Increased ventral striatal BOLD activity during non-drug reward anticipation in cannabis users

Nestor, Liam; Hester, Robert; Garavan, Hugh

doi:10.1016/j.neuroimage.2009.07.022

Cited by 178 publications

(200 citation statements)

References 96 publications

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“…Despite this contention, sensitization has been shown to enhance the pursuit of natural rewards in animals, where exposure to substances of abuse has been observed to significantly increase cue-elicited approach behaviour for non-drug rewards (Wyvell et al, 2001). Interestingly, a similar effect has also been observed in humans, where the neural correlates of reward and loss anticipation are greater in cannabis users (Filbey et al, 2013;Nestor et al, 2010), cigarette smokers (Martin et (Gilman et al, 2015;Grodin et al, 2016) and even cocaine addicts (Balodis et al, 2016). This may suggest that chronic exposure to nicotine through smoking sensitizes striato-orbitofrontal circuitry that subserves motivational processes for loss avoidance and reward gain.…”

Section: Greater Ofc Activation During Loss and Gain Anticipation Inmentioning

confidence: 54%

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Smokers and ex‐smokers have shared differences in the neural substrates for potential monetary gains and losses

et al. 2016

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Abstract:Despite an increased understanding of nicotine addiction, there is a scarcity of research comparing the neural correlates of non-drug reward between smokers and ex-smokers. Long-term changes in reward-related brain functioning for non-drug incentives may elucidate patterns of functioning that potentially contribute to ongoing smoking behaviour in current smokers. Similarly, examining the effects of previous chronic nicotine exposure during a period of extended abstinence may reveal whether there are neural correlates responsible for non-drug reward processing that are different from current smokers. The current study, therefore, set out to examine the neural correlates of reward and loss anticipation, and their respective outcomes, in smokers, ex-smokers and matched controls using a monetary incentive delay task during functional MRI. Here we report that in the absence of any significant behavioural group differences, both smokers and ex-smokers showed a significantly greater activation change in the lateral orbitofrontal/anterior insular cortex compared to smokers when anticipating both potential monetary gains and losses. We further report that ex-smokers showed a significantly greater activation change in the ventral putamen compared to both controls and smokers, and in the caudate compared to controls during the anticipation of potential monetary losses only. The results suggest that smoking may sensitize striato-orbitofrontal circuitry subserving motivational processes for loss avoidance and reward gain in nicotine addiction. Comments to the Author This is a revision of an article detailing brain response differences between smokers, ex-smokers and non-smokers using the monetary incentive delay task. The authors did a great job addressing previous concerns and clarifying the analysis methods.A major limitation of the study is the sample size which could only be addressed by recruiting more subjects, despite this limitation the study is the first step towards dissociating theoretical models of reward processing in smokers.The inclusion of the mask in the supplemental materials is helpful, however, the inclusion of the whole-brain analysis in the supplemental materials would be helpful (although not necessary). The exploratory whole brain analysis demonstrates that the ROI approach did not miss any key reward processing regions. New Author Response: We have now included the ROI mask as a supplementary figure.Reviewer: 1 Comments to the Author SummaryThis report titled 'Smokers and ex-smokers have shared differences in the neural substrates for potential monetary gains and losses' tests the neural correlates of reward and loss anticipation and outcomes via the Monetary Incentive Delay task during fMRI in current cigarette smokers, exsmokers, and non-smoking young adults. This reviewer continues to have no major concerns, but there were some responses that may require further thought and elaboration (outlined below) before this paper is accepted for publication. Materials and MethodsfMRI Data Analysis ...

