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The Cat Primary
Visual Cortex
This Page Intentionally Left Blank
The Cat Primary
Visual Cortex
ACADEMIC PRESS
San Diego London Boston New York Sydney Tokyo Toronto
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Orlando, Florida, 32887-6777
Academic Press
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PREFACE XIII
1
THE CONCEPT OF CAT PRIMARY VISUAL CORTEX 1
BERTRAM R. PAYNE AND ALAN PETERS
Prologue 1
Milestones in the Development of the Concept of Cat Primary Visual Cortex 11
Connections 25
Composition of Area 17 39
Comparison of the Architectonics of Areas 17 and 18 and Identification of
Borders 59
Visual Maps in Areas 17 and 18 63
Circuitry and Signal Processing in Areas 17 and 18 76
Visually Guided Behavior 100
Synthesis 102
Recent Challenges to the Primacy of Areas 17 and 18 106
Epilogue 108
2
OPTICAL IMAGING OF FUNCTIONAL ARCHITECTURE IN
CAT PRIMARY VISUAL CORTEX 131
MARK HÜBENER AND TOBIAS BONHOEFFER
Introduction 131
Methodological Aspects of Optical Imaging 132
Optical Imaging of Functional Maps in Cat Visual Cortex 136
Relationships Between Columnar Systems 152
v
VI Contents
3
2-DEOXYGLUCOSE ARCHITECTURE OF CAT PRIMARY
VISUAL CORTEX 167
SIEGRID LÖWEL
Introduction 167
Orientation Domains 170
Ocular Dominance Domains 173
Spatial Frequency Domains 178
Development and Experience-Dependent Changes of Cortical Maps 179
Advantages and Disadvantages of the 2-DG Technique 186
Outlook 188
4
FUNCTIONAL MAPPING IN THE CAT PRIMARY VISUAL
CORTEX USING HIGH MAGNETIC FIELDS 195
DAE-SHIK KIM, TIMOTHY Q. DUONG, KAMIL UGURBIL, AND SEONG-GI KIM
Introduction 195
Limitations of Current Techniques, or Why We Need Another Mapping
Technique 196
Functional Magnetic Resonance Imaging 196
Functional MRI of the Cat Primary Visual Cortex 200
Conclusions 215
5
RELATIONSHIPS OF LGN AFFERENTS AND CORTICAL
EFFERENTS TO CYTOCHROME OXIDASE BLOBS 221
JOANNE A. MATSUBARA AND JAMIE D. BOYD
6
INFLUENCE OF TOPOGRAPHY AND OCULAR DOMINANCE ON
THE FUNCTIONAL ORGANIZATION OF CALLOSAL
CONNECTIONS IN CAT STRIATE CORTEX 259
JAIME F. OLAVARRIA
Introduction 259
The Vertical Meridian Rule 260
Callosal Fibers Interlink Cortical Sites That are in Retinotopic, Rather Than
Anatomical, Correspondence 262
Interhemispheric Correlated Activity Guides Callosal Development 268
Summary and Concluding Remarks 286
7
ESSENTIAL AND SUSTAINING LGN INPUTS TO CAT
PRIMARY VISUAL CORTEX 295
THEODORE G. WEYAND
Introduction 295
The Reversible Inactivation Technique 296
Two Circuits in Area 17 297
Area 18: More Integrative Than Area 17 308
Functional Architecture of Visual Cortex 310
8
INTEGRATION OF THALAMIC INPUTS TO CAT PRIMARY
VISUAL CORTEX 319
R. CLAY REID, JOSE-MANUEL ALONSO, AND W. MARTIN USREY
Introduction 319
Simple Receptive Fields 320
VIII Contents
9
THE EMERGENCE OF DIRECTION SELECTIVITY IN
CAT PRIMARY VISUAL CORTEX 343
ALLEN L. HUMPHREY AND ALAN B. SAUL
Overview 343
Directional Tuning: The Basics 344
Computational Requirements for Direction Selectivity 346
Biological Instantiation of Computational Principles 348
Origins of Cortical Timings: The Lagged/Nonlagged Cell Model 351
Comparison with Recent Models 357
Intracortical Inhibition: Experimental Evidence 360
How are Inputs Combined? 368
Intralaminar and Interlaminar Interactions 376
