Studies of Brain Function - Böcker

This booklet, together with the following two,-which are well under way and will succeed it at intervals of, we hope, no more than six months, sets the stage for a new editorial enterprise in the field of brain science. The accent is on the functional aspects of brains rather than on their develop­ ment, hence the title of the series. The central question being how neural activity is related to behavior, there will be, naturally, a wide scatter of sub­ jects, and Heiligenberg's monograph on electric fish may be considered typ­ ical of the expected standard deviation from the mean. Deviations in other directions may go as far as the sensory neuron, or brain theory, or aphasia, or farther. The next contributions planned for the series are: Precht, Neuronal Operations in the Vestibular System, and Movshon, Genes and Environment in the Development of the Visual Cortex. Our aim is to ap­ proach the central area by means of something like an evolving handbook of brain science. The individual monographs should describe promising and successful approaches, even in areas where the last word is far from being said. Besides originaI monographs and compounds of the author's own published papers, reviews are also we1come if they are more than the sum of the parts. The publisher promises speedy publication, and the editors will see that the manuscripts will be readable as well as interesting. Tübingen, Summer 1977 V.

The original intent of the series Studies of Brain Function was to offer a forum to neurobiologists working in different fields to present some of their recent results in a more extensive way. What may have been or might be published in several papers appearing in different journals will thus be com­ bined in one monograph, thus making the data more easily available to a wider scientific community. It is also believed that such an attempt will provide a more comprehensive insight into one particular field of neurobiol­ ogy. Admittedly, the monograph will represent a more subjective view than that provided by a classical review article. In this monograph I am going to describe a major aspect of my research, i.e., the central processing of information arising from the receptors in the semicircular canals and otoliths of the inner ear. I shall restrict this report to those systems that are concerned with the vestibuloocular transmission, since they offer particular opportunity to study sensory-motor integration.

The brain functions like a computer composed of subsystems which in­ teract in a hierarchical manner. But it is not a single hierarchy, but a com­ plex system of hierarchies each of which has its very own and unique fea­ ture. One of these concerns the cyclic or rhythmic control of neuronal ac­ tivities which, among others, give rise to alternating states of wakefulness and sleep. The phenomenon of sleep still remains a mystery. The present monograph does not give us any new insights into its meaning and significance. Yet sleep research may not be the same after the appearance of this book be­ cause it gives us a comprehensive mathematical theory which opens our eyes to new insights into the mechanism of the rhythm generation that under­ lies the "wake-sleep" cycle. No one who has worked his way through this book can again look at ex­ perimental data without recognizing features which the "models" developed in its various chapters so strikingly reveal.

The invitation by the editors of the series "studies of brain function" to contribute a monograph on the visual cortex gives me the opportunity to present in a concentrated manner much of the work I have done on the visual cortical areas of cat and monkey. However, the field of visual cortical physi­ ology is so active and so diverse that the presentation of only my own work would have given a very incomplete view of visual cortical functioning. Therefore this monograph also reviews most of the studies carried out on the subject in the last two decades. Where possible I have tried not only to describe the cortical machinery but also its possible functional purpose regarding vision. In doing this I have expressed my personal views rather than just reviewing the experimental facts. Much of the work presented in this monograph has been supported by the National Research Council of Belgium and the Research Council of the Catholic University of Leuven. I express my gratitude to them. I have en­ joyed collaborating in these studies with P. O. Bishop, H. Kato, H. Kennedy, K. P. Hoffmann, H. Maes, J. Duysens, E. Vandenbussche, and H. van der Glas. I am much indebted to all those who have commented on earlier versions of this monograph: J. Allman, H. Barlow, J. BuBier, M. Callens, J. Duysens, O. J. Griisser, P. Heggelund, H. Kennedy, L. C. Orban and L. Palmer.

