputs enter a memory system via shared connections. Finally, we apply our framework to a human psychophysics experiment in which subjects reported two remembered orientations. By varying the training conditions of the RNNs, we test and support the hypothesis that human behavior is a product of both neural noise and reliance on the more stable and behaviorally relevant memory of the ordinal relationship between the two orientations. This suggests that suitable inductive biases in RNNs are important for uncovering how the human brain implements working memory. Together, these results offer an understanding of the neural computations underlying a class of visual decoding tasks, bridging the scales from human behavior to synaptic connectivity.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1177/0963721420922185