Summary and Conclusions 377
Future Directions 378
10
LONG-RANGE INTRINSIC CONNECTIONS IN CAT PRIMARY
VISUAL CORTEX 387
KERSTIN E. SCHMIDT AND SIEGRID LÖWEL
Introduction 387
Historical Overview 388
Layout of Long-Range Horizontal Connections 390
Types of Neurons Forming Long-Range Horizontal Connections 393
Synaptic Targets of Long-Range Intrinsic Connections 394
Divergence and Convergence of Long-Range Horizontal Connections at the
Ultrastructural Level 395
Topographic Relations between Long-Range Intrinsic Connections and
Functional Cortical Maps 396
Possible Functions 407
Plasticity of Long-Range Connections in the Adult 410
Conclusions 416
Contents IX
11
PHARMACOLOGICAL STUDIES ON RECEPTIVE
FIELD ARCHITECTURE 427
ULF T. EYSEL
12
ORIENTATION SELECTIVITY AND ITS
MODULATION BY LOCAL AND LONG-RANGE
CONNECTIONS IN VISUAL CORTEX 471
DAVID SOMERS, VALENTIN DRAGOI, AND MRIGANKA SUR
13
RESPONSE SYNCHRONIZATION,
GAMMA OSCILLATIONS, AND PERCEPTUAL BINDING
IN CAT PRIMARY VISUAL CORTEX 521
WOLF SINGER
Introduction 521
Two Complimentary Strategies for the Representation of Relations: Smart
Neurons and Assemblies 523
A Need for Dynamic Response Selection and Binding 525
Dynamic Grouping Mechanisms 530
X Contents
Predictions 533
Response Synchronization in Striate Cortex 533
Response Synchronization, Mechanisms and Properties 534
Relation between Response Synchronization and Perceptual
Phenomena 537
Dependency on Central States and Attention 542
Plasticity of Synchronizing Connections 546
The Impact of Synchronized Responses 549
Gamma Oscillations and Visual Perceptions in Human Subjects 551
Stimulus Locked Synchronization and Perceptual Grouping 552
Conclusions 553
14
THE SPECIAL RELATIONSHIP BETWEEN
β RETINAL GANGLION CELLS AND CAT PRIMARY
VISUAL CORTEX 561
BERTRAM R. PAYNE AND R. JARRETT RUSHMORE
Introduction 561
Identification of Subsystems and Connections 563
Visual System Connections and Function in the Newborn 579
Visual Cortex Lesions 580
Factors Linked to Survival and Death of Ganglion Cells 590
Primates 594
Summary 597
15
PRIMARY VISUAL CORTEX WITHIN THE
CORTICO-CORTICO-THALAMIC NETWORK 609
JACK W. SCANNELL AND MALCOLM. P. YOUNG
Introduction 609
Function 611
Structure 619
Structure-Function Relationships 641
Conclusions 645
Contents XI
16
BEHAVIORAL ANALYSES OF THE CONTRIBUTIONS OF CAT
PRIMARY VISUAL CORTEX TO VISION 655
DONALD E. MITCHELL
Introduction 655
The Behavioral Consequences of Lesions of the Visual Cortex 656
Insights Gained from Cats Reared with Selected Forms of Early Visual
Deprivation 686
Conclusions 687
INDEX 695
This Page Intentionally Left Blank
Preface
We hope that this volume will appeal to those with a specific interest in cat pri-
mary visual cortex, as well as neuroscientists with a general interest in the struc-
ture and operations of cerebral cortical systems. It is estimated by some that more
is known about the cat primary visual cortex than about any other cerebral area, or
even any other structure in the brain of any other species. In recent years, many
new investigative tools and strategies have been used to probe the construction
and workings of this cortex. Together they have enabled us to gather information
of unparalleled quality. Much of this information is contained in this volume.
