Abstract
Drug addiction is a chronic relapsing behavioral disorder. The high relapse rate has often been attributed to the perseverance of drug-associated memories due to high incentive salience of stimuli learnt under the influence of drugs. Drug addiction has also been interpreted as a memory disorder since drug associated memories are unusually enduring and some drugs, such as cocaine, interfere with neuroepigenetic machinery known to be involved in memory processing. Here we used the honey bee (an established invertebrate model for epigenomics and behavioral studies) to examine whether or not cocaine affects memory processing independently of its effect on incentive salience. Using the proboscis extension reflex training paradigm we found that cocaine strongly impairs consolidation of extinction memory. Based on correlation between the observed effect of cocaine on learning and expression of epigenetic processes, we propose that cocaine interferes with memory processing independently of incentive salience by directly altering DNA methylation dynamics. Our findings emphasize the impact of cocaine on memory systems, with relevance for understanding how cocaine can have such an enduring impact on behavior.
Highlights
Abused drugs cause debilitating drug addiction in a small fraction of users (McLellan et al, 2000)
Since we found that cocaine most strongly inhibited consolidation of extinction memory, we tried testing for acquisition memory at the same time point to ensure the effect of cocaine was specific to consolidation of extinction memory
There were, differences in the recall of acquisition memory for bees treated with cocaine 1 h before (Experiment 1: χ2 = 8.8245, p = 0.0030, n = 236, φ = 0.1933, Figure 2A) and after acquisition training (Experiment 2: χ2 = 3.9503, p = 0.0469, n = 234, φ = 0.1299, Figure 2B), and 2 h before the recall of acquisition memory (Experiment 3: χ 2 = 12.043, p = 0.0005, n = 139, φ = 0.2943, Figure 2C)
Summary
Abused drugs cause debilitating drug addiction in a small fraction of users (McLellan et al, 2000). Recovering addicts suffer high relapse rates due to persistent drug associated memories (Hser et al, 2001). This has led some authors to conclude that drug addiction is a disease of learning and memory (Hyman, 2005; Hyman et al, 2006). Stimuli associated with drug administration are readily learned, and memories of them are persistent (Uslaner et al, 2006). Many drugs of abuse alter neurotransmission in the dopaminergic midbrain pathway either by increasing release or inhibiting clearance of dopamine (Kuhar et al, 1991; Han and Gu, 2006), thereby increasing the incentive salience of a given stimuli (Berridge, 2007)
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