The "neurosciences" is now a common 'term to describe several branches of the biology related to studies of the nervous system. In fact, this term also character- izes a multidisciplinary approach to studies of probably the most complicated system of the most complicated living organisms. Investigation of the central ner- vous system (CNS) is the most quickly developing branch of the neurosciences. According to Konorski's definition, the CNS "is endowed with two principal properties which are referred to as reactivity and plasticity. Reactivity of the sys- tem is its capacity to be activated by stimulation of receptive organs; plasticity is the capacity to change its reactive properties as the result of successive activa- tions" ([520], p. 7). According to Kostyuk [535], plastic reorganizations include "any changes in the efficacy or direction of neuronal connectivity which exceed in their duration usual synaptic and spike events" ([535], p. 25). Neuronal plasticity underlies adaptive modifications of various complexities both in normal CNS, e. g. its development, formation of memory traces and condi- tioned responses (CRs) , as well as in brain pathology, e. g. reorganization and compensation of damaged nervous functions.Clarification of plasticity mecha- nisms is of great cognitive importance and might be of practical value in the treatment of mental and especially memory disorders.

This monograph is the result of a course given to graduate students and to the faculty of the Dept. of Medical Physics and Biophysics of Nijmegen University, Nijmegen, The Netherlands, in the fall of 1984 and 1985. The course was intended to put together experi­ ment, theory, and analysis methods in order to study neural in­ teraction and coding in the brain. The following pages give a survey of neural interaction and its experimental substrate: cor­ related neural activity. The basic reason for restricting myself to vertebrate brains was to keep the material concise. As the text developed, however, it became more of a review, than a research monograph, in the attempt to balance theoretical and experimen­ tal aspects in brain research. Consequently, the book can be read from various points of view: that of requiring an overview of theories and theoretical principles, or an overview of experimental studies in neural interaction and the methods that can be used, or with the conviction that theory and experiment cannot be separat­ ed. In the latter case the book should be read from beginning to end. A way to read through the theoretical sections and the ex­ perimental sections of the book is presented in the following flow chart; Theory: /Chap. 2 -Chap. 4 -Chap. 5 ___ ~ Introduction -+ Chap. 1 \, Chap. 10 -+ Chap. 14 Experim~Chap. 3 -Chap. 6 -Chap. 7 -Chap. 8 ~ Chap.

"Theorizing about brain functions is often considered slightly disreputable and anyhow a waste of time -perhaps even 'philoso- ical'" 1 P. S. CHURCHLAND At present there are no unanimously accepted general con­ cepts of brain operation and function. This is especially the case with regard to so-called "higher" functions such as per­ ception, memory or the coupling between sensory input and motor output. There are a number of different reasons for this. Some may be related to experimental limitations allowing the simultaneous recording of the activities of only a restricted number of neurones. But there are also conceptual difficulties hindering the transition from "single-neurone" schemes, in which neurones are assigned relatively specific tasks (such as feature detection), to more complex schemes of nerve cell as­ semblies (for a discussion of some of the difficulties see Abeles 1982; von der Malsburg 1981; Kriiger 1983). Whilst much is known about the basic properties and functions of single neu­ rones, whose operations we hope to understand in the foresee­ able future, this does not hold true in the same way for the working of large assemblies of neurones.

This monograph represents the current status of neuro­ ethological research on the diurnal behavior of the stick in­ sect, Carausius morosus. The growing profusion of inter­ related studies, many of which are published only in German, makes an overview of this field increasingly difficult. Many stick insect results contribute to general problems like con­ trol of catalepsy, control of walking, program-dependent reactions and control of joint position. For this reason I decided to compile and synthesize the results that are pre­ sently available even though the analyses are far from con­ cluded. In addition to both published and unpublished results of the group in Kaiserslautern (Bassler, Cruse, Ebner, Graham, Pfluger, Storrer, as well as doctoral and masters students), I have drawn upon the literature which had ap­ peared as of summer 1981. This includes above all the work of Godden and of Wendler and his colleagues in Cologne. A summary of the anatomical and physiological background, necessary for an understanding of these investigations, is provided in an appendix (Chap. 6). Methodological details must be obtained from the original publications. Figures for which no source is given are from my own studies. I intend to update this monograph on an annual basis. Requests for these supplements should be directed to me in Kaiserslautern. I would like to express my appreciation to all members of the group in Kaiserslautern for their constructive discussions, their unflagging cooperation, and their permission to include hitherto unpublished results.

