Table Of ContentCONTRIBUTORS TO THIS VOLUME
ENOCH CALLAWAY III ARUNAS PAKULA
Ε. M. EISENSTEIN Β. PERETZ
PHILIP M. GROVES EUGENE N. SOKOLOV
RICHARD M. HILL RICHARD F. THOMPSON
FREDERIC G. WORDEN
HABITUATION
Edited by
HARM AN V. S. PEEKE MICHAEL J. HERZ
Langley Porter Neuropsychiatrie Institute Langley Porter Neuropsychiatrie Institute
University of California University of California
San Francisco, California San Francisco, California
VOLUME II
PHYSIOLOGICAL SUBSTRATES
ACADEMIC PRESS New York and London 1973
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List of Contributors
Numbers in parentheses indicate the pages on which the authors' contributions begin.
ENOCH CALLAWAY 111(153), Department of Psychiatry, University of Califor-
nia, San Francisco Medical Center, San Francisco, California
Ε. M. EISENSTEIN (1), Department of Biophysics, Michigan State University,
East Lansing, Michigan
PHILIP M. GROVES(175), Department of Psychology, University of Colorado,
Boulder, Colorado
RICHARD M. HILL (139), College of Optometry, Ohio State University,
Columbus, Ohio
ARUNAS PAKULA* (35), Department of Psychophysiology, Moscow State
University, Moscow, U.S.S.R.
B. PERETZ (1), Department of Physiology and Biophysics, University of
Kentucky Medical Center, Lexington, Kentucky
EUGENE N. SOKOLOV (35), Department of Psychophysiology, Faculty of
Psychology, Moscow State University, Moscow, U.S.S.R.
RICHARD F. THOMPSON (175), Department of Psychobiology, University of
California, Irvine, California
FREDERIC G. WORDEN (109), Department of Psychiatry, Neurosciences
Research Program, Massachusetts Institute of Technology, Brookline,
Massachusetts
* Present address: Institute for Cardiovascular Research. Kaunas. Lithuania U.S.S.R.
vii
Preface
The phenomenon of habituation, the waningof responsiveness to repeated
or constant stimulation, has received much recent attention. Although
historically dismissed as a functionally insignificant form of behavior, most
contemporary scientists view habituation as a form of adaptive modification
of behavior (learning). The research and theory presented in these volumes
reflect the fact that habituation has recently achieved a position of promin-
ence among investigators concerned with the neurobiology of behavior. The
current interest appears to have evolved from two previously somewhat
separate lines of research which have converged upon a common goal, i.e.,
the understanding of both the behavioral and physiological bases of habitua-
tion.
Early biologists working in apparent isolation provided a foundation of
empirical studies of behavioral response waning in many species, mostly
invertebrates. Later, habituation was accorded a central role in the organism'
adaptive capacity by the inclusion of a chapter on habituation in Humphrey's
"The Nature of Learning" (1933), a source still frequently referenced and
quoted today. Hinde, an ethologist, studying the waning of predator-
mobbing behavior in birds, has demonstrated the field relevance of the
phenomenon in a quasi-natural situation in a series of papers published
between 1954 and 1961. More recently, Thorpe's "Learning and Instinct in
Animals" (1963) placed habituation on a par with classical conditioning
and instrumental learning as an important form of learning. All of these
influences have contributed to the contemporary interest in behavioral
habituation, much of which is reviewed and discussed in the first volume of
this two-volume treatise.
The second major influence on the study of habituation, reflected in the
second volume, has come from the laboratories of neurobiologists who have
demonstrated the plasticity of the nervous system utilizing repeated pre-
sentation of stimuli that have resulted in decrement or cessation of neuronal
activity. While habituation in neurophysiological experiments often is a
much shorter term phenomenon than that observed with behavioral re-
sponses, Thompson and Spencer's (1966) properties of habituation appear
to occur even when responses of single neurons are examined. This similarity
between the neuron and the whole organism has led many investigators to
seek the physiological basis of habituation in terms of neurophysiological
and neurochemical consequences of repeated stimulation in partial organ-
ix
χ PREFACE
ism preparations and then to attempt to relate these results to intact,
behaving animals.
In assembling these volumes we have attempted to cover a good portion
of the literature on behavioral habituation and its substrates by choosing
representatives from the many investigators concerned with this pheno-
menon. While we feel that the work presented represents much of the best
available, many additional chapters could have been added. It is our hope
that this selection of papers presents a fair and representative sample of the
large body of literature available on this subject.
