The highlight for November is by Sadahiko Nakajima who is at the Department of Psychological Science, Kwansei Gakuin University in Nishinomiya,
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1 The highlight for November is by Sadahiko Nakajima who is at the Department of Psychological Science, Kwansei Gakuin University in Nishinomiya, Japan. Dr. Nakajima s interest and efforts in taste aversion learning have been extensive and have addressed a range of interesting issues (see below). Unlike many researchers in this area who have either examined taste aversions as a specialized form of learning or have sought to understand the dynamics of the phenomenon itself, Dr. Nakajima has primarily used aversion learning as a tool to examine facets of learning in general. Although the use of aversion learning as a tool is not new, such use most recently has been to target the biological bases of learning and memory or to assess issues ranging from satiety to drug use to toxicity. Dr. Nakajima s initial interest focused on understanding learning, and his work has described the clever use of aversion learning in this capacity. For example, using various parametric innovations, he and his colleagues have explored issues as diverse as occasion setting, retroactive inference (backward blocking), the effects of post conditioning exposure to the US (in a conditioned flavor preference model) and the interaction of overshadowing and latent inhibition. Although much of his work has focused on using aversion learning as a procedural variant to examine interesting aspects of associative learning, Dr. Nakajima has also explored a host of issues regarding aversion learning itself. My initial introduction to Dr. Nakajima s research was through this latter work, specifically activity- and swimming-induced aversions. Following up on the initial work by Bow Tong Lett and her colleagues examining aversions induced by wheel running in rats, Dr. Nakajima and his colleagues explored a variety of parametric conditions under which such an effect occurred and then extended these assessments to examine other conditions that might induce such aversions, e.g., swimming. He reported that swimming-induced aversions were sensitive to several parametric conditions known to affect taste aversion learning in general, e.g., duration of US exposure, US history, and described effects consistent with the position that these aversions were a function of energy expenditure. Interestingly, his group has shown similarities between wheel running and LiCl in that a history of one (in this case LiCl) attenuated aversion learning induced by the other (wheel running). His lab is continuing this investigation of the nature of the US of these activity-induced aversions by assessing the effects of swimming on aversions induced by wheel running. Dr. Nakajima s work has shown breadth in the use of the taste aversion design as a tool in assessing general associative learning and as a creative assay to investigate the nature of the US in aversion conditioning.
2 Conditioned taste aversion as a test tube of associative learning Sadahiko Nakajima Professor, Department of Psychological Science, Kwansei Gakuin University, Nishinomiya, Japan Personal history My first encounter with conditioned taste aversion (CTA) was in my final undergraduate year (1988) at Sophia University, Tokyo. After the early submission of a graduation thesis on the resurgence of extinguished operant responding in rats, I had plenty of time before the graduation. My supervisor, the late Prof. Hisashi Hirai, very generously allowed me to freely perform short experiments in various areas, including a bait-shyness study in which thirsty rats tasted lithium chloride (LiCl) solution on a plate in an open field and avoided it the next day. After graduating from Sophia University, I entered Keio University Graduate School, under the supervision of Prof. Masaya Sato, where I obtained an MA in problem-solving behavior in pigeons, followed by a Ph.D. in hierarchical stimulus control (i.e., occasion setting) in pigeons. I was indifferent to CTA in my graduate school days. I was lucky enough to continue behavioral research in the laboratory of Prof. Hiroshi Imada at Kwansei Gakuin University (KGU), Nishinomiya, with a grant from the Japan Society for the Promotion of Science (JSPS), which is a quasi-governmental organization under the auspices of the Ministry of Education, Culture, Sports, Science and Technology (MEXT) of Japan. In this laboratory, I became deeply involved with CTA in rats. The laboratory had sufficient setups for traditional CTA studies such as chemicals, flavor essences, glass tubes, syringes, and electric balances for fine measuring, but