Normal olfactory discrimination learning set and facilitation of reversal learning after medial-temporal damage in rats: implications for an account of preserved learning abilities in amnesia

Abstract

Recent evidence of preserved skill learning in patients with "global" amnesia has led to the postulation of a qualitative distinction between functionally separate memory systems, one of which may remain preserved when the other is profoundly impaired. On one account, the separate memory systems support either the learning of declarative knowledge, i.e., facts and associations, or the learning of procedural knowledge, i.e., knowledge that permits the expression of skilled performance without reference to specific facts or associations. In an effort to develop a rodent model of amnesia that illustrates the same distinction between memory systems, rats were trained in a series of discrimination and reversal problems using olfaction, a sensory modality in which they rapidly learn new associations. Rats with bilateral fornix, amygdala, or combined fornix and amygdala damage learned successive two-odor discriminations as quickly as normal and sham-operated control subjects.Furthermore, all groups rapidly acquired the skills of discrimination as revealed in the development of a learning set. Subsequent presentation of a reversal of one discrimination elicited a marked dissociation among groups: Normal rats and rats with amygdala lesions required many more trials to acquire the reversal than to acquire a new discrimination problem, whereas rats with fornix lesions learned the reversal rather easily. A detailed analysis of response strategies suggested that normal rats and rats with amygdala lesions first extinguished the prior response tendencies and then abandoned the learning set skills and treated the reversal much as they did the initial discrimination problem. In contrast, after prior response tendencies were extinguished, rats with fornix lesions were relatively unaffected by the prior cue-associations and treated the reversal much as they would a new discrimination problem. These results distinguish between impaired and spared memory capacities in rodents with amnesia, in conformance with findings on human amnesia.Until recently, investigators involved in developing animal models of amnesia have reported discrepancies in the phenomenology of behavioral impairment after comparable lesions in humans versus animals. Thus, whereas the memory disorder in human amnesic patients is remarkably pervasive, affecting many different categories of material, animals with lesions in the same brain structures suffer a rather more limited behavioral impairment. In particular, early experimenters were dismayed to

Reinstatement of Alcohol-Seeking Behavior by Drug-Associated Discriminative Stimuli after Prolonged Extinction in the Rat

“…In fact, the presence of olfactory cues while rats were waiting for ethanol or water to become available was inherent to the training procedures, since the odor of the respective drinking solution was able to escape from the tubing supplying the drinking reservoirs within the operant chambers. It appears that these odors served as effective S⌬s for ethanol vs. water availability and, in fact, superseded the predictive value of the auditory S⌬s, which is not surprising in a species in which olfaction is the primary sensory modality (Eichenbaum et al 1986(Eichenbaum et al , 1989Slotnick and Katz 1974). In addition, the odor of the drinking solutions became available earlier in the training sessions than the auditory cues, a circumstance that may have added to the greater efficacy of the olfactory over the auditory S⌬s.…”

Differential effects of fornix and caudate nucleus lesions on two radial maze tasks: evidence for multiple memory systems

“…Other learning paradigms in which hippocampal/fomix lesions have similar effects include various avoidance tasks (see O'Keefe and Nadel, 1978) cue-guided lever press alternation (Stevens and Cowey, 1972) 2-bar alternation (Jackson and Strong, 1969) single-bar go/no go alternation olfactory discrimination reversal (Eichenbaum et al, 1986;Fagan and Olton, 1986) and successive cue go/no go olfactory discrimination (Eichenbaum et al, 1988). …”

“…Hippocampal damage in rats causes deficits in the acquisition of various learning tasks (Hirsh, 1974;O'Keefe and Nadel, 1978;Olton, 1978) while sparing the acquisition of others (Silveria and Kimble, 1968;Harley, 1972;Samuels, 1972;Eichenbaum et al, 1986). The types of tasks in which learning is spared following hippocampal damage typically involve the consistent performance of a single response in the presence of a specific sensory cue.…”

Dynamic Analysis of Learning in Behavioral Experiments

“…This technique, based on using the binomial test in a sliding window, has been used frequently to identify a learning trial (Eichenbaum et al, 1986). The moving average method estimates the learning curve by computing in a series of overlapping windows of length 2w ϩ 1 the probability of a correct response at trial k as follows:…”