Optimal information loading into working memory in prefrontal cortex

Working memory involves the short-term maintenance of information and is critical in many tasks. The neural circuit mechanisms underlying this information maintenance are thought to rely on persistent activities resulting from attractor dynamics. However, how information is loaded into working memory for subsequent maintenance remains poorly understood. A pervasive assumption is that information loading requires inputs that are similar to the persistent activities expressed during maintenance. Here, we show through mathematical analysis and numerical simulations that optimal inputs are instead largely orthogonal to persistent activities and naturally generate the rich transient dynamics that are characteristic of prefrontal cortex (PFC) during working memory. By analysing recordings from monkeys performing a memory-guided saccade task, and using a novel, theoretically principled metric, we show that PFC exhibits the hallmarks of optimal information loading. Our theory unifies previous, seemingly conflicting theories of memory maintenance based on attractor or purely sequential dynamics, and reveals a normative principle underlying the widely observed phenomenon of dynamic coding in PFC. These results suggest that optimal information loading may be a key component of attractor dynamics characterising various cognitive functions and cortical areas, including long-term memory and navigation in the hippocampus, and decision making in the PFC.

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Faculty Opinions recommendation of Bump attractor dynamics in prefrontal cortex explains behavioral precision in spatial working memory.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.718262129.793494533 ◽

2014 ◽

Author(s):

Nicolas Brunel ◽

Elisa Tartaglia

Keyword(s):

Working Memory ◽

Prefrontal Cortex ◽

Spatial Working Memory ◽

Attractor Dynamics

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The role of prefrontal cortex in working memory: examining the contents of consciousness

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.1998.0334 ◽

1998 ◽

Vol 353 (1377) ◽

pp. 1819-1828 ◽

Cited By ~ 159

Author(s):

◽

S. M. Courtney ◽

L. Petit ◽

J. V. Haxby ◽

L. G. Ungerleider

Keyword(s):

Working Memory ◽

Prefrontal Cortex ◽

Visual Processing ◽

Right Hemisphere ◽

Functional Organization ◽

Spatial Working Memory ◽

Domain Specificity ◽

Long Term Memory ◽

Present Evidence ◽

The Right

Working memory enables us to hold in our ‘mind's eye’ the contents of our conscious awareness, even in the absence of sensory input, by maintaining an active representation of information for a brief period of time. In this review we consider the functional organization of the prefrontal cortex and its role in this cognitive process. First, we present evidence from brain–imaging studies that prefrontal cortex shows sustained activity during the delay period of visual working memory tasks, indicating that this cortex maintains on–line representations of stimuli after they are removed from view. We then present evidence for domain specificity within frontal cortex based on the type of information, with object working memory mediated by more ventral frontal regions and spatial working memory mediated by more dorsal frontal regions. We also propose that a second dimension for domain specificity within prefrontal cortex might exist for object working memory on the basis of the type of representation, with analytic representations maintained preferentially in the left hemisphere and image–based representations maintained preferentially in the right hemisphere. Furthermore, we discuss the possibility that there are prefrontal areas brought into play during the monitoring and manipulation of information in working memory in addition to those engaged during the maintenance of this information. Finally, we consider the relationship of prefrontal areas important for working memory, both to posterior visual processing areas and to prefrontal areas associated with long–term memory.

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Stable population coding for working memory coexists with heterogeneous neural dynamics in prefrontal cortex

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1619449114 ◽

2016 ◽

Vol 114 (2) ◽

pp. 394-399 ◽

Cited By ~ 128

Author(s):

John D. Murray ◽

Alberto Bernacchia ◽

Nicholas A. Roy ◽

Christos Constantinidis ◽

Ranulfo Romo ◽

...

