Research Notes in Neural Computing

Managing Editor Bart Kosko

Editorial Board S. Amari M.A. Arbib C. von der Malsburg

Advisory Board Y. Abu-Mostafa A.G. Barto E. Bienenstock J. D. Cowan

M. Cynader W. Freeman G. Gross U. an der Heiden M. Hirsch T. Kohonen 1.W. Moore

L. Optican A.I. Selverston R. Shapley B. Soffer P. Treleaven W. von Seelen B. Widrow S. Zucker

Michael A. Arbib Jorg-Peter Ewert Editors

Visual Structures and

Integrated Functions

With 174 Illustrations

Springer-Verlag Berlin Heidelberg New York

London Paris Tokyo Hong Kong Barcelona

Budapest

Michael A. Arbib Center for Neural Engineering University of Southern California Los Angeles. CA 90089-2520 USA

Managing Editor

Bart Kosko Engineering Image Processing Institute University of Southern California University Park Los Angeles. CA 90089-0782 USA

Jorg-Peter Ewert Universitat Kassel. GhK FB 19 - Abt. Neurobiologie Heinrich-Plett-Str. 40 W-3500 Kassel FRG

ISBN -13 :978-3-540-54241-4 e-ISBN-13 :978-3-642-84545-1

DOl: 10.1007/978-3-642-84545-1

Library of Congre;,;, Cataloging-in-PublIcation Data Visual structures and integrated functions I edited by Michael A. Arblb and lorg-Peter Ewert. -­(Research note;, in neural computing: v. 3) "Papers presented at the Workshop on Vi;,ual Structure;, and Integrated Functions held at the University of Southern Callforllla 111 Lm. Angele;, on Augu;,t 8-10. 1990"--Pref.

1. Visual pathways--Congress. 2. Phy;,iology. Comparative-Congre;,;,. I. Arbib. Michael A. II. Ewert. Jorg-Peter. 1938 III. Workshop on Visual Structures and Integrated FunctlOm ([990: UllIver;,ity of Southern Ca[iforllla) IV. Serie;,. QP475.V6 [99[ 596'.OI823-dc20 9[-223[2

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Preface

This volume integrates theory and experiment to place the study of vision

within the context of the action systems which use visual information. This theme

is developed by stressing:

(a) The importance of situating anyone part of the brain in the context of its

interactions with other parts of the brain in subserving animal behavior. The title

of this volume emphasizes that visual function is to be be viewed in the context of

the integrated functions of the organism.

(b) Both the intrinsic interest of frog and toad as animals in which to study the

neural mechanisms of visuomotor coordination, and the importance of

comparative studies with other organisms so that we may learn from an analysis of

both similarities and differences. The present volume thus supplements our

studies of frog and toad with papers on salamander, bird and reptile, turtle, rat,

gerbil, rabbit, and monkey.

(c) Perhaps most distinctively, the interaction between theory and experiment.

Thus we offer a rich array of models in this volume. High-level schema models

show the basic functional interactions underlying visuomotor coordination, testable

by lesion experiments. Neural network models address data from neurophysiology

and neuroanatomy. We also offer fascinating new data with pointers towards the

way that models must develop to- address them. Although the stress in the

modeling is on Computational Neuroscience (the use of computational methods to

understand neurobiological phenomena), our results have implications for Neural Engineering (the use of ideas inspired, but not necessarily constrained, by the study

of the brain to design highly parallel, often adaptive, machines).

The present volume comprises the papers presented at the "Workshop on

Visual Structures and Integrated Functions" held at the University of Southern

California in Los Angeles on August 8-10, 1990. This Workshop is the fourth in a

series entitled "Visuomotor Coordination in Frog and Toad: Models and

Experiments." These workshops have centered on the evolving body of data about

frog and toad, and on the development of a set of models which together constitute

Rana computatrix, the "frog that computes." The study of Rana computatrix has

VI

implications that go far beyond the study of frogs and toads, per se, and past

workshops - and the present volume - have devoted much space/time to these

implications. It is not so many years ago that the study of invertebrates was regarded

as being, at best, peripheral by the majority of neuroscientists. Yet the increasing

attention to mechanisms of neural function has made Aplysia and other

invertebrates invaluable in the study of basic cellular mechanisms of facilitation,

rhythm generation, and habituation. However, drastic differences in organizational

principles separate the primate brain from the Aplysia nerve net. The study of

"creatures" which "evolve in the computer" can provide opportunities for

understanding organizational principles which are not to be sought solely in terms of cellular mechanisms but in terms of structural constructs (layers and modules),

functional constructs (schemas), and computational strategies (cooperative

computation in neural nets, adaptation, etc.).