After reading the manuscript, some biologists inquired why, on the basis of the broad experimental material presented in this book, we had not come up with a model describing the operation of the cerebellum. To answer this question, we decided to write a preface to our book. How the nervous system copes with the complexity of the world is one of the central problems of neurophys­ iology. The question was clearly formulated for the frrst time by N. A. Bernstein. Considering the problem of motor control, he pointed out that the main objective of motor coordination is to overcome the redundant number of degrees of freedom of the motor apparatus or, in other words, to diminish the number of independent variables which control the movement (Bernstein 1967). These I. M. Gelfand and M. L. Zetlin ideas were further developed by (Gelfand and Zetlin 1966). They proposed, in particular, the "non-individualized" ("non-addressed") mode of control in complex systems, where only the highest levels of the system have the full notion about the fmal task while the main "effectors" act on the basis of very limited information. These propositions were made by Gelfand and Zetlin in a very general form, but, nevertheless, proved to be fruitful in determining the direction of experimental research. For instance, the discovery of the "locomotory region" of the brain stem (Shik et al.

Salamanders are subject to misconceptions even among vertebrate zoologists and physiologists. They are often said to exist only in northern temperate zones, being bound to aquatic or very moist cool habitats. In reality, more than half of all salamander species live in subtropical and tropical zones, ex­ clusively in the New World. Again, more than half of the salamand~r species have become totally independent of aquatic habitats following the loss of a free larval stage. Many of the subtropical and tropical salamanders have become adapted to rather high temperatures up to 26-28 DC. The brain and the sensory systems of salamanders are often considered to be primitive, and their behavior is thought to be simple and uninfluenced by learning. However, careful studies show that the salamander brain possesses virtually all the ana­ tomical and functional properties found in anurans, which are usually regarded as being much more evolved with respect to the guidance of comparable behavior. Most of the salamander species not only possess a highly efficient visual system, which is the topic of the present work, but can orient themselves almost as effectively by means of olfaction, vibration sense, and electroreception. Furthermore, it has recently been shown that at least part of their behavior, especially that concerned with feeding and prey preferences, is strongly influenced by individual experience.

This is a timely opus. Most of us now are too young to remember the unpleasant ring of a polemic between those who produced "hair-splitting" parcellations of the cortex (to paraphrase one of O. Vogt's favourite expressions) and those who saw the cortex as a homogeneous matrix sus­ taining the reverberations of EEG waves (to paraphrase Bailey and von Bonin). One camp accused the other of producing bogus preparations with a paint brush, and the other way around the accusation was that of poor eye-sight. Artefacts of various sorts were invoked to explain the opponent's error, ranging from perceptual effects (Mach bands crispening the areal borders) to poor fixation supposedly due to perfusion too soon (!) after death. I have heard most of this directly from the protagonists' mouths. The polemic was not resolved but it has mellowed with age and ultimately faded out. I was relieved to see that Professor Braak elegantly avoids dis­ cussion of an extrememist tenet, that of "hair-sharp" areal boundaries, which makes little sense in developmental biology and is irrelevant to neurophysiology. It was actually detrimental to cortical neuroanatomy, since its negation led to the idea that structurally distinct areas are not at all existent. Yet, nobody would deny the reality of five fingers on one hand even if the detailed assignment of every epidermal cell to one finger or another is obviously impossible.