While the cat visual cortex is recognized to be a premier system for studying
the mysteries of vision, visual processing, cerebral circuitry, and cerebral pro-
cessing, the question has to be asked “ What is cat primary visual cortex?” As we
reason in Chapter 1, we believe that both areas 17 and 18 should be included
under the single umbrella term of “Cat Primary Visual Cortex.” The appropriate-
ness of our view becomes apparent as we review the historical background and
evolution in thinking that emerges from a large number of studies on neural archi-
tecture, connections, anatomical and functional aspects of circuitry, functional
maps, receptive field properties, and contributions that areas 17 and 18 make to
visual processing in the cat. Indeed, from numerous aspects areas 17 and 18 are
very similar: basically, both areas process primary signals from LGN in parallel
and both areas contribute to overall visual processing, but in distinct, yet overlap-
ping, ways.
Subsequent chapters describe the representational architecture of areas 17 and
18 as revealed by optical imaging (Hübener and Bonhoeffer), 2-deoxyglucose
(Löwel), and functional MRI techniques (Kim and colleagues). These chapters
provide an overall view of the functional columnar architecture of cat primary
xiii
XIV Preface
visual cortex at the level of neural systems. This level of analysis provides a per-
spective into which anatomical and electrophysiological analyses of the connec-
tions and neuronal operations can be readily comprehended. The anatomical
studies summarize the organization of afferent and efferent connections within
one hemisphere (Matsubara and Boyd) and between the hemispheres (Olavarria),
and they describe the structural bases for comprehending the fundamental visual
cortex operations that have been revealed by elegant electrophysiological studies
(Weyand; Reid, Alonso, and Usrey; and Humphrey and Saul). Next, the topic of
long-range intrinsic circuitry is reviewed from an anatomical perspective
(Schmidt and Löwel) and from the perspective of emergence of orientation and
direction preferences of neurons as revealed by techniques to reversibly deacti-
vate specific cerebral circuits (Eysel). These reviews are complemented nicely by
the chapter in which Somers, Dragoi, and Sur discuss models to conceptualize the
emergence of orientation selectivity and its modulation by ancillary circuits,
while the chapter by Singer places the neuronal operations of cat primary visual
cortex in the context of overall brain function, gamma oscillations, and perceptual
binding.
The chapter by Payne and Rushmore provides a new view on the special rela-
tionship between β retinal ganglion cells and the primary visual cortex, and the
volume is rounded out with the chapters of Scannell and Young and of Mitchell.
The thought provoking chapter by Scannell and Young analyzes the brain connec-
tivity in which the primary visual cortex is embedded, while Mitchell reviews the
contributions areas 17 and 18 make to vision and visually guided behavior. From
Mitchell’s description we learn the importance of primary visual cortex for high
acuity vision, hyperacuity, and stereoscopic depth perception. In toto these stud-
ies show that comprehensive analyses of enormous breadth and sophistication are
required to probe the structure and function of brain regions. But even using
modern techniques we have, to date, only made a small dent in our comprehen-
sion of the nature of neural signals, transformations, and syntheses carried out by
neurons.
What emerges repeatedly in the chapters is the perspicacity and overarching
role played by David Hubel and Torsten Wiesel in opening up meaningful inves-
tigations of the cat primary visual cortex. Even after 40 years their descriptions of
receptive field properties, connections, and formulations on receptive field prop-
erties and their emergence still have a powerful hold over the way that we think
about visual cortex. Interestingly, in the 1980s many felt that the neural opera-
tions of cat primary visual cortex were well understood, and little additional work
needed to be done. However, all of the chapters in this volume argue otherwise.
They show that while many advances have been made over the previous two
decades, there is still so much more to learn. Particularly important areas that
need to be investigated include the topics of receptive field dynamics, influence of
feedback projections, and imaging of functional representations at ever-finer lev-
els of resolution.
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