Parallel Processing in the Visual System THE CLASSIFICATION OF RETINAL GANGLION CELLS AND ITS IMPACT ON THE NEUROBIOLOGY OF VISION

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1 Parallel Processing in the Visual System THE CLASSIFICATION OF RETINAL GANGLION CELLS AND ITS IMPACT ON THE NEUROBIOLOGY OF VISION

2 PERSPECTIVES IN VISION RESEARCH Series Editor: Colin Blakemore University oj Oiford Oxford, England Parallel Processing in the Visual System THE CLASSIFICATION OF RETINAL GANGLION CELLS AND ITS IMPACT ON THE NEUROBIOLOGY OF VISION Jonathan Stone A Continuation Order Plan is available for this series. A continuation order will bring delivery of each new volume immediately upon publication. Volumes are billed only upon actual shipment. For further information please contact the publisher.

3 Parallel Processing the Visual System THE CLASSIFICATION OF RETINAL GANGLION CELLS AND ITS IMPACT ON THE NEUROBIOLOGY OF VISION In ]ONA THAN STONE School oj Anatomy University oj New South Wales Sydney, Australia PLENUM PRESS. NEW YORK AND LONDON

4 Library of Congress Cataloging in Publication Data Stone, Jonathan, Parallel processing in the visual system. (Perspectives in vision research) Bibliography: p. Includes index. 1. Retinal ganglion cells-classification. 2. Vision. 3. Mammals-Physiology. I. Title. II. Series. [DNLM: 1. Retina. 2. Neurons-Classification. 3. Classification-Methods. 4. Visual perception-physiology. WW 270 S878p] QP479,S ' ISBN-13: e-isbn-13: : / Plenum Press, New York A Division of Plenum Publishing Corporation 233 Spring Street, New York, N.Y All rights reserved No part of this book may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, microfilming, recording, or otherwise, without written permission from the Publisher

5 F or Margaret

6 Foreword In the mid-sixties, John Robson and Christina Enroth-Cugell, without realizing what they were doing, set off a virtual revolution in the study of the visual system. They were trying to apply the methods of linear systems analysis (which were already being used to describe the optics of the eye and the psychophysical performance of the human visual system) to the properties of retinal ganglion cells in the cat. Their idea was to stimulate the retina with patterns of stripes and to look at the way that the signals from the center and the antagonistic surround of the respective field of each ganglion cell (first described by Stephen Kuffier) interact to generate the cell's responses. Many of the ganglion cells behaved themselves very nicely and John and Christina got into the habit (they now say) of calling them I (interesting) cells. However. to their annoyance, the majority of neurons they recorded had nasty, nonlinear properties that couldn't be predicted on the basis of simple summ4tion of light within the center and the surround. These uncooperative ganglion cells, which Enroth-Cugell and Robson at first called D (dull) cells, produced transient bursts of impulses every time the distribution of light falling on the receptive field was changed, even if the total light flux was unaltered. From this chance discovery of two major classes of ganglion cells (now called X and Y cells) has grown a whole new approach to the anatomy, physiology, and development of the visual pathway, as well as to human psychophysics. Jonathan Stone has made a number of important contributions to this study of parallel analysis within the visual system, including the first full description of the third (rather motley) class of ganglion cells, the W cells. In this monograph he shows how influential this way of thinking has been in visual science as well as in other aspects of sensory physiology. What better start could there be to this new series of monographs on vision, Perspectives in Vision Research? The series will provide up-to-the-minute authoritative accounts of all aspects of visual science, still perhaps the broadest and most active area within neuroscience. Colin Blakemore Oxford vii

