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PSYCHOLOGICAL SCIENCE
Special Section
NEW DIRECTIONS FOR A CLASSICAL PARADIGM:
Human Eyeblink Conditioning
Diana S. Woodruff-Pak
Temple University
Abstract—The knowledge base on neural substrates and mechanisms
involved in classical eyeblink conditioning makes it an ideal paradigm
for investigating fundamental issues in learning and memory. New
applications for the model system presented here include its use in (a)
assessment to evaluate neurocognitive development in infancy, (b) theory building in abnormal psychology to test relationships between
obsessive-compulsive behavior and learning rate, (c) evaluation of
hypotheses about brain memory systems, and (d) exploration of the
role of brain structures such as the cerebellum in learning and timing.
Human eyeblink conditioning is a prototype of the utility of a model
system that has become well characterized at both the behavioral and
the neurobiological levels.
A major question for psychologists and neuroscientists alike is,
“How are new associations formed?” A model paradigm for the study
of associative learning about which there is an abundance of psychological and neuroscientific data is eyeblink classical conditioning.
Now that fundamental neural circuitry and neurobiological mechanisms as well as behavioral attributes have been elaborated, there is
renewed interest in this classical method for studying associative
learning in humans. In this section of Psychological Science, we identify some promising new directions for research on human eyeblink
classical conditioning in domains ranging from theory to clinical
application.
Taking a theoretical perspective to the clinic, Tracy, Ghose, Stecher, McFall, and Steinmetz relate eyeblink conditioning to obsessivecompulsive disorder (OCD). Although the leading treatment of OCD
is based on learning theory (Mowrer, 1960), associative learning in
OCD has apparently not been assessed directly until now. The results
Tracy et al. obtained support Mowrer’s theory: Eyeblink conditioning
was more rapid in participants with high OCD scores. This groundbreaking application opens a new research domain in which the neural and pharmacological bases of rapid learning in OCD can be
explored, and it provides a promising means to develop and understand more fully the therapeutic regimens.
There is almost complete identification of the neural circuitry
underlying eyeblink classical conditioning in several mammalian
species (Thompson et al., 1997). The essential site of the plasticity for
learning in all eyeblink conditioning paradigms resides in the cerebellum, and the hippocampus modulates learning in some paradigms and
is essential in others. Recent research with normal human adults using
positron emission tomography (PET; e.g., Logan & Grafton, 1995)
and dual-task paradigms (e.g., Papka, Ivry, & Woodruff-Pak, 1995), as
well as recent work with patients with neurological disease (e.g.,
Sears, Finn, & Steinmetz, 1994), extends the animal model system to
Address correspondence to Diana S. Woodruff-Pak, Department of Psychology, 1701 N. 13th St., Temple University, Philadelphia, PA 19122; e-mail:
[email protected].
VOL. 10, NO. 1, JANUARY 1999
There’s still life in one of psychology’s oldest paradigms. In
this Special Section, PS prints articles derived from a symposium on human classical eyeblink conditioning presented at the
May 1998 meeting of the American Psychological Society in
Washington, D.C.
humans and demonstrates dramatic parallels among mammals in the
brain structures engaged in eyeblink classical conditioning.
In addition to the neurobiological parallels among mammalian
species, there are dramatic parallels in eyeblink conditioning in development over the life span. Most of the life-span data have been collected among adults, and it has been demonstrated that age-related
eyeblink conditioning deficits appear in rats, rabbits, and humans in
middle age. In this issue, Ivkovich, Collins, Eckerman, Krasnegor, and
Stanton make an important contribution by describing techniques and
results with eyeblink classical conditioning in 4- and 5-month-old
infants. This approach has the potential to offer fundamentally important data on the early development of cognitive and neural processes
in associative learning, as well as to provide a tool for testing infants
at high risk for neurobehavioral disorders.
The basic classical conditioning paradigm, called the delay paradigm, involves the presentation of a neutral stimulus, the conditioned
stimulus (CS), followed by the reflex-eliciting unconditioned stimulus
(US). Learning occurs when the organism associates the CS with the
US, producing a conditioned response (CR). A widely used variant of
the delay paradigm is the trace paradigm (so named by Ivan Pavlov),
in which the offset of the CS precedes a blank trace period when no
stimuli are presented. To produce CRs, the organism must associate
the CS and US even though they do not overlap. Some classical conditioning paradigms use more than one CS. In the discrimination paradigm, the CS+ is always followed by a US, whereas the CS– is never
followed by a US. The discrimination-reversal paradigm reverses the
contingency, so that the former CS+ becomes the CS– and the former
CS– becomes the CS+.
