Persistent activity in the prefrontal cortex during working memory

doi:10.1016/S1364-6613(03)00197-9

Trends in Cognitive Sciences

Volume 7, Issue 9, September 2003, Pages 415-423

https://doi.org/10.1016/S1364-6613(03)00197-9 Get rights and content

Abstract

The dorsolateral prefrontal cortex (DLPFC) plays a crucial role in working memory. Notably, persistent activity in the DLPFC is often observed during the retention interval of delayed response tasks. The code carried by the persistent activity remains unclear, however. We critically evaluate how well recent findings from functional magnetic resonance imaging studies are compatible with current models of the role of the DLFPC in working memory. These new findings suggest that the DLPFC aids in the maintenance of information by directing attention to internal representations of sensory stimuli and motor plans that are stored in more posterior regions.

Section snippets

Representations and operations

Understanding PFC functions is likely to hinge on our ability to resolve the nature of stored representations in addition to the types of operations performed on such representations necessary for guiding behavior [13]. Representations are symbolic codes for information stored either transiently or permanently in neuronal networks. Operations are processes or computations performed on representations. Models of working memory 1, 14 and models of PFC function 15, 16, 17, 18, 19, 20, 21 vary

Models of dorsolateral prefrontal cortical function

Founded on experimental lesion and unit recording data in awake-behaving monkeys, Goldman-Rakic formalized her highly influential theory of PFC function [17]. In this model, lesions of area 46 in the DLPFC impair the ability to maintain on-line sensory representations that are no longer present in the environment but are necessary for adaptive performance. Damage to the DLPFC results in the forgetting of relevant information. Persistent delay-period activity reflects the temporary storage of

Evidence from fMRI studies

To test whether the DLPFC supports maintained representations and/or control operations, fMRI has been used to detect and characterize persistent delay period activity during delayed response type tasks. We will now review key studies that address the role of the DLPFC in working memory. We exclusively focus on recent fMRI studies that employed event-related designs because blocked designs cannot isolate the component processes (e.g. maintenance) of working memory [32] (see Box 2).

Durability

If the delay period activity reflects the stored representation, then one might expect that the activity should endure throughout the entire length of the retention interval until it can be used to guide a response. This is exactly what has been reported now several times in unit recordings in the PFC of monkeys 5, 6, 7, 28, 33, 39. A few event-related fMRI studies have varied the length of the retention delay up to 24 s and have reported that the DLPFC activity does indeed span the entire

Selection processes

Recently, in a series of fMRI studies, Rowe and Passingham have begun to challenge the notion that the DLPFC represents or stores information in memory 46, 47, 48. Instead, they have emphasized its role in selection, the process of choosing among the most task-relevant internal representations. In these studies, area 46 of the DLPFC was active when the appropriate location being maintained was selected for response, but not during a memory delay interval (Fig. 3). Null effects with fMRI, just

Atop the motor hierarchy

One possible way to reconcile many of the findings that we have discussed thus far is a greater and renewed appreciation that the prefrontal cortex is a motor area; it sits at the apex of the motor hierarchy and most probably evolved from more posterior motor areas that are phylogenetically older. Fuster, and others, argue that the PFC is especially important for the selection, planning, and execution of motor behavior 21, 27. All delayed response tasks in monkey and human, require an action to

Focusing on selection

Persistent neural activity has been observed in many cortical and subcortical regions of the brain, notably in the PFC, during the retention intervals of delayed response tasks. Such activity might reflect the active representation of some past item, future motor plan, or abstract rule that one is actively remembering. As of yet, we have not been able to identify what this persistent activity represents and the nature of the code is likely to differ across different brain regions. Regardless,

Conclusions

The role of the DLPFC in cognition seems at first glance to involve a varied collection of processes [69]. Many behaviors are impacted by damage [70] and a variety of tasks activate it. However, the key to a more unified role of the DLPFC in cognition could lie in its connectivity with other regions [71]. The exact same top-down signal from the DLPFC could have very different behavioral expressions depending on the recipients of the signal. In that sense, the DLPFC is performing the same

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Trends in Cognitive Sciences

Persistent activity in the prefrontal cortex during working memory

Abstract

Section snippets

Representations and operations

Models of dorsolateral prefrontal cortical function

Evidence from fMRI studies

Durability

Selection processes

Atop the motor hierarchy

Focusing on selection

Conclusions

Neuropsychologia

Neuropsychologia

Neuron

Neuroimage

Neuropsychologia

Brain Res. Cogn. Brain Res.

Neuron

Neuron

Neuroimage

Neuroimage

Brain Res. Cogn. Brain Res.

Neuroimage

Trends Cogn. Sci.

Neuroimage

Trends Neurosci.

Trends Neurosci.

Delayed-matching and delayed-response deficit from cooling dorsolateral prefrontal cortex in monkeys

J. Comp. Physiol. Psychol.

Dorsolateral prefrontal lesions and oculomotor delayed-response performance: evidence for mnemonic “scotomas”

J. Neurosci.

Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex

J. Neurophysiol.

Neuron activity related to short-term memory

Science

Prefrontal cortical unit activity and delayed alternation performance in monkeys

J. Neurophysiol.

Neural mechanisms of visual working memory in prefrontal cortex of the macaque

J. Neurosci.

Lateral prefrontal syndrom: a disorder of executive control

Contributions of subregions of the prefrontal cortex to working memory: evidence from brain lesions in humans

J. Cogn. Neurosci.

Segregation of areas related to visual working memory in the prefrontal cortex revealed by rTMS

Cereb. Cortex

Human prefrontal cortex: processing and representational perspectives

Nat. Rev. Neurosci.

Working Memory

Prefrontal cortical contributions to working memory: evidence from event-related fMRI studies

Exp. Brain Res.

Circuitry of primate prefrontal cortex and regulation of behavior by representational memory

The prefrontal cortex and cognitive control

Nat. Rev. Neurosci.

An integrative theory of prefrontal cortex function

Annu. Rev. Neurosci.

The role of the mid-dorsolateral prefrontal cortex in working memory

Exp. Brain Res.

The Frontal Lobes and Voluntary Action

The domain of supervisory processes and temporal organization of behaviour

Philos. Trans. R. Soc. Lond. B Biol. Sci

Storage and executive processes in the frontal lobes

Science

The sensory nature of mnemonic representation in the primate prefrontal cortex

Nat. Neurosci.

Matching patterns of activity in primate prefrontal area 8a and parietal area 7ip neurons during a spatial working memory task

J. Neurophysiol.