Effects of nicotine self-administration on incentive salience in male Sprague Dawley rats

Overby, Paula F.; Daniels, Carter W.; Franco, Armani P. Del; Goenaga, Julianna; Powell, Gregory L.; Gipson, Cassandra D.; Sanabria, Federico

doi:10.1007/s00213-018-4829-4

Cited by 20 publications

(17 citation statements)

References 45 publications

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“…In rats trained with the same nicotine dose and schedule, we previously reported that substituting saline for nicotine before a Pavlovian conditioning session resulted in a reduction in behavior that returned the nicotine-enhanced CRs to the level of control animals [22]. Furthermore, at blood plasma levels relevant to human cigarette inhalation, self-administered nicotine increases sign-tracking behaviors, but this effect may be transient and dissipate when nicotine is no longer on board, despite an extensive history of drug exposure [24]. Thus, it is possible that despite 30 days of nicotine exposure, the nicotine dose in this study was not sufficient to elicit changes in BDNF expression measurable after 24 h.…”

Section: Discussionmentioning

confidence: 99%

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Sex differences in nicotine-enhanced Pavlovian conditioned approach in rats

et al. 2019

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Background Nicotine exposure enhances Pavlovian conditioned approach (PCA), or the learned approach to reward-predictive cues. While females show elevated approach to conditioned stimuli compared to males, potentially indicating heightened addiction vulnerability, it is unknown how sex may interact with nicotine to influence approach behavior. Additionally, brain-derived neurotrophic factor (BDNF) levels can be altered significantly after repeated nicotine exposure, suggesting a potential mechanism contributing to nicotine-induced behavioral phenotypes. The present study investigated the role of sex on nicotine-induced changes to stimulus-response behavior and associated BDNF protein levels. Methods Male and female rats were exposed to nicotine (0.4 mg/kg, subcutaneously) or saline 15 min prior to each PCA session. PCA training consisted of 29 sessions of 15 trials, in which a 30-s cue presentation ended concurrently with a sucrose reward (20% w / v in water, 100 μL), and a 120-s variable intertrial interval occurred between trials. Approach behavior to the cue and reward receptacle was recorded. Preference toward the reward receptacle indicated a goal-tracking phenotype, and preference toward the cue indicated a sign-tracking phenotype, demonstrating that the cue had gained incentive salience. Twenty-four hours after the last PCA session, brain tissue was collected and BDNF levels were measured in the basolateral amygdala, orbitofrontal cortex, and nucleus accumbens using Western blot analysis. Results Nicotine exposure enhanced both sign- and goal-tracking conditioned approach, and females showed elevated sign-tracking compared to males. There were no sex-by-drug interactions on conditioned approach. Day-to-day variability in conditioned approach was similar between sexes. In contrast to prior studies, neither repeated exposure to nicotine nor sex significantly affected BDNF expression. Conclusions Drug-naïve females exhibited heightened sign-tracking compared to males, and nicotine enhanced conditioned approach similarly in males and females. Further, non-significant changes to BDNF expression in brain regions highly associated with PCA indicate that BDNF is unlikely to drive nicotine-enhanced conditioned behavior.

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Section: Discussionmentioning

confidence: 99%

“…Nicotine, in particular, exerts reinforcement- and incentive-enhancing properties in both humans and animals, suggesting that nicotine amplifies the rewarding or incentive properties of non-nicotine stimuli [17–20]. For example, nicotine increases CRs to a non-drug-associated CS [18, 21, 22], especially sign-tracking CRs [16, 23, 24].…”

Section: Introductionmentioning

confidence: 99%

Sex differences in nicotine-enhanced Pavlovian conditioned approach in rats

et al. 2019

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“…It is also possible that stimuli associated with food (test chamber, house-light, lever insertion) mediated the nicotinic effects on motivation. Nicotine enhances the incentive value of such stimuli, facilitating a conditioned approach to them ( sign tracking , Palmatier et al, 2013; Overby et al, under review). In the presence of the lever press-food contingency, it is likely that such approach would be directed to the lever.…”