The chapter by Drs. Pakula and Sokolov requires special mention.To our
knowledge, this is the first exposure of some of this Soviet research to
Western readers. The authors gave us permission to edit the chapter in
order to clarify points and to make it more readable. Dr. Bertran Peretz
spent many additional hours on this contribution attempting to clarify points
from his perspective as an expert in the behavior and neurophysiology of
Mollusca. We hope that our efforts have improved understanding and
apologize for any inaccuracies which we may have introduced into the
chapter. We would also like to thank Dr. David Galin who was also
particularly helpful in the editing of one of the chapters, and Dr. Shirley
Peeke who was of immeasurable help in assembling the Subject Index.
We would like to express our appreciation to Dr. Alex Simon, Director of
Langley Porter Neuropsychiatrie Institute and the University of California,
Chairman, Department of Psychiatry who has actively supported our
scholarly and basic research activities. Finally, we would like to especially
thank Dr. Enoch Callaway III, Professor and Chief of Research, for his
personal encouragement as well as for his having created a scientific scholas-
tic atmosphere conducive to free inquiry in the bio-behavioral sciences.
Finally, we would like to express our appreciation to Professor Everett
Wyers, who kindled our interest in habituation and inhibitory processes
while we were still impressionable graduate students and with whom we
have argued for many years about the topics covered in these volumes.
HARMAN V. S. PEEKE
MICHAEL J. HERZ
Contents of Volume I
Behavioral Habituation in Invertebrates
Everett J. Wyers, Harman V. S. Peeke, and Michael J. Herz
Habituation in Fish with Special Reference to Intraspecific Aggressive
Behavior
Harman V. S. Peeke and Shirley C. Peeke
Habituation in "Lower" Tetrapod Vertebrates: Amphibia as Vertebrate
Model Systems
David A. Goodman and Norman M. Weinberger
A Species-Meaningful Analysis of Habituation
Lewis Petrinovich
Habituation and Dishabituation of Responses Innervated by the Auto-
nomic Nervous System
Frances K. Graham
Habituation, Habituability, and Conditioning
H. D. Kimmel
A Dual-Process Theory of Habituation: Theory and Behavior
Richard F. Thompson, Philip M. Groves, Timothy J. Teyler, and Richard
A. Roemer
Author Index-Subject Index
XI
Chapter 7
Comparative Aspects of Habituation
in Invertebrates
Ε. M. EISENSTEIN AND B. PERETZ
I. Introduction 1
II. Habituation in Intact Nervous Systems—Selected Examples 3
III. Ganglionic Changes with Habituation 6
IV. Plasticity in the Absence of Central Ganglia 14
A. Facilitation at Neuromuscular Sites 14
B. Habituation in Peripheral Structures 15
V. Habituation in the Absence of a Nervous System—Protozoa 24
VI. Discussion 27
References 31
I. Introduction
The change in behavior which we term learning has at least two recogniz-
able temporal factors underlying it: (1) the temporal order of events to be
associated or learned and (2) the rate at which stimuli are presented. In
Pavlovian conditioning we recognize that the change in response of the
organism to the conditioned stimulus (CS) is a function of, among other
things, the amount of stimulation [number and intensity of the CS and un-
conditioned stimulus (UCS)] in a given amount of time as well as the tem-
poral order of the CS with respect to UCS.
Habituation is considered to be a more elemental form of learning than
Pavlovian conditioning. It is defined as a progressive decrease in response
amplitude or frequency of occurrence to discrete and repetitive stimuli. It
is also, as is conditioning, dependent on the total number of stimuli pre-
sented per unit time; that is, a loud bell which produces an orienting re-
sponse in a dog will fail to do so at a faster rate the higher the frequency of
stimulus presentation. Habituation studies involve a change in an innate
behavioral response. The neural organization underlying this behavior is
considered less complex than that involved in other kinds of learning. The
aim is to specify the mechanisms involved. The mechanisms underlying
habituation shows plasticity in (a) response decrement to repetitive stimula-
1
2 Ε. Μ. EISENSTEIN AND Β. PERETZ
tion, (b) recovery of responsiveness, and (c) retention of the effects of pre-
vious tests sessions using the same stimulus.
