Structural divisions and functional fields in the human cerebral cortex¹

Abstract

The question of what is a cortical area needs a thorough definition of borders both in the microstructural and the functional domains. Microstructural parcellation of the human cerebral cortex should be made on multiple criteria based on quantitative measurements of microstructural variables, such as neuron densities, neurotransmitter receptor densities, enzyme densities, etc. Because of the inter-individual variations of extent and topography of microstructurally defined areas, the final microstructurally defined areas appear as population maps. In the functional domain, columns, patches and blobs signifying synaptically active parts of the cortex appear as cortical functional fields. These fields are the largest functional entities of the cerebral cortex according to the cortical field hypothesis. In its strong version, the cortical field hypothesis postulates that all neurons and synapses within the fields perform a co-operative computation. A number of such fields together provide the functional contribution of the cerebral cortex. The functional parcellation of the human cerebral cortex must be based on field population maps, which after intersection analysis appear as functional domains. The major structural–functional hypothesis to be examined is whether these functional domains are equi-territorial to the microstructurally defined meta-maps. The cortical hypothesis predicts that, if two brain tasks make use of one or several identical or largely overlapping fields, they cannot be performed simultaneously without errors or increases in latency. Evidence for such interference is presented. This evidence represents a restriction in the parallel processing of the human brain. In the posterior part of the brain not only visual cortical areas may qualify for parallel processing, but also the somatosensory cortices appear to have separate functional streams for the detection of microgeometry and macrogeometry.

Introduction

This paper presents some ideas on how the cerebral cortex of man could be parcelled based on structural and functional criteria. Any parcellation is based on an assumption of what is a cortical area. Since cortical areas are thought to reflect the principle of organization of the cerebral cortex, the issue of parcelling the cortex is also fundamental for the organization of the cerebral cortex. The question of what is a cortical area needs several qualifications. Is it possible to define an area by one single criterion, for example cytoarchitectonics? What is a border of a cortical area? If cortical areas have borders how are these borders defined? Here we suggest the approach that quantitative criteria, that is criteria based on measurements of microstructure and functional activations of the human brain should be used to define and delimit areas.

The microstructure of the human cerebral cortex is defined by more than a single structural modality. It consists of (1) the cytoarchitecture, the packing density and laminar distribution of pyramidal and non-pyramidal neurons; (2) the myeloarchitecture, i.e. the packing density and laminar distribution of myelinated fibers; (3) the receptor architecture, the density of neurotransmitter receptors in fmol/mg protein and laminar distribution of different receptor types; (4) the density of reuptake sites on nerve terminals for different neurotransmitters; (5) distribution of other neurochemical variables such as the densities of enzymes, specific structural proteins, etc.; (6) the architecture of synapses. Since especially the densities of receptors, reuptake sites and enzymes is modifiable to some extent even under non-pathological conditions, this illustrates that the distinction between structure and function is fuzzy. The measurements of microstructural variables should be taken in vivo as well as in postmortem brains. By functional activations is meant immediate biochemical changes and changes in ion channels which accompany synaptic activity and are locally resulting in changes in the regional cerebral blood flow (rCBF), regional cerebral metabolism, optical signals, extended dipoles, etc.

Although it is possible to delimit areas based on microstructural measurements and delimit functional activations in single subjects, the concept of a cortical area should be more general. We therefore show that this concept should be realized as population (probability) maps. The quantitative nature of data often implies the use of statistics or mathematics to unambiguously delimit the borders of microstructurally defined areas or functional fields.

We present the cortical field hypothesis (CFH), i.e. the functional organization of the human cerebral cortex is based on functional fields each occupying a certain, relatively large territory of the cortex. Such fields are the largest functional entities. Some major postulates of the CFH are presented with examples to illustrate these. It is not the purpose of this review to present all experimental evidence for the CFH. This has been done elsewhere in more detail 1, 2. Rather this article is an attempt to derive some principles of how the relation between structure and function could be studied; to present some quantitative methods which will be necessary tools for such studies, and to point out some consequences of the CFH for the organization of the cerebral cortex in parallel and non-parallel processing. These aspects are illustrated with typical examples. The literature cited also should be regarded as examples, since this communication by no means is exhaustive in this respect.