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Stimulant drugs trigger transient volumetric changes in the human ventral striatum

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Abstract

The ventral striatum (VStr) integrates mesolimbic dopaminergic and corticolimbic glutamatergic afferents and forms an essential component of the neural circuitry regulating impulsive behaviour. This structure represents a primary target of psychostimulant medication, the first-choice treatment for attention-deficit/hyperactivity disorder (ADHD), and is biochemically modified by these drugs in animals. However, the effects of stimulants on the human VStr remain to be determined. We acquired anatomical brain MRI scans from 23 never-medicated adult patients with ADHD, 31 adult patients with a history of stimulant treatment and 32 control subjects, and VStr volumes were determined using individual rater-blinded region of interest delineation on high-resolution neuroanatomical scans. Furthermore, we also extracted VStr volumes before and after methylphenidate treatment in a subsample of the medication-naïve adult patients as well as in 20 never-medicated children with ADHD. We observed smaller VStr volumes in adult patients with a history of stimulant treatment in comparison to never-medicated patients. Moreover, our longitudinal analyses uncovered a reduction of grey matter volume in the bilateral VStr in adult patients after exposure to methylphenidate, which was followed by volumetric recovery to control level. In children, the same pattern of VStr volume changes was observed after treatment with methylphenidate. These findings suggest that the altered VStr volumes previously observed in patients with ADHD may represent a transitory effect of stimulant exposure rather than an intrinsic feature of the disorder. More generally, these data show that stimulant drugs can render plastic volume changes in human VStr neuroanatomy.

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Acknowledgments

This work was supported by the Fundación Alicia Koplowitz and the Ministerio de Ciencia e Innovación (SAF2009-10901). The latter institution also awarded a Postdoctoral Research grant to SC and a Formación de Profesorado Universitario grant to EH. The funding agencies did not play a role in any aspect of this study. We want to thank TDAH Catalunya for their collaboration and for referring patients for our study.

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The authors declare no conflicts of interest.

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  1. Elseline Hoekzema

    Present address: Neuroendocrinology, Netherlands Institute for Neuroscience, Meibergdreef 47, 1105 BA, Amsterdam, The Netherlands

Authors and Affiliations

  1. Unitat de Recerca en Neurociència Cognitiva, Departament de Psiquiatria i Medicina Legal, Universitat Autònoma de Barcelona, Campus Bellaterra, 08193, Barcelona, Spain

    Elseline Hoekzema, Susana Carmona, Clara Canals, Ana Moreno, Marisol Picado, Juan Carlos Soliva, Adolf Tobeña & Oscar Vilarroya

  2. Grup de Recerca en Neuroimatge, Fundació IMIM, c/Dr. Aiguader 88, 08003, Barcelona, Spain

    Elseline Hoekzema, Susana Carmona, Clara Canals, Ana Moreno, Marisol Picado, Juan Carlos Soliva & Oscar Vilarroya

  3. Harvard Social Cognitive and Affective Neuroscience Lab, Harvard University, 52 Oxford street, Cambridge, MA, 02138, USA

    Susana Carmona

  4. Department of Psychiatry, Hospital Universitari Vall d’Hebron, CIBERSAM, Passeig de la Vall d’Hebron 119-129, 08035, Barcelona, Spain

    J. Antoni Ramos-Quiroga, Vanesa Richarte Fernández, Rosa Bosch & Miguel Casas

  5. Departament de Psiquiatria i Medicina Legal, Universitat Autònoma de Barcelona, Campus Bellaterra, 08193, Barcelona, Spain

    J. Antoni Ramos-Quiroga, Vanesa Richarte Fernández, Rosa Bosch, Adolf Tobeña & Miguel Casas

  6. CRC Corporació Sanitaria, c/Tavern 82, 08006, Barcelona, Spain

    Mariana Rovira

  7. Institut de Neuropsiquiatria i Adiccions, Hospital del Mar, Parc de Salut Mar, Passeig maritim 25-29, 08003, Barcelona, Spain

    Lurdes Duñó & Antonio Bulbena

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  1. Elseline Hoekzema
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Correspondence to Elseline Hoekzema.

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E. Hoekzema and S. Carmona contributed equally to this work.

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Hoekzema, E., Carmona, S., Ramos-Quiroga, J.A. et al. Stimulant drugs trigger transient volumetric changes in the human ventral striatum. Brain Struct Funct 219, 23–34 (2014). https://doi.org/10.1007/s00429-012-0481-7

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