Neuronal circuit involved in inhibitory control

Clinical studies show that addicted patients suffer from a lack of inhibitory control (Feil et al., 2010). In the Go/NoGo task, anterior cingulate cortex (ACC) is active during both go and no-go trials, while ventrolateral and dorsolateral prefrontal cortex (VLPFC and DLPFC, respectively) are more active during the no-go trials (Liddle et al., 2001). Similar results were obtained with the color-word Stroop task (Kerns et al., 2004; MacDonald et al., 2000).

These results suggest VLPFC and DLPFC are particularly involved in response inhibition.

Cocaine addicted patients display more errors than healthy subjects in the both Go/NoGo (Kaufman et al., 2003) and Stroop task (Bolla et al., 2004). This worse performance has been attributed to the hypoactivity in the ACC or DFPFC (Bolla et al., 2004; Kaufman et al., 2003). The causal relation between the loss of inhibitory control and hypoactivity in the ACC or DLPFC has not been tested in human studies. However, in a preclinical study, silencing of the ACC, PL or IL diminished the inhibition of reward pursuit under threat of punishment (Verharen et al., 2019), suggesting that these brain regions are crucial for the inhibitory control. Prolonged cocaine self-administration induced massive reduction of firing rate in the PL, which is more profound in persevering animals (Chen et al., 2013).

The optogenetic inhibition of the PL facilitats compulsive cocaine seeking, indicating that the hypoactivity of the PL is casually related to the compulsive behavior (Chen et al., 2013).

It has yet to be determined how cocaine self-administration induces the reduction of the firing rate in the PL. The inhibition of the PL pyramidal neurons projecting to the NAc promotes reward seeking associated with punishments (Domingo-rodriguez et al., 2020;

Kim et al., 2017) but not the VTA projection (Kim et al., 2017), suggesting that the PL to NAc pathway is particularly important for the inhibitory control. However, it has been unclear how neuronal plasticity control the inhibitory control. Clinical studies show that addicted patients have lower D2 receptor availability in the striatum (Volkow et al., 2009).

Although we have not measured the expression of D2 receptor, this needs to be measured in the laboratory animals. The role of D2 receptors in the addiction has been investigated for decades but it’s still unclear. Pharmacological experiments shows that D2 receptors have higher affinity than D1 (Marcellino et al., 2012). Because of its high affinity, D2 receptors are tonically active at the basal state. Aversive events, such as foot shock

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triggers the dip of dopamine (de Jong et al., 2018), and the dip of dopamine triggers the potentiation in D2-MSNs (Iino et al., 2020). In other words, D2 receptors are necessary to detect the dip of dopamine. The deletion of D2 receptors in NAc abolishes the active avoidance behavior (Danjo et al., 2014). We would like to hypothesize that when there is less D2 receptor availability in NAc, patients or laboratory animals are less sensitive to the aversive events. As a result, they don’t stop drug seeking despite negative consequences because of the insensitivity to negative events.

4.6 Conclusion

Combining optogenetic dopamine neurons self-stimulation with seek-take chained schedule, we confirmed that the potentiation at OFC-striatum is crucial for compulsive reward seeking. We also measured neuronal plasticity at mPFC-striatum and M1-striatum, detecting no differences between naïve, renouncing and persevering mice. This negative result suggests the septicity of the potentiation at OFC-striatum pathway. To investigate the impact of the synaptic potentiation on neuronal activity, we performed fiber photometry experiment in the striatum. Correlating with the plasticity, persevering mice showed stronger neural activity in the dorsal striatum at the end of seeking behaviour than renouncers. The activity was sustained during punishment sessions in persevering mice while in renouncers, the peak amplitude was diminished, suggesting that punishment induced neuronal adaptations exclusively to renouncers. To test the causality between the potentiation at OFC-striatum and strong neuronal activity in the striatum, chemogenetic inhibition was combined with the photometry experiment. The inhibition of the OFC flattered calcium signal observed in the striatum and attenuated compulsive reward seeking. Finally, to investigate the contribution of the neuronal activity in the striatum to compulsive reward seeking, we used inhibitory opsin in the dorsal striatum, allowing time locked inhibition. The inhibition at the end of the seeking behaviour attenuated compulsive reward seeking. This result has raised the idea that OFC-striatum encodes the value of the state, which was degraded by the inhibition.

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Altogether, this work expanded the knowledge of how synaptic plasticity at OFC-striatum control the neuronal activity and eventually compulsive reward seeking. This knowledge might be inspiring the development of more efficient therapy of addiction.

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