Cortical Areas

Unity and Diversity

Almut Schuez, Robert Miller

• Publisher: CRC Press
• Year: 2002
• ISBN:
  9781134473519
• Edition: 1
• Topic: Medicine
• Subtopic: Anatomy

The study of areas in the cerebral cortex has a long history, bringing empirical data into close relation with fundamental conceptual issues about the cortex. The subject is currently being revitalized with the advent of new experimental methods and this book brings a modern perspective to the study of these areas. Cortical Areas: Unity and Diversi

1 Introduction: Homogeneity and Heterogeneity of Cortical Structure: A Theme and its Variations

Almut Schüz

Max-Planck-Institut für biologische Kybernetik, Spemannstr. 38, 72076 Tübingen, Germany

Tel: [phone]; FAX: [phone]; e-mail: [email protected]

The cortex is subdivided into anatomically recognizable areas. This phenomenon, though described in detail nearly a century ago, is still difficult to grasp precisely. The local differences in structure are subtle enough to have evoked debates which still continue about the exact definition of a cortical area, the number of areas, the exact location of their borders and the comparability of areas between species. It depends on the context whether one considers the cortex as a more or less homogeneous structure, or rather emphasizes its heterogeneity. In view of the very different tasks in which the cortex is involved, such as sensory processing of different modalities, learning, long-term planning, decision taking, movement or human speech, one may be impressed by the relative homogeneity of the overall structure of the cortex, both within and between species. If, on the other hand, one compares the cerebral cortex to the cerebellar cortex, which shows no signs of local differences in architectonics, the heterogeneity of the structure of the cerebral cortex is striking.

Both aspects have to be explained: the fact that the cortex can perform a large variety of tasks on the basis of a more or less uniform structure, as well as the reasons for the local variations in structure. The homogeneous aspects, the “theme” of cortical structure, indicate that some common denominator can be found for the whole spectrum of tasks in which the cortex is involved. The heterogeneous aspects, the “variations” superimposed upon the theme, may point the way to relevant parameters for local variations in cortical function.

Much knowledge has accumulated concerning both aspects during the last few decades. New anatomical methods and the enormous developments in electrophysiology have increased our understanding of the basic structure and function of the cortex, and they have also added a large amount of detailed knowledge about individual cortical areas.It therefore seems timely to revisit the work of Brodmann (1909), Vogt (1910, 1911), von Economo and Koskinas (1925), Flechsig (1920) and others, on the basis of these new developments, and to make a new effort to better understand the anatomical differences in terms of function. We will see that this effort will lead us deep into crucial questions of information processing in the cortex.

OUTLINE OF THE BOOK AND BASIC QUESTIONS

The topic of cortical areas can be approached in different ways. Fascinating insights into the role of cortical areas have come from the analysis of the various processing stages within one modality, in particular in the visual system, as detailed in the work by Hubel and Wiesel (e.g. 1977), Zeki and co-workers (e.g. Zeki, 1993), Oram and Perrett (1994), Gauthier and Logothetis (2000), and others. Another approach is based on a comparison between the various sensory systems, as in the volumes edited by Woolsey (1981a,b, 1982) and by Peters and Jones (1985a,b, 1986). The present book follows that line. It does not concentrate on one particular modality, but is concerned with the entire cortex, including a comparison between areas dealing with different modalities. The main emphasis is on anatomy, but with the aim of rising above the descriptive level as far as possible, to reach a better understanding of the role of cortical areas in general. This is why we have also included a few chapters based on other techniques such as electrophysiology and experimental surgery.

The book is divided into several parts, by grouping the chapters according to their main topic. The division is, however, not a strict one: Some topics come up in various chapters, viewed from different vantage points. Following the five parts, we have therefore included a Discussion Chapter in which we try to pull together threads from the preceding parts.

