An adaptive coding model of neural function in prefrontal cortex

Abstract

The prefrontal cortex has a vital role in effective, organized behaviour. Both functional neuroimaging in humans and electrophysiology in awake monkeys indicate that a fundamental principle of prefrontal function might be adaptive neural coding — in large regions of the prefrontal cortex, neurons adapt their properties to carry specifically information that is relevant to current concerns, producing a dense, distributed representation of related inputs, actions, rewards and other information. A model based on such adaptive coding integrates the role of the prefrontal cortex in working memory, attention and control. Adaptive coding points to new perspectives on several basic questions, including mapping of cognitive to neurophysiological functions, the influences of task content and difficulty, and the nature of frontal lobe specializations.

Key Points

  • The prefrontal cortex is crucial for effective, organized behaviour. On the basis of data from functional neuroimaging in humans and single-cell electrophysiology in the behaving monkey, this paper proposes an adaptive coding model of prefrontal function.

  • Functional imaging data show some specific associations between particular cognitive functions and local prefrontal activations. However, there is also strong evidence for common regions of recruitment in response to a wide range of different cognitive demands. These regions include the cortex in and around the posterior part of the inferior frontal sulcus, the frontal operculum/anterior insula and the dorsal part of the anterior cingulate.

  • Converging data come from electrophysiology in the monkey. Over large regions of the lateral frontal cortex, many cells show activity related to whatever arbitrary task a monkey has been trained to perform. These cells code many aspects of task events, including information relevant to stimuli, responses, working memory delays, response rules and reward states. Cells of many different types are found closely intermingled and widely distributed across the lateral surface. Even individual cells show evidence for adaptability of function, coding different information in different task contexts.

  • In the adaptive coding model, the central idea is that neurons throughout large regions of prefrontal cortex have the capacity to code many different types of information. In any given task context, neurons adapt to preserve only information of relevance to current behaviour. At the same time, they support the representation of related information elsewhere in the brain, including coding of relevant stimuli, responses, representations in semantic memory and reward states. This view links previous accounts of prefrontal function that are based on concepts of working memory, selective attention and control.

  • The model implies that, within the prefrontal cortex, regional specializations will be statistical rather than absolute. Neurons with the capacity to contribute to any given function might be widely distributed across the prefrontal cortex, although possibly with different distributions for different functions. This view of quantitative rather than qualitative specialization is consistent with data from electrophysiological, imaging and lesion studies. It suggests that conclusions concerning regional specialization will depend on criteria for assessing selectivity and, in imaging experiments, on experimental demand and power.

  • The adaptive coding model points to several key issues and approaches for future work. These include an assessment of long- and short-term adaptability, a quantitative comparison of cell properties between different prefrontal regions, and an investigation of how prefrontal adaptability differs from that in other cortical regions.

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Figure 1: 'General intelligence' reflects prefrontal function.
Figure 2: Prefrontal activations associated with five different cognitive demands.
Figure 3: Neural responses in macaque prefrontal cortex.
Figure 4: The adaptive coding model.

Change history

  • 27 March 2018

    This article was initially published with an incorrect DOI that did not match the registered version at Crossref. The DOI has been corrected in the article.

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Acknowledgements

I am grateful to E. Miller for his contribution to many of the ideas presented in this paper.

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DATABASES

MIT Encyclopedia of Cognitive Sciences

attention

hemispheric specialization

magnetic resonance imaging

positron emission tomography

working memory

Glossary

SPEEDED RESPONSE CHOICE

Tasks in which simple stimuli, such as lights or tones, call for speeded keypress or other responses.

EPISODIC MEMORY

The recollection of events in an autobiographical context.

EXECUTIVE FUNCTION

High-level processes that are proposed to organize and control cognitive function.

DIVIDED VISUAL ATTENTION

A requirement to process two or more simultaneous stimuli in a visual display.

CROSS-MODAL INTEGRATION

A requirement to combine information from different sensory modalities.

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