In its relevance to brain memory systems in cognitive neuroscience, eyeblink conditioning has added yet another dimension of
interest. Investigators have proposed models in which conscious memory, termed declarative memory, is critically linked to the integrity of
the hippocampus and medial temporal lobe structures (Squire, 1992).
In contrast, nondeclarative, or unconscious, memory systems do not
require these structures. The role of the hippocampus and medial temporal lobe in various eyeblink classical conditioning paradigms results
in one group of paradigms being nondeclarative and another group
being declarative (Green & Woodruff-Pak, 1998). (See Table 1.)
The article in this issue by Clark and Squire focuses on one of the
defining features of the brain’s memory systems: awareness. These
investigators implemented a clever design to manipulate awareness,
and the ensuing results clarify more than previous work the fact that
Copyright © 1999 American Psychological Society
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PSYCHOLOGICAL SCIENCE
New Directions
Table 1. Eyeblink classical conditioning: Paradigms, memory systems, and example studies
Example studies
Paradigm
Memory system
Nonhuman mammals
Humans
Delay
Trace
Nondeclarative
Declarative
Schmaltz and Theios (1972)
Moyer, Deyo, and Disterhoft (1990)
Discrimination
Discrimination reversal
Nondeclarative
Declarative
Berger and Orr (1983)
Weikart and Berger (1986)
Gabrieli et al. (1995)
McGlinchey-Berroth, Carrillo,
Gabrieli, Brawn, and Disterhoft (1997)
Daum, Channon, and Gray (1992)
Daum, Channon, and Canavan (1989)
Note. The declarative form of learning and memory requires the hippocampus and medial temporal lobe structures, but nondeclarative learning and
memory occurs in the absence of the hippocampus.
awareness is essential for conditioning in the trace paradigm but not in
the delay paradigm. This result is robust. Clark and Squire tested older
adults, used a true/false questionnaire to determine awareness, and
embedded the trace paradigm in discrimination conditioning. Employing the trace paradigm alone, testing young participants in the age
range of 15 to 30 years, and using a very different awareness questionnaire, Coleman-Valencia and I replicated the results, finding that
striking differences between groups emerged in the first 10 trials of
conditioning (see Fig. 1; Woodruff-Pak & Coleman-Valencia, 1998).
Much remains to be determined about the neural pathways connecting the medial temporal lobes and the cerebellum and about the
functional interactions among the cerebellum, hippocampus, and related structures. The timing of activations between the hippocampus and
cerebellum may be a critical feature of learning. The cerebellum must
have information input simultaneously or in close temporal proximity
in order to form an association. It is the hippocampus and neocortex
that hold sequentially presented bits of information that can be read
out together and input to the cerebellum at the critical time.
Timing is of central importance in the neural and cognitive bases
of perception, learning, and action. The experiments Green, Ivry, and
I report in this issue drew upon Weber’s law and the perception of temporal intervals to address timing in the cerebellum. To determine if
two quite different tasks, timed-interval tapping and eyeblink classical
conditioning, have a common timing substrate, we tested the tasks
over common intervals. Variability changed in a similar manner in the
two tasks, suggesting a common timing mechanism. This novel
approach provides a new tool for determining commonalities and differences between tasks, as well as for comparing the effects of lesions
in different neural systems.
Human eyeblink conditioning has seen a revival, perhaps driven by
neurobiological research on the animal models. Here we present some
of the vigorous new directions arising from this renaissance.
REFERENCES
Fig. 1. Percentage of participants who produced a conditioned
response (CR) in each of the first 10 conditioning trials in a trace eyeblink classical conditioning paradigm (Woodruff-Pak & ColemanValencia, 1998). The paradigm used a 400-ms, 1-kHz, 80-dB-SPL
tone as the conditioned stimulus (CS), a 1,000-ms trace interval, and a
100-ms, 7-psi corneal airpuff as the unconditioned stimulus (US).
Thus, the CS-US interval was 1,400 ms. Participants ranged in age
from 15 to 30 years. Awareness of the contingency between the tone
CS and producing an eyeblink CR was measured by a postconditioning questionnaire: The 6 “aware” subjects agreed with statements that
their blinking was related to the tone, whereas the 11 “unaware” subjects disagreed with the statements.
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VOL. 10, NO.1, JANUARY 1999
PSYCHOLOGICAL SCIENCE
Diana S. Woodruff-Pak
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