7 Preface This monograph began as an account of the classification of retinal ganglion cells in the cat and other mammals, and its scope could well have been limited to that. But although the classification of ganglion cells is a complex and intriguing problem in itself, its major importance lies, I believe, in the impact that it has had on our understanding of the visual pathways. Once it was established that retinal ganglion cells form a number of functionally distinct groups, the visual centers of the brain were analyzed and reanalyzed in terms of those groups. From this work there emerged a new understanding of these centers, leading to the idea of "parallel processing" in the visual system, i.e., that the visual pathways comprise parallel-wired sets of neurons that code and transmit different aspects of the visual image. It has become a challenge to trace this parallel organization and to ascertain both the value and the limitations of the concept of parallel processing in the analysis of the visual pathways. Historically, the idea of parallel processing was first developed in the study of the somatosensory pathways, and it is currently being extended to audition and olfaction, as well as vision. Its value and limitations in all these contexts need exploration and assessment. As a consequence, only the first of the three parts of this monograph is concerned with the classification of retinal ganglion cells. Much the longest part is Part III, which concerns the impact that the classification has had on our understanding of the lateral geniculate nucleus, superior colliculus, and visual cortex, and on the analyses of retinal topography, of the influence of deprivation on the visual pathways, and of visual perception. Part III ends with a survey of parametric processing in sensory systems other than vision, and a proposal for a "parametric systematics" of neuronal classification. Part II concerns the methodology of classification. I argue there that although classification is a fundamental process in the conceptual organization of scientific knowledge, many visual neurobiologists (myself included) have paid too little attention to the methodologies we have used in classifying nerve cells. A case is argued for a particular approach to classification, in the context of (1) historical and contemporary approaches to classification, (2) the epistemological issues involved, and (3) the biological context of the problem. I have incurred many debts in writing this monograph. Some are old and intangible. From my father, I learned from childhood the value for scholarship of erudition, simplicity of analysis, and self-reliance. My scientific mentor, P. O. Bishop, brought me into this field, many of whose horizons he had pioneered or was about to explore; from him I learned the value of constant recourse to experimentation and of tolerance for others' interpretations. Their influence on my work has been strong and abiding. Other of the debts are more recent and tangible. lowe much to colleagues with whom several sections of the monograph have been developed as separate essays, in particular Michael IX

8 x PREFACE H. Rowe, Bogdan Dreher, and Audie G. Leventhal. Their contributions to Chapters 1, 2, 5, 8, 10, and 11 were fundamental. lowe warm gratitude to Daniele Dubois (who typed the first draft) and to Trudy Wiedeman (who typed the second draft); to Sharon McDonald and Peter Wells for their help with the illustrations; and to Paul Halasz for his patience and engineering skills in developing and helping me with a computer-based storage of the text. Many colleagues, including Colin Blakemore, Bogdan Dreher, Michael Cooper, Audie Leventhal, James McIlwain, Marilee Ogren, David Rapaport, Michael Rowe, and Mark Rowe, read and improved the manuscript, and for their valuable ideas and suggestions lowe my thanks and appreciation. I am grateful also to the many scientists and writers who gave ready permission for the reproduction of illustrations and text from their papers. My wife has borne and parried my recurring frustrations with the task with an affection and intelligence on which I have come much to rely. Jonathan Stone Sydney

9 Contents I. THE CLASSIFICATION OF RETINAL GANGLION CELLS 1. From the Beginning: Ganglion Cell Classification to Conduction Velocity Groupings in the Optic Nerve Receptive Field Studies of Retinal Ganglion Cells Parametric Analyses of Receptive Fields Feature Extraction Analyses of Receptive Fields Morphological Classifications of Ganglion Cells Function or Phylogeny as a Basis for Ganglion Cell Classifications? The Y /X/W Classification of Cat Retinal Ganglion Cells The Development of the Y /X/W Classification Description of the X/V Difference Conduction Velocity Correlates of X and Y Cells The W-Cell Grouping Morphological Classes of Cat Ganglion Cells The Y /X/W Classification: Categories and Taxa Evidence for Choice of Categories Evidence for Choice of Taxa The Interpretation of Variation: A Central Problem in Cell Classification "Single" and "Multiple" Interpretations of Variation Sources of Variation in the Properties of Ganglion Cells A Multiple Interpretation of Variation in the Properties of Ganglion Cells A Two-Group (XY/W) Classification of Cat Retinal Ganglion Cells Two Notes on the Classification of Nerve Cells Incommensurable Classifications Mixed Classifications: The Best of Both Approaches? Ganglion Cell Classification in Other Species In the Monkey Conduction Velocity Groupings Physiological Classifications: Parametric and Feature Extraction The W -like System of Ganglion Cells Morphological Classifications Summary 97 Xl