An often less recognized but equally important component in the habit-
uation process is the role of temporal order of stimuli in the response decre-
ment seen. Its role is most clearly seen by the effect on the habituation process
of altering the temporal order of the stimuli presented. If, in the intermittent
presentation of the loud bell in the previous example, another stimulus (or
the same one) is presented out of the previous temporal order, a phenome-
non frequently seen is an erasure or loss of the previous state of habituation;
that is, the probability of response to the stimulus used for habituation tends
to return to its starting level or even exceed it (Groves and Thompson, 1970).
This phenomenon is termed dishabituation 1 and is clearly an example of the
importance of temporal factors in the habituation process as it is in other
kinds of learning (Pumphrey and Rawdon-Smith, 1937; Eisenstein, 1967).
Pavlov (1927) first described behavioral habituation in dogs. (Sherrington,
in 1906, reported a waning of the scratch reflex in the spinalized dog.) In his
review, Harris (1943) stated that representative animals of all phyla display
response decrement to repetitive stimuli.
Until recently little attempt had been made to describe specific properties
associated with behavioral habituation. Thompson and Spencer (1966)
ascribed nine parameters to behavioral habituation which have been ex-
tremely useful in comparing various preparations to a relatively fixed set of
criteria (see Table I).
A number of preparations, intact and semi-intact, from several phyla are
listed in Table I. Interestingly enough, what emerges is that three properties
are common to almost all: response decrement, spontaneous recovery, and
dishabituation. The exceptions are Spirostomum and Stentor, two proto-
zoans which do not appear to dishabituate. Aneural organisms may not
possess this property.
We see then that habituating systems not only show response decrement
but recovery of responsiveness. An apparent difference between aneural
habituating systems and those which contain some level of neural investment
is that the latter display dishabituation. A question to consider is whether
a habituating system requires synapses to possess the type of plasticity mani-
fested by rapid recovery of responsiveness (dishabituation)?
'Throughout this article the term dishabituation is used to describe rapid recovery of re-
sponsiveness after application of a stimulus (often of higher intensity) out of the previous
temporal order to the same or to another sensory field of the animal. This does not argue
against the underlying mechanism's being a type of sensitization (Groves and Thompson,
1970), nor does using the term dishabituation imply a reversal of habituation. The term is
used for convenience.
1. ASPECTS OF HABITUATION IN INVERTEBRATES 3
This review will address itself to (a) comparing habituation across inverte-
brate phyla as well as in various types of surgical preparations, (b) quantita-
tive analysis of habituation, and (c) describing neural correlates of habitua-
tion in selected preparations and suggesting underlying mechanisms.
II. Habituation in Intact Nervous Systems—Selected Examples
Habituation in intact coelenterates has been shown. Rushforth (1965),
working with Hydra, demonstrated that these animals contract when shaken.
When the amount of mechanical agitation was standardized and delivered
intermittently, the percentage of contracting animals gradually diminished
over a 6 to 8-hour period. This response decrement was found to last up to
4 hours after training. It was not the result of fatigue since contractions
could be evoked by a light stimulus after the animals were habituated by
mechanical agitation. Dishabituation has been reported in other coelen-
terates (Harris, 1943).
The nereid polycheates have been shown capable of habituation of the
withdrawal reflex through repetition of mechanical shock, a moving shadow,
and sudden increases or decreases in light intensity. They are also capable
of shock avoidance training. Thus, Clark (1965) has reported that if the
worm is placed at the entrance to a glass tube and is shocked when it crawls
through to the other side, it crawls more slowly on successive trials, often
reversing in the tube to return to the entrance, and eventually refusing to
enter. There is considerable retention for 6 hours but almost no retention
after 24 hours.
Early behavioral habituation experiments with mollusks showed that
snails retained the effects of visual stimuli for at least 24 hours (Piéron, 1909,
1913) and tactile stimuli for several hours (Humphrey, 1930). Also, the rate
of habituation was directly dependent upon stimulus rate and appear to
follow an exponential curve with respect to time (Pieron, 1913). Humphrey
(1930), studying behavioral habituation in the snail, described four of the
nine parameters associated with habituation (Table I). The results also
indicated generalization of habituation to other stimuli occurred in snails
and probably habituation to the dishabituating stimulus.
More recently in a tethered intact Aplysia at least six parameters have been
observed (Pinsker et al., 1970; Kupfermann et al., 1970, see Table I). In other
experiments carried out in intact Aplysia, the siphon can be made to habituate
to either light or tactile stimulation; also, habituation to one stimulus can be
dishabituated by the other (Lukowiak and Jacklet, 1972). Long-term studies