Part I attempts to provide a better grasp of the local differences in architechtonics, by way of more recent methods, or by way of a new look at the classic methods. It deals with questions like the following: Do cortical maps derived with different histological methods agree with each other? In other words, do the various histological methods basically describe the same map, though perhaps with different precision, or are there several maps independently superimposed onto each other (chapters by Hellwig, Amunts et al., Rademacher)? How do maps differ between individual brains, and how is this variation related to that of gyri and sulci (Rademacher, Seitz)? How do the anatomical maps relate to functional mapping (Seitz)? This latter chapter leads us towards the long-standing topic of debate between localization vs distribution of function.

Part II focusses on another crucial question with respect to information processing: How can the structural variations described in architectonic maps be interpreted as variations in connectivity? Differences and similarities in intracortical connectivity are dealt with in the chapters by Jacobs and Scheibel and by Levitt and Lund, but are also adressed in some chapters of the other sections (Hellwig, Valverde et al., Pallas, and Shipp). The relationship between thalamus and cortical areas is treated by Cusick. Differences and similarities between areas with respect to cortico-cortical long-range connectivity are dealt with in the chapter by Kaas, but are also touched upon in the various chapters in Part V.

In Part III, the questions of mapping and of connectivity come up again in the comparison between species (Valverde et al.) and between iso- and allocortex (Miller and Maitra).

Part IV takes up another crucial question: Is the cortex, in principle, a largely equipotent network in which the inputs from different modalities could be exchanged? This question is related to two other important questions: (1) What role does the thalamic and/or sensory input play in shaping the structure of a cortical area (Pallas); and, (2) as pointed out in the same chapter, in what respects does sensory processing differ at all in different modalities? To a certain extent, an apparent equipotentiality of the cortex may be simply due to the fact that there are basic similarities in information processing between different sensory modalities. These questions are dealt with in the chapters by Pallas, Dinse and Schreiner.

Part V discusses integration between cortical areas, as well as the segregation of functions, as determined by the cortico-cortical long-range system (Young, Shipp). This leads us to the question of hierarchical vs parallel processing in the cortex and to the topic of feature extraction and feature combination. The chapter by Miller deals with the integrative role of the thalamus, the basal ganglia and the hippocampus for cortical functions. In these chapters, the term “unity” in the title of the book gets a somewhat different meaning from that in the other parts in which it was used in the sense of “uniformity” in structure or “universality” in function. In this last section, the term “unity” may be understood as the integration of different parts of the cortex involved in a particular task, thinking perhaps of the various regions which light up in functional imaging during a particular task.

BASIC CONNECTIVITY OF THE CORTEX AND LOCAL VARIATIONS

Homogeneous aspects of cortical structure are those which are common to all cortical areas, both within and between mammalian species, such as the existence of layers, similar input and output organization to – and from – subcortical structures, and the orthogonal orientation of pyramidal cells with respect to the layers. In order to offer some starting point for a discussion of the role of cortical areas, I will briefly summarize some of the homogeneous features of cortical connectivity from which one can draw conclusions about the basic function of the cortex (Braitenberg, 1974, 1978a; Braitenberg and Schüz, 1998). The following list is based on quantitative anatomical studies from our own laboratory (e.g. Braitenberg, 1978b, 1986; Schüz and Palm, 1989; Schüz and Demianenko, 1995) as well as on those by Sholl (1956), Cragg (1967), Scheibel and Scheibel (1968), Valverde (1971), Foh et al. (1973), Wolff (1976), Winkelmann et al. (1977), Peters (e.g. Peters and Feldman, 1976; Peters and Kara, 1985), Beaulieu and Colonnier (1985), Braak and Braak (1986), White (1989) and others.

1. The neurones in the cortex are mainly connected to other cortical neurones. Input and output connections with subcortical neurones contribute only a small percentage to the synapses of cortical neurones (see also chapter by Young, this volume).
   
2. The majority of neurones in the cortex are of one type, the pyramidal cells.
   
3. They are excitatory, and form an extensive network mainly among themselves.
   Inhibitory interneurones are loosely interspersed and contribute only about 11% of the synapses.
   
4. Each pyramidal cell projects to, and gets input from thousands of other neurones, but makes usually only one or few synapses with any one of them.
   
