Significant association of nicotine reinforcement and cue reactivity: a translational study in humans and rats

Butler, Kevin; Forget, Benoît; Heishman, Stephen J.; Foll, Bernard Le

doi:10.1097/fbp.0000000000000607

Cited by 6 publications

(3 citation statements)

References 42 publications

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“…Network activity correlated close to significance ( p = 0.0545) with relapse-like behavior after 28 d of nicotine abstinence which was associated with total nicotine exposure. This suggest that activity of the DLS-amygdala network is related to nicotine seeking which in turn is affected by nicotine exposure ( X. Liu et al, 2008 ; Butler et al, 2021 ).…”

Section: Discussionmentioning

confidence: 99%

Abstinence-Induced Nicotine Seeking Relays on a Persistent Hypoglutamatergic State within the Amygdalo-Striatal Neurocircuitry

Domi

Lagström

et al. 2023

eNeuro

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Nicotine robustly sustains smoking behavior by acting as a primer reinforcer and by enhancing the incentive salience of the nicotine associated stimuli. The motivational effects produced by environmental cues associated with nicotine delivery can progressively manifest during abstinence resulting in reinstatement of nicotine seeking. However, how the activity in reward neuronal circuits is transformed during abstinence-induced nicotine seeking is not yet fully understood. In here we used a contingent nicotine and saline control self-administration model to disentangle the contribution of cue-elicited seeking responding for nicotine after drug abstinence in male Wistar rats. Using ex vivo electrophysiological recordings and a network analysis approach, we defined temporal and brain-region specific amygdalo-striatal glutamatergic alterations that occur during nicotine abstinence. The results from this study provide critical evidence indicating a persistent hypoglutamatergic state within the amygdalo-striatal neurocircuitry over protracted nicotine abstinence. During abstinence-induced nicotine seeking, electrophysiological recordings showed progressive neuroadaptations in dorsal and ventral striatum already at 14-days abstinence while neuroadaptations in subregions of the amygdala emerged only after 28-days abstinence. The observed neuroadaptations pointed to a brain network involving the amygdala and the dorsolateral striatum (DLS) to be implied in cue-induced reinstatement of nicotine seeking. Together these data suggest long-lasting neuroadaptations that might reflect neuroplastic changes responsible to abstinence-induced nicotine craving. Neurophysiological transformations were detected within a time window that allows therapeutic intervention advancing clinical development of preventive strategies in nicotine addiction.SIGNIFICANT STATEMENTMost people attempting to quit smoking, experience multiple periods of remission and relapse within the first month of abstinence. Our results provide evidence of a persistent hypoglutamatergic state over four weeks of nicotine abstinence when assessing parallel changes in evoked glutamate transmission in multiple amygdalo-striatal subregions at once. The observed neuroadaptations pointed to a brain network involving the amygdala and the dorsolateral striatum that correlated with cue-induced reinstatement of nicotine seeking. The importance of these findings resides in an improved picture when capturing a single frame of the amygdalo-striatal circuitry in abstinence-induced nicotine craving. The neurophysiological transformations were detected within a time window that allows therapeutic intervention advancing clinical development of preventive strategies in nicotine addiction.

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Section: Discussionmentioning

confidence: 99%

Abstinence-Induced Nicotine Seeking Relays on a Persistent Hypoglutamatergic State within the Amygdalo-Striatal Neurocircuitry

Domi

Lagström

et al. 2023

eNeuro

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“…56 A large volume of human and non-human animal studies have shown that organisms will exert high levels of effort to obtain especially potent reinforcers, such as high-fat foods, nicotine, and other drugs. [57][58][59][60][61] Further, the degree to which individuals will exert effort towards certain problematic behaviors has been associated with negative psychological and health outcomes (e.g., effort for nicotine is higher in heavy smokers, effort for food is higher for binge eating). 62,63 These findings correspond with the clinical phenomenon that some individuals will go to great lengths to engage in addictive behaviors because of the strong reward derived from those behaviors.…”