As organizers of the meeting, we invited a group of scientists who could between

them address the issues (a) to (c) above of our continuing scientific enterprise. They

responded with lively talks, which generated much discussion to provide

"connective tissue" which greatly strengthened the meeting. To help the reader

gain an understanding of the connection between the papers and the broader

enterprise of which they are a part, we have provided two opening perspectives,

with Arbib reviewing the "Neural Mechanisms of Visuomotor Coordination: The

Evolution of Rana computatrix," while Ewert offers "A Prospectus for the Fruitful

Interaction Between Neuroethology and Neural Engineering." Following these, the

workshop papers have been grouped into sections, each with a unifying theme as set

forth in the following paragraphs:

From the Retina to the Brain: Jeffrey L. Teeters, Frank H. Eeckman, and Frank S.

Werblin build on Teeters' work in developing a leaky integrator model of cells in

frog retina to show how biophysical modeling can be coupled to experiments to help

understand change-sensitive inhibition in ganglion cells of the salamander retina.

Frederic Gaillard and Rene Garcia discuss properties of retinal cells which suggest

that classical ganglion cell types are best seen as representing peaks in a continuum

rather than discrete cell types, and extends this scheme to cells of the nucleus isthmi.

Thomas J. Anastasio provides further insights into distributed representations in

cell populations by showing how the distributed coding in the vestibular nuclei can

be understod in terms of an adaptive technique for identifying properties of cells

VII

mediating the vestibulo-oculomotor reflex in mammals; while Robert F. Waldeck and Edward Gruberg offer new findings about cells of the nucleus isthmi, studying the effects of optic chasm hemisection on the parsing of visual information.

Approach and Avoidance: Information from the two retinas must be combined and gated in an action-dependent way if it is to serve the needs of the organism. Paul Grobstein has shown a parcellation of tectal output which segregates the heading of a prey object from other data about its position. He further finds that these tectal outputs are coded by overall activity in a pathway, rather than by some variant of retinotopic coding. In their two papers, Michael A. Arbib and Alberto Cobas extend this work by providing models of prey-catching and predator avoidance which stress that, whereas stimulus and response direction are the same for prey, different maps are involved for predator location and escape direction. They then provide models of schema interactions which explain Grobstein's data on the medullary hemifield deficit and suggest new experiments on both approach and avoidance. Jim-Shih Liaw and Arbib then provide neural network models for a number of the schemas involved in predator-avoidance, while David J. Ingle provides exciting new data on "triggering" and "biasing" systems in avoidance behavior. The last two papers in this section introduce a comparative dimension. Paul Dean and Peter Redgrave discuss the involvement of the rat superior colliculus in approach and avoidance behaviors (most mammalian studies .note only its role in approach movements, as in visual saccades) while Colin G. Ellard and Melvyn A. Goodale offer data, on the computation of absolute distance in a visuomotor task by the mongolian gerbil, which is most suggestive for future modeling.

Generating Motor Trajectories: The previous sections show how visual data enters the brain, and give a high level view of the overall interactions involved in processing those data to commit the animal to some form of approach or avoidance behavior. This section looks briefly at the actual generation of motor behavior. Simon Giszter, Ferdinando A. Mussa-Ivaldi and Emilio Bizzi report experiments on the coding of motor space in the frog spinal cord which suggest that a wide variety of stimulation sites code for the movement of the frog's leg towards some (site­dependent) equilibrium situation. Reza Shadmehr's theoretical analysis of movement generation with kinematically redundant biological limbs provides a general limb control strategy consistent with this "equilibrium point hypothesis."