5. Most pyramidal cells make both short-range connections in their immediate vicinity via axon-collaterals, and long-range connections somewhere else in the cortex via the main axon traversing the white matter.
   
6. The pyramidal cells are connected with each other mainly via dendritic spines. Much speaks in favour of the assumption that the spines are structural specializations which are particularly suited for regulating the strength of synapses and thus have to do with plasticity and learning (for review see Horner, 1993; for recent experimental evidence see Engert and Bonhoeffer, 1999).
   

The definition of pyramidal cells adopted by our group does not put emphasis on the shape of the cell body or the dendritic tree, but more on the presence of spines and the existence of a long-range connection, in accordance with the definition of the Class I cells used by Globus and Scheibel (1967). Such a definition of this class of cells has received further support from electronmicroscopical studies (summarized in Peters and Jones, 1984). The class comprises the excitatory neurones of the cortex, and, in addition to their main group (the pyramidal cells of older classifications), also includes spiny neurones without an apical dendrite (even though a subpopulation of those does not participate in the long-range system; see Valverde et al., this volume).

The fact that each pyramidal cell is connected to thousands of other neurones makes it very unlikely that the genetic instruction for cortical wiring reaches down to the level of connectivity between individual neurones. Genetic instruction can be assumed to be limited to the determination of neuronal types and the approximate distribution of projections, i.e. to the determination of probabilities of connections (Sholl, 1956; Cragg, 1967; Braitenberg, 1978a).

Although this does not allow us to say anything about the connectivity between individual neurones, the shape and location of dendritic and axonal trees will tell us something about the connectivity between neuronal populations. The ramifications of axons and dendrites reflect the location of synapses on a neurone quite faithfully: Synapses are distributed throughout dendritic trees (with some well-known gradients; e.g. Globus and Scheibel, 1967; Marin-Padilla, 1967; Valverde and Ruiz-Marcos, 1969; Kunz et al., 1972) and—as far as it is known—also throughout unmyelinated axonal ramifications (Amir et al., 1993; Hellwig et al., 1994). This suggests that the neurones tend to make synapses with the neuronal processes, they meet in the neuropil without too much selectivity. This view is supported by other anatomical data which suggest a statistical connectivity between cortical neurones (summarized in Braitenberg and Schüz, 1998; Schüz, 1992). Moreover, although some neuronal populations do show interesting deviations from a purely statistical connectivity (Johnson and Burkhalter, 1997; for evidence for both selectivity and nonselectivity, see White, 1989), complete selectivity has only been shown for one type of non-pyramidal cell, the chandelier cells, which seem to connect only to pyramidal cells (see data collected by White, 1989). Thus, whatever the details of the rules which decide that a synapse is established between two individual neurones (be it only a question of “who hits onto whom” in the crowd of cell processes or beyond that some developmental or activity-dependent selectivity), the shapes, densities and locations of dendritic and axonal trees can be taken as an indicator of the network structure at any given place.

To a large extent, the architectonic differences, as seen for example in the Nissl picture, may reflect local differences in the density and shape of dendritic and axonal ramifications, i.e. local variations in the statistics of the connectivity between neurones (see also the chapter by Hellwig). For example, in a region or layer in which pyramidal cells have loosely ramifying dendritic trees, individual axons may have a lower chance of hitting a particular dendritic tree more than once than in case of more densely ramifying dendrites. Thus, looseness of dendritic trees entails a higher degree of convergence, while density of dendritic ramifications correlates with the strengt...

Table of contents

• Cover Page
• Title Page
• Copyright Page
• Preface
• Contributors
• 1 Introduction: Homogeneity and Heterogeneity of Cortical Structure: A Theme and its Variations
• Part I The Empirical Status of Cortical Maps
• Part II Cortical Areas: Correlation with Connectivity
• Part III Constancy and Variation Across Species
• Part IV Functional Equivalence Between Areas
• Part V Morphological Substrates of Segregation and Integration