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The anatomical basis of functional localization in the cortex

Nature Reviews Neuroscience volume 3, pages 606–616 (2002)Cite this article

Key Points

  • The functions of a cortical area are determined by its extrinsic connections and intrinsic properties. Each cortical area has a unique pattern of cortico-cortical connections — a 'connectional fingerprint'.

  • No two areas share identical connection patterns. Instead, there are families of areas that share a resemblance in their connections.

  • Cortical areas also have their own 'functional fingerprints': the proportions of cells that fire in association with different tasks or task events differ between areas. The connectional fingerprint seems to underlie such cell-firing differences.

  • In addition to electrophysiological approaches, imaging will be a useful tool for detecting functional fingerprints, because it allows comparisons of activations across many cortical areas and across a wide range of tasks.

Abstract

The functions of a cortical area are determined by its extrinsic connections and intrinsic properties. Using the database CoCoMac, we show that each cortical area has a unique pattern of cortico-cortical connections — a 'connectional fingerprint'. We present examples of such fingerprints and use statistical analysis to show that no two areas share identical patterns. We suggest that the connectional fingerprint underlies the observed cell-firing differences between areas during different tasks. We refer to this pattern as a 'functional fingerprint' and present examples of such fingerprints. In addition to electrophysiological analysis, functional fingerprints can be determined by functional brain imaging. We argue that imaging provides a useful way to define such fingerprints because it is possible to compare activations across many cortical areas and across a wide range of tasks.

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Figure 1: Diagram of anatomical fingerprints for two prefrontal areas — Walker's areas 9 and 14.
Figure 2: Analysis of prefrontal connectivity.
Figure 3: Diagram of anatomical fingerprints for two premotor areas — F3 and F5.
Figure 4: Analysis of premotor connectivity.
Figure 5: Cell firing associated with a pair of visually and memory-guided tasks.
Figure 6: Functional fingerprints for five motor areas.

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Acknowledgements

This work was supported by the Wellcome Trust (R.E.P.), the Brain Research Trust (K.E.S.) and the Deutsche Forschungsgemeinschaft (R.K.). We are grateful to C. Hilgetag and K. Friston for their comments on the manuscript before submission, and to A. Duggins and W. Penny for helpful statistical discussions.

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Authors and Affiliations

  1. Department of Experimental Psychology, University of Oxford, South Parks Road, Oxford, OX1 3UD, UK

    Richard E. Passingham

  2. Wellcome Department of Imaging Neuroscience, Institute of Neurology, University College London, 12 Queen Square, London, WC1N 3BG, UK

    Richard E. Passingham & Klaas E. Stephan

  3. Institute for Medicine, Research Centre Jülich, Jülich, 52045, Germany

    Klaas E. Stephan

  4. Department of Psychology, University of Newcastle upon Tyne, Ridley Building, Claremont Place, Newcastle, NE1 7RU, UK

    Klaas E. Stephan

  5. C. & O. Vogt Brain Research Institute and Department of Morphological Endocrinology & Histochemistry, Heinrich-Heine-Universität Düsseldorf, Universitätsstr. 1, Düsseldorf, 40225, Germany

    Rolf Kötter

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  3. Rolf Kötter
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Correspondence to Richard E. Passingham.

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FURTHER INFORMATION

CoCoMac

Encyclopedia of Life Sciences

brain imaging: localization of brain functions

brain imaging: observing ongoing neural activity

computed tomography

magnetic resonance imaging

MIT Encyclopedia of Cognitive Sciences

cerebral cortex

cortical localization, history of

Lashley, Karl Spencer (1890–1958)

magnetic resonance imaging

positron emission tomography

Glossary

BETZ CELLS

Giant pyramidal neurons that are located in layer V of the primary motor cortex. Their axons project to the spinal cord, terminating directly on motor neurons.

MULTIDIMENSIONAL SCALING

A multivariate statistical method that provides a visual representation of the pattern of similarities between data sets. For example, given a matrix of similarities between various phenotypes, multidimensional scaling plots them on a map such that phenotypes that are perceived to be similar are placed near to each other, and those that are perceived to be different are placed far apart.

HIERARCHICAL CLUSTER ANALYSIS

A multivariate method for solving classification problems. The object is to sort items into groups such that the degree of association is strong between members of the same cluster and weak between members of different clusters. In addition, this technique visualizes the hierarchical structure of similarity between all identified clusters.

SPEARMAN CORRELATION MATRIX

A matrix of so-called Spearman correlation coefficients, each of which represents a measure of association between two sets of rank-ordered measurements.

STRYCHNINE NEURONOGRAPHY

A method in which (potentially polysynaptic) anatomical connections are identified by applying strychnine to one area and then recording spikes in other areas.

SET-RELATED ACTIVITY

Neuronal activity that reflects the behavioural 'set' of the animal, which can include information about a planned movement or about the state of readiness of the animal.

MULTIPLE CORRESPONDENCE ANALYSIS

A method that aims to explain the relationships between multiple variables that are identified on identical or different measurement scales, and may include categorical data.

GENERAL LINEAR MODEL

A general mathematical framework from which many commonly used statistical procedures (for example, analysis of variance) are derived.

INFORMATION THEORY

A scientific discipline that is concerned with mathematical laws underlying systems that transmit, store and process information. It also deals with the quantitative measurement of various types of information.

DIFFUSION-WEIGHTED IMAGING

A magnetic resonance imaging method that makes use of the variability in the random movement of water molecules in nervous tissue, which is restricted by cell bodies, blood vessels, axon bundles and other structures. Two opposite magnetic field gradients are applied. The magnetic spins will be de-phased by the first gradient and, because of water diffusion, the second gradient will not completely re-phase them. As the directionality of diffusion is highly ordered in white matter, the spatial orientation of the bundles can be reconstructed.

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Passingham, R., Stephan, K. & Kötter, R. The anatomical basis of functional localization in the cortex. Nat Rev Neurosci 3, 606–616 (2002). https://doi.org/10.1038/nrn893

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