Section: Comparing Learned Industriousness To Other Theories Of Effor...mentioning

confidence: 99%

Learned industriousness as a translational mechanism in anorexia nervosa

2022

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Researchers have long grappled to understand the persistence of behaviors that are nonhedonic and, ostensibly, aversive. At times, such behaviors are taken to excess in the form of psychopathology. Anorexia nervosa characterizes a prototype of a disorder in which behaviors that most people find unpleasant (e.g., restrictive eating, excessive exercise) are repeatedly performed, despite significant personal cost and risk of death. The learned industriousness theory, which originated from social psychology and behavioral neuroscience, provides a novel theoretical account for such serious, yet unexplained phenomena. Informed by human and animal data, this theory posits that effort (intense physical or mental activity) can be conditioned to acquire secondary rewarding properties through repeatedly pairing high-effort behavior with reward. Over time, effort sensations become less aversive and more appetitive because they signal impending reward, generalizing willingness to engage in effortful behavior. In this manuscript, we: 1) review behavioral and biological data supporting learned industriousness; 2) contrast learned industriousness with other conceptual models of effort persistence (e.g., goaldirected and habit learning); 3) highlight evidence that learned industriousness may account for the persistence of weight-control behaviors in anorexia nervosa; and 4) consider clinical and research implications of this model, including the translation to other psychological disorders.

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“…It is well-known that drug-associated cues play a large role in the formation and continuation of drug taking behaviors, and the presence of drug-paired cues is of particular importance in nicotine self-administration behavior (Butler, Forget, Heishman et al, 2021; Caggiula, Donny, Palmatier et al, 2009; Caggiula, Donny, White et al, 2001; Chaudhri, Caggiula, Donny et al, 2007; Donny, Caggiula, Knopf et al, 1995; Donny, Chaudhri, Caggiula et al, 2003; LeSage, Burroughs, Dufek et al, 2004; X. Liu, Caggiula, Yee et al, 2006; Sorge, Pierre, & Clarke, 2009).…”

Section: Introductionmentioning

confidence: 99%

Nicotine Modifies Responding for Cocaine in a Concurrent Rodent Self-administration Model

Dawes¹,

Estave²,

Albertson³

et al. 2022

Preprint

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Prevailing preclinical models of cocaine use have not resulted in an FDA-approved treatment for cocaine use disorder, potentially due to a focus on cocaine use in isolation, which may not translate well to polysubstance use in clinical populations. Clinically, nicotine has been shown to increase cocaine potency and reinforcing efficacy, but some preclinical studies suggest that non-contingent nicotine exposure is not sufficient to alter cocaine self-administration in rats; therefore, this experiment examined if the addition of nicotine to the cocaine solution would alter self-administration behavior. Male Sprague Dawley rats (N=7) were trained to self-administer cocaine (0.75mg/kg/inf), and tested on a long access, fixed ratio 1 schedule of reinforcement (6 hour sessions, unlimited inf, 5 days), for cocaine alone (0.75mg/kg/inf), followed by cocaine and nicotine (0.75mg/kg/inf cocaine +0.03mg/kg/inf nicotine). Finally, rats responded on a progressive ratio schedule for varied doses of cocaine with and without concurrent nicotine at a consistent dose (1.5, 0.75, 0.375, 0.19mg/kg/inf cocaine ± 0.03mg/kg/inf nicotine). Unexpectedly, under long access conditions, rats self-administering cocaine and nicotine responded less than for cocaine alone, and did not escalate responding. However, under progressive ratio conditions, responding for cocaine and nicotine was greater than responding for cocaine alone across low and moderate cocaine doses, and decreased at high cocaine doses, indicating a leftward shift in the dose response curve. Together, these data highlight the importance of evaluating multiple outcome measures in nicotine + cocaine paradigms, and suggest that concurrent self-administration of cocaine and nicotine results in greater motivated responding than for cocaine alone.

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Significant association of nicotine reinforcement and cue reactivity: a translational study in humans and rats

Cited by 6 publications

References 42 publications

Abstinence-Induced Nicotine Seeking Relays on a Persistent Hypoglutamatergic State within the Amygdalo-Striatal Neurocircuitry

Abstinence-Induced Nicotine Seeking Relays on a Persistent Hypoglutamatergic State within the Amygdalo-Striatal Neurocircuitry

Learned industriousness as a translational mechanism in anorexia nervosa

Nicotine Modifies Responding for Cocaine in a Concurrent Rodent Self-administration Model

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