Structural divisions and functional fields in the human cerebral cortex1
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.
Section snippets
Microstructural organisation of the cerebral cortex
It is generally assumed that the microstructural parcellation of the human cerebral cortex is a more or less settled issue when it comes to cytoarchitectonics and myeloarchitectonics (for example Ref. [3]). Although Brodmann's map is known to neurobiologists as the accepted parcellation of the cerebral cortex based on cytoarchitecture, it reflects a parcellation based on subjective criteria of where the borders should be. This map and others 4, 5, 6, 7, 8are usually derived from observations on
Population maps
A population map of a microstructurally defined area is a three dimensional representation in standard anatomical format of the delimitation of the area in a population of subjects. Let the microstructural quantitative variable be m. Further let the area in question be defined as m exceeding a certain value mc. It is then possible in an individual brain of subject Si to define a volume within which m > mc. In the 3D pictorial standard anatomical representation of Si's postmortem brain all
Functional parcellation of the cortex, the cortical field activation hypothesis
It is often quoted that the elements of neuronal activity are segregated into functional columns 3, 34, 35. Whereas this arrangement is obvious in konio-cortices or perhaps in parakonio-cortices, the increased synaptic and neuronal activity elsewhere seems to occur more like in fields, blobs or patches, questioning the columnar organisation as a general principle of organisation 36, 37, 38, 39. At a more coarse level, studies in which tracer methods have been used to reveal the activation of
Intersection analysis
Whereas it is hazardous to claim a particular functional specialization of a field on the basis of a subtraction paradigm applied on a single group of subjects, repeated applications of subtraction paradigms (with different control conditions, and/or test conditions, all containing the functional aspect searched for) provide, if a consistent set of fields is identified, a stronger evidence for the functional contributions of the isolated field. Thus put in another way, the set of fields
Another example of intersection analysis of short term and long term memory representations
Although fields are the largest functional elements of the cortex, this does not imply that fields are modular. In other words, the appearance of a functional field (obtained with PET and fMRI) marks the afferent and intrinsic synaptic activity, and since the same region may receive different combinations of active afferents in different brain tests, it is not guaranteed that all combinations of active afferents will cover the exact same cortical territory. On one hand one expects fields
Formulation of the structural–functional problem in cortical parcellation
As stated, a cortical area is defined by multiple criteria on the microstructural domain. For the cerebral cortex of man, one important microstructural criterion is — for practical reasons — missing, that of connectivity. Cortical areas defined by microstructure vary in localization, extent and topography among individuals. In the functional domain, changes in activity of the cerebral cortex manifest themselves as functional fields. Similarly, the localization and extent of functional fields
The interference principle
If it is so that neurons in the cerebral cortex activate in large distinct populations or fields, and if the field in essence consists of neurons performing cooperative computation as described in Section 4, it follows that two different brain tasks requiring the participation of one or several identical fields cannot be performed simultaneously. This is the interference principle: “If two different brain tasks make use of one or several identical fields, they cannot be performed
Parallel processing in the human brain
A prerequisite of a demonstration of parallel processing, under the strong version of the CFH, is to have two tasks and show that the fields executing the brain part of the tasks would be non-overlapping. This, as repetitively argued in this report, requires a mathematically unambiguous measure of field shape and extent and a high sensitivity of the statistical methods. A further requirement is that the neurons at one set of fields increase their firing rate or synchronize exclusively in the
Conclusions
- 1.
Microstructural parcellation of the human cerebral cortex must be made on the basis of: Quantitative measurements and multiple criteria. Such microstructurally defined areas appear as population maps.
- 2.
The organisation of cerebral cortex into functional columns may apply for koniocortices — elsewhere the active synaptic populations take the form of larger blobs or patches. The columns, patches or blobs combine in cortical functional fields, postulated to be the largest functional entities of the
Acknowledgements
This work was supported by EU Biotech programme and the Swedish Medical Research Council. We appreciate the help of Jonas Larsson, Anders Ledberg, Torkel Klingberg, Katrin Amunts and Aleksandar Malikovic who kindly provided some of the figures and data.
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Published on the World Wide Web on 20 February 1998.