when I arrived there, nobody was performing CTA studies. Thus, I learned basic procedures, including intraperitoneal injections, by reading textbooks on the handling of laboratory animals. My first publication on CTA concerned contextual control of CTA in rats (Nakajima, Kobayashi & Imada, 1995), which demonstrated that the background contexts set the occasion for sucrose-licl association. In Imada s laboratory, I met a bright graduate student, Nobuyuki Kawai, who is now an associate professor of Nagoya University. Nobu and I shared an interest in retrospective inference (i.e., the effects of post-conditioning manipulations) in rats and began a series of CTA experiments on backward blocking (attenuation of X aversion acquired by an AX LiCl trial by the post-treatment of A LiCl) and recovery from overshadowing (enhancement of X aversion acquired by an AX LiCl trial by the post-treatment of a non-reinforced A trial). Although we failed to find any sign of retrospective inference in these experiments (Nakajima & Kawai, 1997), our continuing interest in retrospective inference was rewarded after I moved to the laboratory of Prof. Robert A. Rescorla as a JSPS postdoctoral fellow of the research abroad program. In Bob s laboratory, although I did not perform any experiments on CTA, I was influenced by
3 his brilliance and tremendous achievement in associative learning studies. One of the procedures he had developed to clarify the underlying mechanism of associative learning was the post-exposure of an unconditioned stimulus (US). Such a treatment attenuates conditioned fear with an electric shock US (e.g. Rescorla, 1973). The same effect has been demonstrated in CTA (e.g., Colby & Smith, 1977). Nobu (in Nishinomiya) and I (in Philadelphia) started a project involving demonstration of the US post-exposure effect on conditioned flavor preference with a sucrose US as a test of retrospective inference in rats. Nobu conducted the experiments and statistical analyses, while I conceived the designs and prepared the manuscripts. Our overseas collaboration resulted in the successful demonstration of the US post-exposure effect on conditioned flavor preference (Kawai & Nakajima, 1997). After a two-year stay in Philadelphia, where my major research topic was occasion setting and configural learning in pigeons autoshaping, I was called back to Nishinomiya by Prof. Imada to teach his students and manage his animal laboratory as an assistant professor, because he had become the president-to-be of KGU. One of the brightest of his students was Kosuke Sawa, who is now an associate professor of Senshu University, Tokyo. In a sense, he had been on my team before we met one another, because he had done a US post-exposure experiment as an assistant of Nobu (Sawa, Nakajima & Kawai, 1998). My first experiment at KGU was a follow-up of the US post-exposure effect on conditioned flavor preference (Nakajima, 1998). I became the actual supervisor of Kosuke s master thesis on the facilitation of sodium aversion learning in sodium-deprived rats, which was published in Learning and Motivation (Sawa, Nakajima, & Imada, 1999). Kosuke and I also explored reasoning in rats by investigating the acquired equivalence of cues in a CTA preparation as a sideline research project (Sawa & Nakajima, 2001, 2002). Current research topics Although I am engaging in a variety of CTA research, including gustatory discrimination between sodium chloride (NaCl) and LiCl in pigeons (Nakajima & Onimaru, 2006) and discrimination among commercial brands of tea in rats (Masaki, Tatsumi, & Nakajima, 2007), my major interests in CTA rest on the following two topics: 1. Interaction of overshadowing and latent inhibition The stupendous finding reported from the laboratory of Ralph R. Miller (Blaisdell, Bristol, Gunther, & Miller, 1998) that latent inhibition and overshadowing offset each other in rats conditioned fear led me to try to replicate it in rats CTA. This is because such an effect disagrees not only with our intuition but also with many formal theories of Pavlovian conditioning (e.g., Mackintosh, 1975, Pearce & Hall, 1980; Wagner, 1981). According to these theories, latent inhibition and overshadowing should summate rather than counteract each other, resulting in the least conditioned responding in rats exposed to latent inhibition treatment (i.e.,