10 xu CONTENTS In the Rat Conduction Velocity Groupings Receptive Field Correlates: Is There an X-like Group? Morphological Classifications Summary In the Rabbit Conduction Velocity Groupings The Feature Extraction Classification of Rabbit Ganglion Cells More Parametric Analyses Summary In Other Mammals: Tree Shrew, Goat, and Ground Squirrel Tree Shrew Goat and Ground Squirrel.... In Nonmammals: Frog, Toad, Pigeon, Eel, and Mudpuppy Frog and Toad Pigeon Eel and Mudpuppy II. ON THE METHODOLOGY OF CLASSIFICATION Toward Certainty, Objectivity, or Testability? Two Notes on Alternative Methodologies of Classification Alternative Methodologies of Classification: Their Basis in the Concerns of Classifiers Nominalism and Realism Different Realist Approaches: Toward Certainty, Objectivity, or Testability Summary.... Three Stages in the Taxonomy of Animals Aristotle's Taxonomy: Metaphysical Essentialism Physical Typology The Influence of the Theory of Evolution Epistemological Background: Inductivism, Essentialism, Instrumentalism, Falsificationism, and Paradigms Inductivism Essentialism (Typology). Instrumentalism Falsificationism Paradigms and Revolutions 5.6. A Falsificationist Approach to the Classification of Neurons

11 CONTENTS Xlll III. THE IMPACT OF GANGLION CELL CLASSIFICATION 6. On the Understanding of Visual Processing in the Diencephalon The LGN of the Cat Evidence of Parallel Processing in the LGN The W-Cell Relay in the dlgn The Medial Interlaminar Nucleus The vlgn The Lamination of the dlgn Morphology of Relay Cells Cortical Projections of Y-, X-, and W-Class Relay Cells Corticogeniculate Projections The LGN of Primates X/V Analysis of Parvo- and Magnocellular Laminae Other Components of the LGN Corticofugal Projections Summary 6.3. Other Species The LGN of the Rat The LGN of the Tree Shrew The LGN of the Mink Summary Qualifications to the Parallel Processing Model of the LGN The Hypothalamus The Pulvinar: Evidence for an Extrageniculate W -Cell Relay On the Understanding of the Visual Centers of the Midbrain The Midbrain/Forebrain Division of the Visual Pathways: By Branching or Grouping of Ganglion Cells? The Superior Colliculus of the Cat Early Evidence: Conduction Velocity Analysis of the Retinocollicular Projections Receptive Field Correlates: Hoffmann's Three-Channel Model of the Retinocollicular Projection The Influence of the Visual Cortex and of Visual Deprivation on the Superior Colliculus Qualifications and Limitations The Superior Colliculus of the Monkey The Superior Colliculus of Other Species The Rat The Rabbit The Hamster The Opossum Summary

12 XlV CONTENTS 7.5. Other Midbrain Centers The Pretectal Nuclei and the Nucleus of the Optic Tract Nuclei of the Accessory Optic Tract and Nucleus Raphe Dorsalis On the Understanding of Visual Cortex.... Cat Visual Cortex: Processing of Geniculate Input Parallel Pathways to Different Cortical Areas Parallel Organization of Area 17: Correlations between Afferent Input and Receptive Field Properties Parallel Organization of Area 17: Analyses of Its Lamination Corticofugal Projections of Areas 17, 18, and Primate Visual Cortex: Processing of Geniculate Input Parallel Organization of Area Organization of the Prestriate Cortex.... Cortical Afferents from Extrageniculate Sources Sources of Extrageniculate Afferents in the Cat Sources of Extrageniculate Afferents in the Monkey Functional Significance of the "Second" Visual Pathway.... Models of Neuronal Processing within the Striate Cortex: An Argument against Serial Processing The Simple/Complex Model of Serial Intracortical Processing Synaptic Latencies: A Second Line of Evidence for Serial Processing? Summary.... Future Work: The Importance of the Classification and Terminology Used for Cortical Cells On the Understanding of Retinal Topography: A "Two-Axis" Model of Mammalian Retina.... The Problem: The Variability of Retinal Topography.... A Two-Axis Model of the Topography of Mammalian Retina.... The Vertical Axis: The Nasotemporal Division of Retina Historical Note: The Nasotemporal Division of Human Retina The Nasotemporal Division of the Retina in the Monkey The Nasotemporal Division of the Retina in the Common Cat The Nasotemporal Division of the Retina in the Siamese Cat The Nasotemporal Division of the Retina in Marsupials, the Rabbit, Rodents, and the Fox Summary.... The Horizontal Axis: The Visual Streak The Visual Streak of the Rabbit Retina The Visual Streak of the Cat Retina.... Evidence of a Visual Streak in the Monkey and Other Primates. The Opossum: An Exception?... Summary