Keyword(s):

Working Memory ◽

Prefrontal Cortex ◽

Neural Circuit ◽

Temporal Dynamics ◽

Population Level ◽

Population Coding ◽

Neural Dynamics ◽

Stable Population ◽

Neuron Activity ◽

Delayed Response

Working memory (WM) is a cognitive function for temporary maintenance and manipulation of information, which requires conversion of stimulus-driven signals into internal representations that are maintained across seconds-long mnemonic delays. Within primate prefrontal cortex (PFC), a critical node of the brain’s WM network, neurons show stimulus-selective persistent activity during WM, but many of them exhibit strong temporal dynamics and heterogeneity, raising the questions of whether, and how, neuronal populations in PFC maintain stable mnemonic representations of stimuli during WM. Here we show that despite complex and heterogeneous temporal dynamics in single-neuron activity, PFC activity is endowed with a population-level coding of the mnemonic stimulus that is stable and robust throughout WM maintenance. We applied population-level analyses to hundreds of recorded single neurons from lateral PFC of monkeys performing two seminal tasks that demand parametric WM: oculomotor delayed response and vibrotactile delayed discrimination. We found that the high-dimensional state space of PFC population activity contains a low-dimensional subspace in which stimulus representations are stable across time during the cue and delay epochs, enabling robust and generalizable decoding compared with time-optimized subspaces. To explore potential mechanisms, we applied these same population-level analyses to theoretical neural circuit models of WM activity. Three previously proposed models failed to capture the key population-level features observed empirically. We propose network connectivity properties, implemented in a linear network model, which can underlie these features. This work uncovers stable population-level WM representations in PFC, despite strong temporal neural dynamics, thereby providing insights into neural circuit mechanisms supporting WM.

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Bump attractor dynamics in prefrontal cortex explains behavioral precision in spatial working memory

Nature Neuroscience ◽

10.1038/nn.3645 ◽

2014 ◽

Vol 17 (3) ◽

pp. 431-439 ◽

Cited By ~ 182

Author(s):

Klaus Wimmer ◽

Duane Q Nykamp ◽

Christos Constantinidis ◽

Albert Compte

Keyword(s):

Working Memory ◽

Prefrontal Cortex ◽

Spatial Working Memory ◽

Attractor Dynamics

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Prefrontal Cortex Activity Associated with Source Monitoring in a Working Memory Task

Journal of Cognitive Neuroscience ◽

10.1162/0898929041502724 ◽

2004 ◽

Vol 16 (6) ◽

pp. 921-934 ◽

Cited By ~ 76

Author(s):

Karen J. Mitchell ◽

Marcia K. Johnson ◽

Carol L. Raye ◽

Erich J. Greene

Keyword(s):

Working Memory ◽

Prefrontal Cortex ◽

Source Monitoring ◽

Memory Task ◽

Long Term Memory ◽

Source Information ◽

Related Activity ◽

Specific Source ◽

Evaluative Processes

Using functional magnetic resonance imaging (fMRI), we investigated prefrontal cortex (PFC) activity during remembering specific source information (format, location judgments) versus remembering that could be based on undifferentiated information, such as familiarity (old/new recognition [ON], recency judgments). A working memory (WM) paradigm with an immediate test yielded greater activation in the lateral PFC for format and location source memory (SM) tasks than ON recognition; this SM-related activity was left lateralized. The same regions of PFC were recruited in Experiment 2 when information was tested immediately and after a filled delay. Substituting recency for location judgments (Experiment 3) resulted in an overall shift in task context that produced greater right PFC activity associated with ON and recency tasks compared to the format task, in addition to left SM-related activity. These data extend to WM previous findings from long-term memory (LTM) indicating that the left and right PFC may be differentially involved in memory attributions depending on the specificity of information evaluated. The findings also provide evidence for the continuity of evaluative processes recruited in WM and LTM.

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How does the attentional pointer work in prefrontal cortex?

Behavioral and Brain Sciences ◽

10.1017/s0140525x03460160 ◽

2003 ◽

Vol 26 (6) ◽

pp. 751-751

Author(s):

Naoyuki Osaka

Keyword(s):

Working Memory ◽

Prefrontal Cortex ◽

Current Model ◽

Event Related Potential ◽

Anterior Cingulate ◽

Long Term Memory ◽

Connectivity Analysis ◽

Firm Model

The current model, based on event-related potential (ERP) studies, posits that the working-memory system is a state of activated long-term memory; this appears comprehensive, but it needs further detailed analysis of functional neural connectivity analysis within the prefrontal cortex (PFC) and between the posterior and prefrontal cortex. Specifically, the role of dorsolateral PFC and anterior cingulate cortex (ACC) is probably critical for PFC's attentional controller. Neural implementation of the executive function in working memory appears critical to build a firm model.

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