Abstract
In goal-directed pursuits, the basolateral amygdala (BLA) is critical in learning about changes in the value of rewards. BLA-lesioned rats show enhanced reversal learning, a task employed to measure the flexibility of response to changes in reward. Similarly, there is a trend for enhanced discrimination learning, suggesting that BLA may modulate formation of stimulus-reward associations. There is a parallel literature on the importance of serotonin (5HT) in new stimulus-reward and reversal learning. Recent postulations implicate 5HT in learning from punishment. Whereas, dopaminergic involvement is critical in behavioral activation and reinforcement, 5HT may be most critical for aversive processing and behavioral inhibition, complementary cognitive processes. Given these findings, a 5HT-mediated mechanism in BLA may mediate the facilitated learning observed previously. The present study investigated the effects of selective 5HT lesions in BLA using 5,7-dihydroxytryptamine (5,7-DHT) vs. infusions of saline (Sham) on discrimination, retention, and deterministic reversal learning. Rats were required to reach an 85% correct pairwise discrimination and single reversal criterion prior to surgery. Postoperatively, rats were then tested on the (1) retention of the pretreatment discrimination pair, (2) discrimination of a novel pair, and (3) reversal learning performance. We found statistically comparable preoperative learning rates between groups, intact postoperative retention, and unaltered novel discrimination and reversal learning in 5,7-DHT rats. These findings suggest that 5HT in BLA is not required for formation and flexible adjustment of new stimulus-reward associations when the strategy to efficiently solve the task has already been learned. Given the complementary role of orbitofrontal cortex in reward learning and its interconnectivity with BLA, these findings add to the list of dissociable mechanisms for BLA and orbitofrontal cortex in reward learning.
Highlights
Control over inappropriate responding plays a pivotal role in adaptive decision making
Following the behavioral testing, the tryptophan hydroxylase (TPH) levels were significantly reduced in depletion compared to control group: mean effect of treatment group [F(1,12) = 46.395, p < 0.001 Figure 2]; and not different between the left and right hemispheres [F(1,12) = 0.367, p = 0.556]
The lesioned animals demonstrated intact memory for previously learned associations as evidenced by lack of between group differences on the retention task. These animals were unimpaired relative to controls at acquiring a novel discrimination task and flexibly adapted their responses following a change in reward contingencies, at a rate comparable to Sham animals
Summary
Control over inappropriate responding plays a pivotal role in adaptive decision making. Substantial evidence from studies employing pharmacological manipulations of serotonergic neurotransmission by receptor antagonist administration (Boulougouris and Robbins, 2010), selective toxin-mediated depletions of 5-HT and destruction of 5-HT terminals (Clarke et al, 2004, 2007; Masaki et al, 2006) combined with genetic studies (Homberg et al, 2007; Brigman et al, 2010; Jedema et al, 2010) have established a prominent role for this neurotransmitter in reversal learning performance in different species Overall, these studies suggest that global reductions of serotonin levels are associated with a higher degree of perseveration and poor response control. To test whether the BLA-specific depletion of 5-HT produces impairments in reversal learning, we first assessed animals’ performance on initial pairwise discrimination and reversal learning, performed selective 5-HT depletions within this region to examine their subsequent performance on retention of preoperative reward contingencies, novel pairwise discrimination, and reversal learning
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