13 CONTENTS xv 9.5. The Fovea or Area Centralis: A Specialization at the Junction of the Two Axes The Fovea Centralis of the Monkey and Other Primates The Area Centralis of the Cat Evidence of an Area Centralis in the Rabbit Retina Summary Two Regional Specializations Related to the Axis of Nasotemporal Division Nasal-Temporal Gradients in the Properties of Ganglion Cells A Vertical Streak? How Generally Can the Model be Applied? The Generality of the Area Centralis The Generality of the Visual Streak The Generality of the N asotemporal Division of the Retina The Siamese Cat: A Case to Prove Two Points Functional Significance of Regional Specializations The Nasotemporal Division of the Retina The Fovea or Area Centralis and the "Vertical Streak" Nasal-Temporal Differences in Ganglion Cell Properties The Visual Streak Retinal Topography: The Influence of Visual Environment and Phylogenetic Heritage Significance of the Two-Axis Model: A Ground Plan for the Topography of Mammalian Retina On the Understanding of the Visual Pathways' Dependence on the Visual Environment Introduction: Three Starting Points Amblyopia: The Clinical Starting Point The Philosophical Starting Point: Rationalism and Empiricism Animal Models of Amblyopia: The Neurobiologists' Starting Point Summary Effects of Visual Deprivation on the LGN of the Cat The "Loss" of Y Cells from the LGN of Visually Deprived Cats: Its Nature, Morphological Correlates, and Cause An Abnormality of Geniculate X Cells in Visually Deprived Cats: A "Direct" Effect of Deprivation Other Evidence of a "Direct" Mechanism in Visual Deprivation The Effect of Visual Deprivation on W-Class Relay Cells The Effect of Immobilizing the Eye Effects of Visual Deprivation on Cat Retinal Ganglion Cells Effects of Visual Deprivation on the SC of the Cat Effects of Visual Deprivation on the Visual Cortex of the Cat Which Stimulus Selectivities Can Develop without Visual Experience? Determinants of Ocular Dominance Eccentricity-Related Differences in the Modifiability of Orientation Stripes. 347

14 XVI CONTENTS Effects of Visual Deprivation in Other Species In the Monkey In the Tree Shrew Conclusion: W, X, and Y Components of the Neural Basis of Amblyopia On the Understanding of Visual Psychophysics and Behavior Introduction The Focalj Ambient Division of Visual Function and Its Neural Basis The Focalj Ambient Division of Visual Function Evidence in Humans Evidence in Monkeys Evidence in Cats Summary Evidence of Distinct X and Y Contributions to Focal Vision The Dual-Mechanism Hypothesis of the Perception of Form and Motion Qualifications The Oblique Effect: A Psychophysical Correlate of X-Cell Function The Neural Representation of Visual Perception: A Comment Extensions and Limits of the Parallel Processing Analysis Parallel Processing in the Somatosensory Pathways Classification of Somatosensory Afferents Channeling of Submodalities through Spinal Cord and Brain Stem The Parallel Organization of Somatosensory Thalamus The Parallel Organization of Somatosensory Cortex Summary Notes on Other Sensory Pathways The Auditory Pathways The Chemical Senses Ideas and Their Limits "Parametric Systematics": An Approach to the Understanding of Sensory Pathways Two Terms: Reductionist and "Holistic" The Technical Limits of Ideas A "Parametric Systematics" for Sensory Biology References Index