4 pre-exposure of a target cue) and overshadowing (i.e., presenting another cue in conditioning). Our attempts to demonstrate the counteraction of latent inhibition and overshadowing in CTA were always negative (Nakajima, Ka, Imada, 1999; Nakajima & Nagaishi, 2005; Nagaishi & Nakajima, 2008). In all experiments, our results showed summation rather than counteraction of latent inhibition and overshadowing effects, as expected by intuition and formal theories. One of my students, Takatoshi Nagaishi, and I are currently conducting experiments to resolve the discrepancy between the report from Ralph s laboratory (counteraction) and ours (summation) with various Pavlovian conditioning preparations. 2. Activity-based CTA In 1999, two graduate students, Hiroko Hayashi and Tsukasa Kato, joined Prof. Imada s laboratory from other universities. Because they had no experience of animal study, I had to train them as a drill sergeant. The research topic I chose for them was rats CTA based on voluntary wheel running discovered 3 years ago by Lett and Grant (1996), as I had just learned this unique phenomenon from their second paper (Lett, Grant & Gaborko, 1998). Frankly speaking, I was skeptical about it, since it seemed highly unlikely that voluntary activity would work as an effective US agent to establish CTA. Surprisingly, my concern was shown to be baseless by the data collected by the new recruits under my supervision. This study (Nakajima, Hayashi, & Kato, 1999) is the inception of a series of our research on activity-based CTA in rats. Hiroko finished her master degree program with an excellent study on the procedural variables of running-based CTA (Hayashi, Nakajima, Urushihara, & Imada, 2002). We, however, remained unclear as to why running is an effective US for establishing CTA in rats. An idea that had come to mind was that the energy expended by running is the critical factor for this phenomenon. As rats learn to prefer flavors that are associated with calorific (i.e., energy) restoration, it seems reasonable to assume the opposite process. If energy expenditure works as a US for CTA, other physical activities should also endow rats with CTA. The activity I chose was swimming in a water pool, because it was inexpensive to arrange the setup for such a study, simply requiring the purchase of big garbage pails. However, I later realized that we needed pumps to avoid hurting our backs when emptying the pails The project of swimming-base CTA started with a brilliant undergraduate, Takahisa Masaki, who is now working as a JSPS postdoctoral fellow at Nagoya University. This project yielded a number of orderly behavioral findings (Nakajima & Masaki, 2004; Nakajima, 2004; Masaki & Nakajima, 2004a, 2004b, 2005, 2006, in press). We have also conducted research on running-based CTA to clarify its underlying mechanism by cross-agent familiarizations between running and LiCl (Nakajima, Urata & Ogawa, 2006) or between running and swimming (Nakajima, unpublished data). In addition, we are trying to demonstrate the major features of Pavlovian learning such as cue competition in running-based CTA (Nakajima, 2008; Nagaishi & Nakajima, in press). My sabbatical year in 2007 at the University of Sydney was very helpful to contemplate the mechanism and utility of activity-based CTA. I thank my host, Dr. Robert A. Boakes, Professor Emeritus, for making it possible. Bob and I also co-authored a review paper
5 on activity-based CTA studies (Boakes & Nakajima, 2009). Postscript It s a great honor to be listed in the CTA highlights. I feel like a young boy surrounded by major league baseball players. Although I have published two dozen journal papers on CTA, I remain relatively inexperienced in CTA research compared with the superstars highlighted here. Furthermore, I have never considered myself a CTA researcher because for me CTA is just one of the testtubes of associative learning, which is my central interest. Certainly, CTA is highly useful, but my wish is to develop a much more convenient procedure with which to study associative learning. Even if I say so myself, I will continue research with this testtube because the chance to obtain exciting CTA data is highly rewarding. References Blaisdell, A., Bristol, A., Gunther, L., & Miller, R. R. (1998). Overshadowing and latent inhibition counteract each other: Support for the comparator hypothesis. Journal of Experimental Psychology: Animal Behavior Processes. 24, Boakes, R. A., & Nakajima, S. (2009). Conditioned taste aversions based on running or swimming. In S. Reilly & T. R. Schachtman (Eds.), Conditioned taste aversion: Behavioral and neural processes (pp ). New York: Oxford University Press. Colby, J. J., & Smith, N. F. (1977). The effect of three procedures for eliminating a conditioned taste aversion in the rat. Learning and Motivation. 8, Hayashi, H., Nakajima, S., Urushihara, K., & Imada, H. (2002). Taste avoidance caused by spontaneous wheel running: Effects of duration and delay of wheel confinement. Learning and Motivation, 33, Kawai, N., & Nakajima, S. (1997). US postexposure effect on conditioned flavor preference in the rat. Psychological Record, 47, Lett, B. T., & Grant, V. L. (1996). Wheel running induces conditioned taste aversion in rats trained while hungry and thirsty. Physiology & Behavior, 59, Lett, B. T., Grant, V. L., & Gaborko, L. L. (1998). Wheel running simultaneously induces CTA and facilitates feeding in non-deprived rats. Appetite, 31, Mackintosh, N.J. (1975). A theory of attention: variations in the associability of stimuli with reinforcement. Psychological Review, 82, Masaki, T., & Nakajima, S. (2004a). Swimming-induced taste aversion and its prevention by a
