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Endocannabinoid neuromodulation in the neostriatum decreases the GABAergic striato-nigral disinhibitory function and increases the nigro-collicular inhibitory pathway activity

  • Psychiatry and Preclinical Psychiatric Studies - Original Article
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Abstract

We previously reported the involvement of neostriato-nigral projections in the organisation of innate fear and panic attack-like responses organised by dorsal midbrain neurons, such as the periaqueductal grey matter and the deep layers of the superior colliculus (dlSC). In addition, several lines of evidence have demonstrated that cannabinoid receptor type 1 is found in the neostriatum (caudate nucleus and putamen; CPu). In the present study, we investigated the role of endocannabinoid neuromodulation in CPu in the expression of unconditioned fear-related behavioural responses elicited by microinjections of the γ-aminobutyric acid (GABA)A receptor selective antagonist bicuculline (BIC) in the dlSC. Wistar rats received injection of vehicle or anandamide (AEA) at 0.5, 5, 50, 100 pmol in CPu, followed by injections of BIC in a dose of 40 ng in the dlSC. The treatment of the CPu with AEA in a dose of 5 and 50 pmol attenuated the unconditioned fear-related behaviour, such as defensive alertness, defensive immobility and escape, induced by GABAA receptor blockade in dlSC. These findings suggest that endogenous cannabinoids acting on CPu neurons exert an indirect modulatory influence on the activity of superior colliculus neurons, possibly through an inhibitory activity on neostriato-nigral disinhibitory connections that modulate the nigro-collicular inhibitory GABAergic pathways.

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Acknowledgements

This study was supported by the Conselho Nacional de Pesquisa e Desenvolvimento Tecnológico (CNPq) (Grants 483763/2010-1 and 474853/2013-6), Fundação de Apoio ao Ensino, Pesquisa e Assistência do HC-FMRP-USP (FAEPA) (Grants 1291/1997, 355/2000, 68/2001 and 15/2003), Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (Grants 2007/01174-1, 2012/03798-0, and 2017/11855-8), and a Pro-Rectory of the University of São Paulo (USP) Research Grant (NAP-USP-NuPNE; Grant IaPq2012-156-USP-12.1.25440.01.6). None of these organisations had a role in the study design; the collection, analysis, and interpretation of the data; the writing of the report; or the decision to submit the paper for publication. J.A. Silva was a recipient of a Scientific Initiation scholarship from CNPq (PIBIC process 2005.1.891.17.3) and was also supported by FAPESP and CNPq Post-Graduation fellowships (CNPq M.Sc. process 130170/2009-7/FAPESP M.Sc. process 2009/02458-9; CNPq Sc.D. process 142844/2011-0; FAPESP Post-doctoral process 2015/10313-1). R.C. Almada was a researcher supported by CAPES (post-doctoral process fellowship process: PNPD20131680-33002029012P3-PNPD-USP/RP/MEDICINA-NEUROLOGIA) and FAPESP (post-doctoral fellowship process: 2012/22681-7; young investigator program: research grant process 2018/03898-1 and researcher fellowship process 2019/01713-7). Coimbra was granted a research fellowship (Level 1A) from CNPq (processes 301905/2010-0 and 301341/2015-0). The authors are grateful to D.H. Elias-Filho for expert technical assistance. D.H. Elias Filho received a technician scholarship from FAPESP (TT-2, process 02/01497-1) and was the recipient of scholarships sponsored by CNPq (processes 501858/2005-9, 500896/2008-9, 505461/2010-2, and 372838/2018-9) and FAEPA (Grants 345/2009 and 185/2010).

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Authors and Affiliations

  1. Laboratório de Neuroanatomia and Neuropsicobiologia, Departamento de Farmacologia, Faculdade de Medicina de Ribeirão Preto da Universidade de São Paulo (FMRP-USP), Av. Bandeirantes, 3900, Ribeirão Preto, SP, 14049-900, Brasil

    Juliana Almeida da Silva, Rafael Carvalho Almada, Yara Bezerra de Paiva & Norberto Cysne Coimbra

  2. Behavioural Neurosciences Institute (INeC), Av. do Café, 2450, Monte Alegre, Ribeirão Preto, São Paulo, 14050-220, Brazil

    Juliana Almeida da Silva, Rafael Carvalho Almada, Yara Bezerra de Paiva & Norberto Cysne Coimbra

  3. Department of Biological Sciences, School of Sciences, Humanities and Languages, São Paulo State University (UNESP), Assis, São Paulo, 19806-900, Brazil

    Rafael Carvalho Almada

  4. NAP-USP-Neurobiology of Emotions Research Centre (NuPNE), Ribeirão Preto Medical School, University of São Paulo (FMRP-USP), Av. Bandeirantes, 3900, Ribeirão Preto, São Paulo, 14049-900, Brazil

    Norberto Cysne Coimbra

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  1. Juliana Almeida da Silva
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  2. Rafael Carvalho Almada
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da Silva, J.A., Almada, R.C., de Paiva, Y.B. et al. Endocannabinoid neuromodulation in the neostriatum decreases the GABAergic striato-nigral disinhibitory function and increases the nigro-collicular inhibitory pathway activity. J Neural Transm 127, 1199–1208 (2020). https://doi.org/10.1007/s00702-020-02217-8

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