Multiple memory systems and extinction

Abstract

Several lines of evidence suggest that initial acquisition of learned behavior involves multiple memory systems. In particular, lesions of the hippocampus impair the acquisition of cognitive or relational memory, but do not impair the acquisition of stimulus-response habits. Extinction behavior also involves new learning, and therefore it is possible that multiple forms of memory may also underlie extinction. We examined this hypothesis by training rats in a task in which extinction behavior could putatively be acquired by either a cognitive or habit memory system. Adult male Long-Evans rats were initially trained to run in a straight alley maze for food reward. Following training they were placed into one of two extinction conditions. In one condition rats were allowed to run to an empty goal box (i.e. response extinction). In a second condition rats were placed into an empty goal box without making a running response (i.e. latent or non-response extinction). Prior to each daily session of extinction training, rats received intra-hippocampal infusions of either the local anesthetic bupivacaine (0.75% solution/0.5 ul), or saline. Rats receiving saline infusions displayed extinction behavior in both the response and non-response conditions. In contrast, rats receiving intra-hippocampal infusions ofbupivacaine extinguished normally in the response condition, but did not display nonresponse extinction. This latent extinction effect was enhanced by decreasing the amount of time between the last extinction trial and the probe trial. Additionally, administering extinction training and probe trials in different contexts did not appear to prevent latent extinction, however large variability may be masking this effect. The new context administered during extinction prevented latent extinction in some animals, but not others. These findings suggest that, similar to initial acquisition, the learning that occurs during extinction also involves multiple memory systems. Specifically, the hippocampus may selectively mediate extinction under conditions in which new stimulus-response learning is prevented.