The invitation to contribute a volume to the series Studies in Brain Func­ tion offers me a welcome opportunity for a comprehensive presentation of my research on the eye movements of the rabbit, and for a review of the older results in the perspectives offered by the progress of my own work, but even more of the field in general. Characteristically this monograph em­ phasizes the views of the author, which may not always be generally accept­ ed. Although connections with the work by other investigators are discussed as much as possible, I have not attempted to be complete in reviewing all publications related to oculomotor function in the rabbit. While presenting an overview of current understanding of a system, it is always wise to trace the historical roots of our knowledge and concepts. On the one hand, we may find that many established concepts derive their strength more from convention and convenience than from rigorous evi­ dence. Such traditional ideas should be challenged by critical experiments, using the best available techniques. On the other hand, some of the older publications remain a source of inspiration, because they contain valid ideas which generate fruitful experiments even today. A remarkable example of this category is Ter Braak's work on optokinetic nystagmus, published in 1936.

Neurophysiologists are often accused by colleagues in the physical sci­ ences of designing experiments without any underlying hypothesis. This impression is attributable to the ease of getting lost in the ever-increasing sea of professional publications which do not state explicitly the ultimate goal of the research. On the other hand, many of the explicit models for brain function in the past were so far removed from experimental reality that they had very little impact on further research. It seems that one needs much intimate experience with the real nerv-. ous system before a reasonable model can be suggested. It would have been impossible for Copernicus to suggest his model of the solar system without the detailed observations and tabulations of star and planet motion accu­ mulated by the preceeding generations. This need for intimate experience with the nervous system before daring to put forward some hypothesis about its mechanism of action is especially apparent when theorizing about cerebral cortex function. There is widespread agreement that processing of information in the cor­ tex is associated with complex spatio-temporal patterns of activity. Yet the vast majority of experimental work is based on single neuron recordings or on recordings made with gross electrodes to which tens of thousands of neurons contribute in an unknown fashion. Although these experiments have taught us a great deal about the organization and function of the cor­ tex, they have not enabled us to examine the spatio-temporal organization of neuronal activity in any detail.

An invitation from the Editors to contribute to 'Studies of Brain Functions' with a monograph on the parietal lobe of­ fers me an opportunity to present in a concentrated form my studies on this part of the brain from a period of some­ what over a decade. The parietal lobe, notably its posterior part, is a very complex neural system whose functions I have been able to study only superficially and without ex­ tensive coverage of all its parts. Therefore I did not want to limit myself entirely to my own work but found the task of writing more interesti'ng by including sections reviewing rel­ evant literature. Thus Chapter III dealing with the primary somatosensory cortex and Chapters IX, X, and XI concerning area 7 describe work done in my laboratory. Chapter VIII describes microelectrode work on area 7 and covers both the work of my group and that of others working on this area. Chapters II and IV to VII are based on closely related anatomical, physiological and clinical studies performed by others, and Chapter XII is a personal attempt at a synthesis of the functions of the parietal lobe. Thus this monograph is neither a strict review of all important works on the parietal lobe nor is it limited only to my own studies and those of my collaborators. Instead it attempts to be a balanced ex­ position of both aspects promoting, hopefully, a synthetic view of the primate parietal lobe.

"To explain all nature is too difficult a task for anyone man or even for anyone age. Tis much better to do a little with certainty, and leave the rest for others that come after you, than to explain all things ... " Sir Isaac Newton (1642-1727) This book describes and discusses some new aspects of col­ or vision in primates which have emerged from a series of experiments conducted over the past 8 years both on single ganglion cells in monkey retina and on the visually evoked cortical potential in man: corresponding psychophysical mechanisms of human perception will be considered as well. An attempt will be made to better understand the basic mechanisms of color vision using a more comprehensive approach which takes into account new mechanisms found in single cells and relates them to those found valid for the entire visual system. The processing of color signals was followed up from the retina to the visual cortex and to the percepq.tal centers, as far as the available techniques permitted.