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Section: Greater Ofc Activation During Loss and Gain Anticipation Inmentioning

confidence: 54%

“…A semi-structured interview, as used in previous behavioural and functional imaging studies (Carey et al, 2015;Nestor et al, 2010) was conducted to screen participants for past or present histories of psychiatric or neurological illness.…”

Section: Methodsmentioning

confidence: 99%

Smokers and ex‐smokers have shared differences in the neural substrates for potential monetary gains and losses

et al. 2016

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“…There were no significant behavioural differences between the groups in both studies. Nestor et al (2010) [175] reported a greater right ventral striatum activity in cannabis users during reward anticipation, which was significantly correlated with years of lifetime cannabis use. In addition, response to loss and loss avoidance outcome notification was related with hypoactivity in left insula, and in the post hoc analysis comparing loss and win cues with no-outcome cues, right ventral putamen showed greater BOLD response [175].…”

Section: Memorymentioning

confidence: 94%

“…Furthermore, duration of cannabis use was associated with greater activity in ventromedial prefrontal cortex [167]. Nestor et al (2010) [175] and van Hell et al (2010) [176] used fMRI to measure brain activity during reward and anticipation of loss with different versions of a monetary reward task. There were no significant behavioural differences between the groups in both studies.…”

Section: Memorymentioning

confidence: 99%

1301 – Structural and functional imaging studies in chronic cannabis users: a systematic review of adolescent and adult findings

Batalla

Bhattachayyria

Yücel

et al. 2013

European Psychiatry

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Background:The growing concern about cannabis use, the most commonly used illicit drug worldwide, has led to a significant increase in the number of human studies using neuroimaging techniques to determine the effect of cannabis on brain structure and function. We conducted a systematic review to assess the evidence of the impact of chronic cannabis use on brain structure and function in adults and adolescents.

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“…Finally, although most studies have reported that reward anticipation is altered in cannabis users relative to non-users [9][10][11], Lichenstein et al did not find a significant difference between the trajectory groups during the anticipatory period for reward. Rather, they found that the effects of escalation of use were observable only during the receipt of reward.…”

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confidence: 86%

Commentary on Lichenstein et al. (2017): Escalating cannabis use, weak corticostriatal connections and negative outcomes

Filbey

2017

Addiction

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Commentary on Lichenstein et al. (2017): Escalating cannabis use, weak corticostriatal connections and negative outcomes Brain network-level, rather than regional, alterations may be more informative in predicting future negative outcomes in cannabis users. Individual factors that guide these changes in neural network function can facilitate prevention and early intervention more effectively.The study by Lichenstein et al. [1] found that an escalating trajectory of cannabis use during adolescence is associated with weak functional connectivity that is related to depressive symptoms, anhedonia and low educational attainment 3 years later. These findings underscore several important points related to the understanding of brain mechanisms in the development of cannabis use problems. First, there is a growing appreciation for behavioral manifestations of problems related to substance use reflecting network-level changes in the brain. Lichenstein et al.'s observation of altered brain functional architecture during a monetary reward task in the absence of changes in regional activation in cannabis-using adolescents who later present negative psychosocial outcomes is concordant with the growing neurodevelopmental literature showing how maturational changes during this period is centered around network organization and efficiency. Specifically, the changing network topology during adolescence involves the strengthening of connections between higher-order association areas [2]. Thus, escalating cannabis use (versus stable use) during this period may impede the strengthening of the corticostriatal connections that is linked to negative consequences. The usual caveat applies here-that is, whether this decreased functional connectivity predated escalated cannabis use or resulted from it is unknown. However, the important point not to be missed is that these network-level changes differentiated cannabis users who later develop negative psychosocial outcomes from those who do not. Incidentally, reward network connectivity, but not regional activation, during cue-reactivity has also distinguished DSM-IV cannabis-dependent from nondependent adults [3]. Thus, the integrity of the reward network can be used to determine individuals who may later develop problems related to cannabis use.Equally important to determining mechanisms that lead to problematic use is understanding the individual differences that influence these mechanisms. Lichenstein et al.'s findings, which are specific to a sample enriched for antisocial behavior [i.e. adolescent males from low socio-economic status (SES) households], underscore the need to understand these predisposing factors more clearly.

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Increased ventral striatal BOLD activity during non-drug reward anticipation in cannabis users

Cited by 178 publications

References 96 publications

Smokers and ex‐smokers have shared differences in the neural substrates for potential monetary gains and losses

Smokers and ex‐smokers have shared differences in the neural substrates for potential monetary gains and losses

1301 – Structural and functional imaging studies in chronic cannabis users: a systematic review of adolescent and adult findings

Commentary on Lichenstein et al. (2017): Escalating cannabis use, weak corticostriatal connections and negative outcomes

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