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Lack of correlation between the activity of the mesolimbic dopaminergic system and the rewarding properties of pregabalin in mouse

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Abstract

Rationale

Pregabalin is a psychoactive drug indicated in the treatment of epilepsy, neuropathic pain, and generalized anxiety disorders. Pregabalin acts on different neurotransmission systems by inactivating the alpha2-delta subunit of voltage-gated calcium channels. In light of this pharmacological property, the hypothesis has been raised that pregabalin may regulate the mesolimbic dopamine pathway and thereby display a potential for misuse or abuse as recently observed in humans. Although some preclinical data support this possibility, the rewarding properties of gabapentinoid are still a matter for debate.

Objective

The aim of this work was to evaluate the rewarding properties of pregabalin and to determine its putative mechanism of action in healthy mice.

Results

Pregabalin alone (60 mg/kg; s.c.) produced a rewarding effect in the conditioned place preference (CPP) test albeit to a lower extent than cocaine (30 mg/kg; s.c.). Interestingly, when assessing locomotor activity in the CPP, the PGB60 group, similarly to the cocaine group, showed an increased locomotor activity. In vivo single unit extracellular recording showed that pregabalin had mixed effects on dopamine (DA) neuronal activity in the ventral tegmental area since it decreased the activity of 50% of neurons and increased 28.5% of them. In contrast, cocaine decreased 75% of VTA DA neuronal activity whereas none of the neurons were activated. Intracerebal microdialysis was then conducted in awake freely mice to determine to what extent such electrophysiological parameters influence the extracellular DA concentrations ([DA]ext) in the nucleus accumbens. Although pregabalin failed to modify this parameter, cocaine produced a robust increase (800%) in [DA]ext.

Conclusions

Collectively, these electrophysiological and neurochemical experiments suggest that the rewarding properties of pregabalin result from a different mode of action than that observed with cocaine. Further experiments are warranted to determine whether such undesirable effects can be potentiated under pathological conditions such as neuropathic pain, mood disorders, or addiction and to identify the key neurotransmitter system involved.

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Acknowledgments

The authors greatly acknowledge “the Mouse Behavioural Phenotyping Core” (Center of Integrative Biology, Toulouse, France) for its expertise and assistance in setting up behavioral apparatus and procedures.

Funding

This independent study did not receive resources from pharmaceutical companies and was funded by the academic collaborating laboratories.

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Authors and Affiliations

  1. Centre de Recherches sur la Cognition Animale (CRCA), Centre de Biologie Intégrative (CBI), Université Paul Sabatier Toulouse III, Bât4R3, 118 Route de Narbonne, 31062, Toulouse, Cedex 09, France

    Basile Coutens, Lionel Mouledous, Manta Stella, Claire Rampon & Bruno P. Guiard

  2. Pharmacoepidemiology Research Unit, INSERM-Université Toulouse 3, UMR 1027, 31000, Toulouse, France

    Maryse Lapeyre-Mestre, Anne Roussin & Emilie Jouanjus

  3. Faculté de Pharmacie, Université Paris Sud, Université Paris-Saclay, 92290, Chatenay-Malabry, France

    Bruno P. Guiard

  4. CNRS UMR-5169, UPS, 31000, Toulouse, France

    Bruno P. Guiard

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  1. Basile Coutens
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  2. Lionel Mouledous
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  3. Manta Stella
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  4. Claire Rampon
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  7. Bruno P. Guiard
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  8. Emilie Jouanjus
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Corresponding author

Correspondence to Bruno P. Guiard.

Ethics declarations

All experiments were carried out in accordance with the European guidelines for the care of laboratory animals (European Communities Council Directive 86/609/ECC) and approved by the local Ethics Committee and the French Ministry of Education and Research (APAFIS#6659-2016090512114815 v3).

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The authors declare that they have no conflict of interest.

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Bruno P. Guiard and Emilie Jouanjus co-directed this study.

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Supplemental Figure 1

Individual distribution of the percentage of time spent in the drug-paired compartment before (D0) and after (D5) conditioning in response to cocaine (30 mg/kg, s.c.) (A) or pregabalin (PGB 60 mg/kg, s.c.). (PNG 577 kb)

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Coutens, B., Mouledous, L., Stella, M. et al. Lack of correlation between the activity of the mesolimbic dopaminergic system and the rewarding properties of pregabalin in mouse. Psychopharmacology 236, 2069–2082 (2019). https://doi.org/10.1007/s00213-019-05198-z

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