Section: Discussionmentioning

confidence: 99%

Suppressive and enhancing effects of nicotine on food-seeking behavior

Romero

Daniels

Gipson

et al. 2018

Behavioural Brain Research

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The present study examined how systemic low doses of nicotine affect the microstructure of reinforced food-seeking behavior in rats. Rats were first given an acute saline or nicotine treatment (0.1-0.6mg/kg, with an inter-injection interval of at least 48h), and then a chronic saline or nicotine treatment (0.3mg/kg/day for 10 consecutive days). Immediately after each injection, rats were required to press a lever five times to obtain food that was available at unpredictable times (on average every 80s) with constant probability. Acute nicotine dose-dependently suppressed behavior prior to the delivery of the first reinforcer, but enhanced food-reinforced behavior afterwards. These effects were primarily observed in the time it took rats to initiate food-seeking behavior. Enhancing effects were also observed in the microstructure of food-seeking behavior, with lower nicotine doses (0.1-0.3mg/kg) increasing the rate at which response bouts were initiated, and higher doses (0.3-0.6mg/kg) increasing within-bout response rates. A pre-feeding control suggests that changes in appetite alone cannot explain these effects. Over the course of chronic nicotine exposure, tolerance developed to the suppressive, but not to the enhancing effects of nicotine on food-seeking behavior. These results suggest that (a) lower doses of nicotine enhance the reward value of food and/or food-associated stimuli, (b) higher doses of nicotine enhance motoric activity, and (c) ostensive sensitization effects of nicotine on behavior partially reflect a tolerance to its transient suppressive motoric effects.

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“…Albans, VT), which have been previously described in detail (Overby, Daniels et al 2018, Leyrer-Jackson, Overby et al 2020.…”

Section: Food Training Proceduresmentioning

confidence: 99%

Accumbens Cholinergic Interneurons Mediate Cue-Induced Nicotine Seeking and Associated Glutamatergic Plasticity

Leyrer‐Jackson

Holter

Overby

et al. 2020

eNeuro

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Nicotine, the primary addictive substance in tobacco, is widely abused. Relapse to cues associated with nicotine results in increased glutamate release within nucleus accumbens core (NAcore), modifying synaptic plasticity of medium spiny neurons (MSNs) which contributes to reinstatement of nicotine seeking. However, the role of cholinergic interneurons (ChIs) within the NAcore in mediating these neurobehavioral processes is unknown. ChIs represent less than 1% of the accumbens neuronal population and are activated during drug seeking and reward-predicting events. Thus, we hypothesized that ChIs may play a significant role in mediating glutamatergic plasticity that underlies nicotine seeking behavior. Using chemogenetics in transgenic rats expressing Cre under the control of the choline acetyltransferase (ChAT) promoter, ChIs were bi-directionally manipulated prior to cueinduced reinstatement. Following nicotine self-administration and extinction, ChIs were activated or inhibited prior to a cue reinstatement session. Following reinstatement, whole-cell electrophysiology from NAcore MSNs was used to assess changes in plasticity, measured via α-amino-3-hydroxy-5methyl-4-isoxazolepropionic acid (AMPA) / N-Methyl-D-Aspartate (NMDA) (A/N) ratios. Chemogenetic inhibition of ChIs inhibited cued nicotine seeking and resulted in decreased A/N, relative to control animals, whereas activation of ChIs was unaltered, demonstrating that ChI inhibition may modulate plasticity underlying cue-induced nicotine seeking. These results demonstrate that ChI neurons play an important role in mediating cue-induced nicotine reinstatement and underlying synaptic plasticity within the NAcore.

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Effects of nicotine self-administration on incentive salience in male Sprague Dawley rats

Cited by 20 publications

References 45 publications

Sex differences in nicotine-enhanced Pavlovian conditioned approach in rats

Sex differences in nicotine-enhanced Pavlovian conditioned approach in rats

Suppressive and enhancing effects of nicotine on food-seeking behavior

Accumbens Cholinergic Interneurons Mediate Cue-Induced Nicotine Seeking and Associated Glutamatergic Plasticity

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