Research reportIbotenic acid lesions of the amygdala basolateral complex or central nucleus differentially effect the response to reductions in reward
Introduction
It has long been known that rats show impaired performance of rewarded runway approach behavior when the magnitude of the reward is reduced. This effect, described initially by Crespi [8]and also known as successive negative behavioral contrast[14]is typically interpreted as resulting from an aversive emotional reaction to the reduction in reward magnitude 1, 2. A number of studies employing reward reduction in different tasks have reported that lesions of the amygdaloid complex block the response to reductions in reward magnitude 5, 20, 21, 22, 23, 24. However, because all of these studies induced amygdala lesions by radio frequency or electrolytic current, the elimination of behavioral contrast resulting from amygdala lesions induced by these techniques might be attributable either to damage to amygdala nuclei or to destruction of fibers of passage.
The view that the blocking of behavioral contrast is due to amygdala damage is suggested by evidence implicating the amygdala in endocrinological and autonomic responses correlated with emotional states 10, 13, 17and in emotion 26, 39. Furthermore, recent evidence indicating that neurotoxic lesions of the amygdala induced before training impair attentional processes involved in appetitive learning suggests that such an impairment could also affect the response to reward reduction [15]. However, fibers from piriform cortex pass through the amygdala [16]. In the rat, piriform cortex has functional projections to prefrontal cortex [7], including areas known to be part of the extrapyramidal motor system and also areas known to be involved in gustation 19, 38. Further, lesions of the olfactory bulb which would partially deafferent the piriform cortex impair the development of the negative contrast effect [9]. Thus, damage to these fibers may underlie, or contribute to, the effects on the response to reward reduction seen in prior amygdala lesion studies. In order to investigate the selective involvement of amygdala cell bodies in the response to reward reduction, ibotenic acid lesions of the amygdala were induced after acquisition of a food-motivated runway approach task, but prior to a reward reduction. Large lesions were made which included both the central and basolateral/lateral amygdala nuclei in Experiment One. However, consistent with evidence of anatomical and neurochemical heterogeneity of the amygdaloid complex [11]there is extensive evidence indicating that the effects of a particular amygdala nucleus lesion will differ from those of a discete lesion of another nucleus or of a large gross lesion. For example, neurotoxic lesions of the central nucleus have little or no effect on the acquisition of multiple trial inhibitory avoidance, taste potentiated odor aversion, and visual discrimination 18, 31, 36but basolateral lesions impair acquisition of these same tasks 3, 18, 30, 31. Experiment Two examined the involvement of individual amygdala nuclei in the acquisition of the response to a reduction in reward. Discrete bilateral ibotenic acid lesions of the central nucleus or the basolateral/lateral complex of the amygdala were induced after training.
Section snippets
Subjects
Male Sprague-Dawley rats (175–200 g on arrival from Charles River Labs., Wilmington, MA) were used. All rats were individually housed and maintained on a 12:12-h light/dark cycle (lights on at 07.00 h) with food and water available ad lib prior to the beginning of the experiments.
Surgery
Approximately one week after arrival, the rats were anesthetized (87% Ketaset/13% Rompum, 1.2 ml/kg, i.p.) and underwent standard stereotaxic surgery. Bilateral guide cannulae (15 mm length) were implanted with the
Histology
In both experiments we observed considerable atrophy of the lesion site, presumably due to a 2–3 week survival after the lesions were induced.
Experiment one
On the basis of reward and lesion history, the animals were assigned to one of four groups, Unshifted-Sham (n = 6), Unshifted-Lesion (n = 6), Shifted-Sham (n = 6), or Shifted-Lesion (n = 6). Analysis of postlesion/preshift performance on Days 9–11 showed that lesions did not significantly affect the learned runway approach response. The mean runway
Discussion
The findings of Experiment One suggest that large neurotoxic lesions of the amygdala administered after acquisition of a food-motivated runway approach task but prior to a reward reduction do not impair retention of the prior rewarded training or the learning of the aversiveness of the reduced reward. First, the Shifted-Sham and Shifted-Lesion groups increased their latencies in response to reward reduction on the initial day of shift (Day 12). Both groups exhibited a peak increase in mean
Acknowledgements
This research was supported by NSF Graduate Fellowship RCD-9054728 and American Psychological Association Minority Research Fellowship 2 T32 MH 18882 (J.A.S.), 1967 Natural Science and Engineering Research Council of Canada fellowship (M.B.P.), and USPHS Grant MH12526 from NIMH and NIDA (J.L.M.).
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2022, Behavioural Brain ResearchCitation Excerpt :On the other hand, this study adds to existing literature on incentive shifts which suggests that these induce states carrying emotional information related to shift direction, because the shifts seem to depend on similar neural structures as fear conditioning [41]. That is, it has been shown that both fear conditioning [7,92] and negative contrast [35,93–95] are amygdala dependent processes (note that there is no such evidence about positive contrast), which has been extensively related to emotional processing and even the encoding of behavioral states [96]. This dependence on a common neural structure might contribute to explain the modulation of fear by the incentive shift procedures.
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2018, Neurobiology of Learning and MemoryCitation Excerpt :This is the first study describing a Crespi-like negative emotional contrast effect in female, but not male mice. Regarding the neuroanatomical substrate of the Crespi-effect, it was reported that electrolytic and ibotenic acid lesions to the amygdala, including the lateral nucleus, basolateral complex and central nucleus, in male rats modulate the emotional reaction and successive behavioral contrast after the manipulation of the reward magnitude in a food rewarded runway task (Becker, Jarvis, Wagner, & Flaherty, 1984; Salinas, Parent, & McGaugh, 1996). To our knowledge information on sex-differences in rats has not been reported so far.
Reward loss and the basolateral amygdala: A function in reward comparisons
2017, Behavioural Brain ResearchCitation Excerpt :In both cases, the effect of BLA lesions became evident only after some experience with the new conditions, either after one session in iSNC or after five sessions in AS extinction. Salinas et al. [50] favored an interpretation suggesting that while the amygdala is not a site of storage for stimulus-reward associations, its output modulates the consolidation of such emotionally significant memories in other brain sites. However, the results in the iSNC situation could also reflect incomplete damage of the mechanism necessary to compare postshift (current) and preshift (expected) rewards; such incomplete damage may have produced evidence of contrast during the initial downshift session, but the iSNC effect disappeared in the following sessions.
Inactivation of basolateral amygdala prevents chronic immobilization stress-induced memory impairment and associated changes in corticosterone levels
2017, Neurobiology of Learning and MemoryReward loss and addiction: Opportunities for cross-pollination
2017, Pharmacology Biochemistry and BehaviorCitation Excerpt :This picture is complicated by experiments with analogous amygdala manipulations, but involving reward devaluation or omission in instrumental conditioning situations. For example, the effects of instrumental reward devaluations were enhanced by lesions of the central nucleus, but reduced by lesions of the basolateral nucleus (Salinas et al., 1996). As reviewed above, both lesions eliminated the effects of reward devaluation on consummatory behavior (Kawasaki et al., 2015, submitted).
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Present address: Department of Psychology, University of Alberta, Edmonton, Alta. T6G 2E9, Canada.