VIII

Finally, Ananda Weerasuriya focuses on non-limb movements by analyzing data on

motor pattern generators in anuran prey capture and providing pointers to neural

modeling of their interactions.

From Tectum to Forebrain: In many studies of visumotor coordination in frog and

toad, the central role is given to the tectum and its close associates the pretectum

and nucleus isthmi. Here we see that forebrain structures must be taken into

account as well, and we complement studies of frog and toad with comparative

studies of turtles, birds, and monkeys. Ingle explores the role of frog striatum in frog

spatial memory, and looks at mammalian homologies which are explored in greater

detail in the model by Peter F. Dominey and Arbib of the way in which many brain

regions interact in generation of delayed and multiple saccades in primates. Ewert,

N. Matsumoto, W.W. Schwippert and T.W. Beneke extend the data base on the

interactions of tectum and forebrain in toads by providing intracellular studies on

how striato-pretecto-tectal connections provide a substrate for arousing the toad's

response to prey. Philip S. Ulinski, Linda J. Larson-Prior and N. Traverse Slater

offer insights for comparative modeling with data on cortical circuitry underlying

visual motion analysis in turtles, while Toru Shimizu and Harvey Karten's

comparative study of evolutionary origins of the representation of visual space

show that structures brought together in laminated cortex in mammals may be

segregated in other species raises interesting questions about the utility of layered

structures in the brain. Finally, Edmund T. Rolls completes our comparative

analysis of forebrain mechanisms by with a study of information representation in

temporal lobe visual cortical areas of macaques.

Development, Modulation, Learning, and Habituation: The final section of this

volume considers how the nervous system changes on a variety of time scales.

Sarah Bottjer's study of hormonal regulation of birdsong development provides a

comparative dimension for the study by Albert Herrera and Michael Regnier of

hormonal regulation of behavior in male frogs, in which they present data on how

androgens control the neuromuscular substrate for amplexus (clasping) during the

mating season. Gabor Bartha, Richard F. Thompson and Mark A. Gluck provide a

study of sensorimotor learning and cerebellum which shows how modeling and

data are being integrated in the study of conditioning in rabbits. The volume closes

with three papers which exhibit the successful integration of theory and experiment

IX

in the study of basic learning behaviors in toads. Francisco Cervantes-Perez, Angel

D. Guevara-Pozas and Alberto A. Herrera-Becerra analyze data and modeling of the

modulation of prey-catching behavior. C. Merkel-Harff and Ewert expand the data

base with their study of learning-related modulation of toad's responses to prey by

neural loops involving the forebrain, while DeLiang Wang, Arbib and Ewert report

a dialog between modeling and experimentation in unravelling the dishabituation

hierarchy revealed in visual pattern discrimination in toads.

The meeting and this volume were made possible in part by funds from the

Industrial Affiliates Program of the Center for Neural Engineering (CNE) and from

the Program in Neural, Informational and Behavioral Sciences (NIBS) of the

University of Southern California, as well as from NIH grant lROl-NS24926 to

Michael Arbib. As such, they are part of the continuing dialogue between the study

of living brains and the study of neural network technology maintained by the

faculty and students of CNE and NIBS, as well as part of a continuing pattern of

international cooperation in seeking to integrate theory and experiment in our

efforts to understand the function of the brain in animal and human behavior, and

to probe the implications of that understanding for "perceptual robotics." We

would also like to record our warm thanks to Paulina Baligod-Tagle and her

assistant Hao Cao for all their aid in the organization and conduct of the Workshop.

Michael A. Arbib

J6rg-Peter Ewert

Table of Contents

Overview ..................................................................................................................................... 1

Michael A. Arbib: Neural Mechanisms of Visuomotor Coordination:

The Evolution of Rana computatrix ...................................................................................... 3

Jorg-Peter Ewert: A Prospectus for the Fruitful Interaction Between

Neuroethology and Neural Engineering ........................................................................... 31

From the Retina to the Brain ............................................................................................... 57

Jeffrey L. Teeters, Frank H. Eeckman, and Frank S. Werblin: A Computer Model

to Visualize Change Sensitive Responses in the Salamander Retina ......................... 59