6 prior history of swimming. Learning and Motivation, 35, Masaki, T., & Nakajima, S. (2004b). Taste aversion learning induced by delayed swimming activity. Behavioural Processes, 67, Masaki, T., & Nakajima, S. (2005). Further evidence for conditioned taste aversion induced by forced swimming. Physiology & Behavior, 84, Masaki, T., & Nakajima, S. (2006). Taste aversion in rats induced by forced swimming, voluntary running, forced running, and lithium chloride injection treatments. Physiology & Behavior, 88, Masaki S., & Nakajima, S. (in press). The effect of swimming experience on acquisition and retention of swimming-based taste aversion learning in rats. Learning and Motivation. Masaki, T., Tatsumi, K., & Nakajima, S. (2007). Discrimination of "teas" in rats and humans. Japanese Journal of Animal Psychology, 57, (in Japanese with English abstract) Nagaishi, T., & Nakajima, S. (2008). Further evidence for the summation of latent inhibition and overshadowing in rats' conditioned taste aversion. Learning and Motivation, 39, Nagaishi, T., & Nakajims, S. (in press). Overshadowing of running-based taste aversion learning by another taste cue. Behavioural Processes. Nakajima, S. (1998). Retention of US postexposure effect on conditioned flavor preference in the rat. Japanese Journal of Psychonomic Science, 17, (In Japanese with English abstract) Nakajima, S. (2004). Conditioned ethanol aversion in rats induced by voluntary wheel running, forced swimming, and electric shock: An implication for aversion therapy of alcoholism, Integrative Physiological and Behavioral Science, 39, Nakajima, S. (2008). Effect of extra running on running-based taste aversion in rats. Behavioural Processes, 78, Nakajima, S., Hayashi, H., & Kato, T. (2000). Taste aversion induced by confinement in a running wheel. Behavioural Processes, 49, Nakajima, S, Ka, H, & Imada, H. (1999). Summation of overshadowing and latent inhibition in rats' conditioned taste aversion: Scapegoat technique works for familiar meals. Appetite. 33, Nakajima, S., & Kawai, N. (1997). Failure of retrospective inference in the rats' taste aversion. Japanese Psychological Research, 39, Nakajima, S., Kobayashi, Y., & Imada, H. (1995). Contextual control of taste aversion in rats:
7 The effects of context extinction. Psychological Record, 45, Nakajima, S., & Masaki, T. (2004). Taste aversion learning induced by forced swimming in rats. Physiology & Behavior, 80, Nakajima, S., & Nagaishi, T. (2005). Summation of latent inhibition and overshadowing in a generalized bait shyness paradigm of rats. Behavioural Processes, 69, Nakajima, S., & Onimaru, S. (2005). Salt discrimination in domestic pigeons (Columba livia domestica): Poisonous LiCl solution versus equimolar safe NaCl solution. Journal of Ethology, 24, Nakajima, S., Urata, T., & Ogawa, Y. (2006). Familiarization and cross-familiarization of wheel running and LiCl in conditioned taste aversion. Physiology & Behavior, 88, Rescorla, R. A. (1973). Effect of US habituation following conditioning. Journal of Comparative and Physiological Psychology, 82, Sawa, K. Nakajima, S., & Kawai, N. (1998). Attenuation of conditioned flavor preference by US postexposure in the rats. Japanese Journal of Animal Psychology, 48, (In Japanese with English abstract) Sawa, K., & Nakajima, S. (2001). Reintegration of stimuli after acquired distinctiveness training. Learning and Motivation, 32, Sawa, K., & Nakajima, S. (2002). Acquired equivalence of flavour cues with a common antecedent in rats. Behavioural Processes, 57, 1 6. Sawa, K., Nakajima, S., & Imada, H. (1999). Facilitation of sodium aversion learning in sodium-deprived rats. Learning and Motivation, 30, Pearce, J. M., & Hall, G. (1980). A model for Pavlovian learning: Variations in the effectiveness of conditioned but not of unconditioned stimuli. Psychological Review, 87, Wagner, A. R., (1981). SOP: A model of automatic memory processing in animal behavior. In N. E. Spear & R. R. Miller (Eds.), Information processing in animals: Memory Mechanisms (pp. 5 47). Hillsdale, NJ: Erlbaum.
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