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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 1 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. 2 Berger, T.W., & Orr, W.B. (1983). Hippocampectomy selectively disrupts discrimination reversal conditioning of the rabbit nictitating membrane response. Behavioural Brain Research, 8, 49–68. Daum, I., Channon, S., & Canavan, A.G.M. (1989). Classical conditioning in patients with severe memory problems. Journal of Neurology, Neurosurgery, and Psychiatry, 52, 47–51. Daum, I., Channon, S., & Gray, J.A. (1992). Classical conditioning after temporal lobe lesions in man: Sparing of simple discrimination and extinction. Behavioural Brain Research, 52, 159–165. Gabrieli, J.D.E., McGlinchey-Berroth, R., Carrillo, M.C., Gluck, M.A., Cermak, L.S., & Disterhoft, J.F. (1995). Intact delay-eyeblink classical conditioning in amnesia. Behavioral Neuroscience, 109, 819–827. Green, J.T., & Woodruff-Pak, D.S. (1998). Eyeblink classical conditioning: Hippocampus is for multiple associations as cerebellum is for association-response. Manuscript submitted for publication. Logan, C.G., & Grafton, S.T. (1995). Functional anatomy of human eyeblink conditioning determined with regional cerebral glucose metabolism and positron emission tomography. Proceedings of the National Academy of Sciences, USA, 92, 7500–7504. McGlinchey-Berroth, R., Carrillo, M.C., Gabrieli, J.D.E., Brawn, C.M., & Disterhoft, J.F. (1997). Impaired trace eyeblink conditioning in bilateral, medial-temporal lobe amnesia. Behavioral Neuroscience, 111, 873–882. Mowrer, O.H. (1960). Learning theory and behavior. New York: Wiley. Moyer, J.R., Deyo, R.A., & Disterhoft, J.F. (1990). Hippocampectomy disrupts trace eyeblink conditioning in rabbits. Behavioral Neuroscience, 104, 243–252. Papka, M., Ivry, R.B., & Woodruff-Pak, D.S. (1995). Selective disruption of eyeblink classical conditioning by concurrent tapping. NeuroReport, 6, 1493–1497. VOL. 10, NO.1, JANUARY 1999 PSYCHOLOGICAL SCIENCE Diana S. Woodruff-Pak Schmaltz, L.W., & Theios, J. (1972). Acquisition and extinction of a classically conditioned response in hippocampectomized rabbits (Oryctolagus cuniculus). Journal of Comparative and Physiological Psychology, 79, 328–333. Sears, L.L., Finn, P.R., & Steinmetz, J.E. (1994). Abnormal classical eye-blink conditioning in autism. Journal of Autism and Developmental Disorders, 24, 737–751. Squire, L.R. (1992). Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans. Psychological Review, 99, 195–231. Thompson, R.F., Bao, S., Chen, L., Cipriano, B.D., Grethe, J.S., Kim, J.J., Thompson, J.K., Tracy, J.A., Weninger, M.S., & Krupa, D.J. (1997). Associative learning. In VOL. 10, NO. 1, JANUARY 1999 R.J. Bradley, R.A. Harris, & P. Jenner (Series Eds.) & J.D. Schmahmann (Vol. Ed.), International review of neurobiology: Vol. 41. The cerebellum and cognition (pp. 152–189). San Diego: Academic Press. Weikart, C.L., & Berger, T.W. (1986). Hippocampal lesions disrupt classical conditioning of cross-modality reversal learning of the rabbit nictitating membrane response. Behavioural Brain Research, 22, 85–89. Woodruff-Pak, D.S., & Coleman-Valencia, C. (1998). Awareness facilitates learning in the long-trace paradigm. Unpublished manuscript, Temple University, Philadelphia. 3