Frederic Gaillard and Rene Garcia: Properties of Retinal and Retino-Tecto-

Isthmo-Tectal Units in Frogs ................................................................................................ 75

Thomas J. Anastasio: Distributed Processing in Vestibulo-Ocular and Other

Oculomotor Subsystems in Monkeys and Cats ................................................................. 95

Robert F. Waldeck and Edward R Gruberg: Optic Chiasm Hemisection and the

Parsing of Visual Information in Frogs ............................................................................. 111

Approach and Avoidance .................................................................................................... 123

Paul Grobstein: Directed Movement in the Frog: A Closer Look at a Central

Representation of Spatial Location .................................................................................... 125

Michael A. Arbib and Alberto Cobas: Prey-Catching and Predator Avoidance 1:

Maps and Schemas ................................................................................................................ 139

Alberto Cobas and Michael A. Arbib: Prey-Catching and Predator Avoidance 2:

Modeling the Medullary Hemifield Deficit ..................................................................... 153

Jim-Shih Liaw and Michael A. Arbib: A Neural Network Model for Response to

Looming Objects by Frog and Toad .................................................................................... 167

David J. Ingle: Control of Frog Evasive Direction: Triggering and Biasing

Systems ...................................................................................................................................... 181

Paul Dean and Peter Redgrave: Approach and Avoidance Systems in the Rat ....... 191

Colin G. Ellard and Melvyn A. Goodale: Computation of Absolute Distance

in the Mongolian Gerbil (Meriones unguiculatus): Depth Algorithms and

Neural Substrates ................................................................................................................... 205

XII

Generating Motor Trajectories ............................................................................................ 221

Simon Giszter, Ferdinando A. Mussa-Ivaldi and Emilio Bizzi: Equilibrium Point

Mechanisms in the Spinal Frog .......................................................................................... 223

Reza Shadmehr: Actuator and Kinematic Redundancy in Biological Motor

Control ..................................................................................................................................... 239

Ananda Weerasuriya: Motor Pattern Generators in Anuran Prey Capture ............. 255

From Tectum to Forebrain ................................................................................................... 271

David J. Ingle: The Striatum and Short-Term Spatial Memory: From Frog to

Man ........................................................................................................................................... 273

Peter F. Dominey and Michael A. Arbib: Multiple Brain Regions Cooperate in

Sequential Saccade Generation ........................................................................................... 281

J.-P. Ewert, N. Matsumoto, W. W. Schwippert and T. W. Beneke: Striato-Pretecto-

Tectal Connections: A Substrate for Arousing the Toad's Response to Prey ............ 297

Philip S. Ulinski, Linda J. Larson-Prior and N. Traverse Slater: Cortical Circuitry

Underlying Visual Motion Analysis in Turtles .............................................................. 307

Toru Shimizu and Harvey J. Karten: Computational Significance of Lamination

of the Telencephalon ............................................................................................................. 325

Edmund T. Rolls: Information Processing in the Temporal Lobe Visual Cortical

Areas of Macaques ................................................................................................................. 339

Development, Modulation, Learning, and Habituation ............................................... 353

Sarah W. Bottjer: Neural Mechanisms of Song Learning in a Passerine Bird ......... 355

Albert A. Herrera and Michael Regnier: Hormonal Regulation of Motor Systems:

How Androgens Control Amplexus (Clasping) in Male Frogs ................................... 369

Gabor T. Bartha, Richard F. Thompson and Mark A. Gluck: Sensorimotor

Learning and the Cerebellum ............................................................................................. 381

Francisco Cervantes-Perez, Angel D. Guevara-Pozas and Alberto A. Herrera-Becerra:

Modulation of Prey-Catching Behavior in Toads: Data and Modeling ...................... 397

C. Merkel-Harff and J.-P. Ewert: Learning-Related Modulation of Toad's

Responses to Prey by Neural Loops Involving the Forebrain ..................................... 417

De Liang Wang, Michael A. Arbib and Jorg-Peter Ewert: Dishabituation

Hierarchies for Visual Pattern Discrimination in Toads: A Dialog Between

Modeling and Experimentation .......................................................................................... 427