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Cortico-subthalamic inputs from the motor, limbic, and associative areas in normal and dopamine-depleted rats are not fully segregated

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Abstract

The subthalamic nucleus (STN) receives monosynaptic glutamatergic afferents from different areas of the cortex, known as the “hyperdirect” pathway. The STN has been divided into three distinct subdivisions, motor, limbic, and associative parts in line with the concept of parallel information processing. The extent to which the parallel information processing coming from distinct cortical areas overlaps in the different territories of the STN is still a matter of debate and the proposed role of dopaminergic neurons in maintaining the coherence of responses to cortical inputs in each territory is not documented. Using extracellular electrophysiological approaches, we investigated to what degree the motor and non-motor regions in the STN are segregated in control and dopamine (DA) depleted rats. We performed electrical stimulation of different cortical areas and recorded STN neuronal responses. We showed that motor and non-motor cortico-subthalamic pathways are not fully segregated, but partially integrated in the rat. This integration was mostly present through the indirect pathway. The spatial distribution and response latencies were the same in sham and 6-hydroxydopamine lesioned animals. The inhibitory phase was, however, less apparent in the lesioned animals. In conclusion, this study provides the first evidence that motor and non-motor cortico-subthalamic pathways in the rat are not fully segregated, but partially integrated. This integration was mostly present through the indirect pathway. We also show that the inhibitory phase induced by GABAergic inputs from the external segment of the globus pallidus is reduced in the DA-depleted animals.

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Acknowledgements

The authors declare no competing financial interests. They gratefully acknowledge the support of the BrainGain Smart Mix Programme of the Netherlands Ministry of Economic Affairs and the Netherlands Ministry of Education, Culture and Science (Grant No.: SSM06011). The study was also supported by the “Bordeaux University” and the “Centre National de la Recherche Scientifique” (CNRS, France). M. Janssen received travel grants from the Boehringer Ingelheim Foundation and the Dutch Parkinson Association. C. Delaville was supported by a fellowship from the “Ministère de l’Education Nationale, de la Recherche et de la Technologie” (France). We thank L. Cardoit for her technical assistance. The authors declare no competing financial interests.

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Author notes

  1. Veerle Visser-Vandewalle

    Present address: Department of Stereotactic and Functional Neurosurgery, University of Cologne, Cologne, Germany

Authors and Affiliations

  1. Univ. de Bordeaux, Institut des Maladies Neurodégénératives, UMR 5293, 146, Rue Léo-Saignat, 33000, Bordeaux Cedex, France

    Marcus L. F. Janssen, Claire Delaville, Philippe De Deurwaerdère & Abdelhamid Benazzouz

  2. CNRS, Institut des Maladies Neurodégénératives, UMR 5293, 33000, Bordeaux, France

    Marcus L. F. Janssen, Claire Delaville, Philippe De Deurwaerdère & Abdelhamid Benazzouz

  3. School for Mental Health and Neuroscience, Maastricht University, Maastricht, The Netherlands

    Marcus L. F. Janssen & Yasin Temel

  4. Department of Neurology, Maastricht University Medical Center, 6202 AZ, Maastricht, The Netherlands

    Marcus L. F. Janssen

  5. Department of Neurosurgery, Maastricht University Medical Center, 6202 AZ, Maastricht, The Netherlands

    Yasin Temel

  6. MIRA Institute for Biomedical Technology and Technical Medicine, Department of Electrical Engineering, Mathematics and Computer Science, Biomedical Signals and Systems group, Twente University, 7500 AE, Enschede, The Netherlands

    Daphne G. M. Zwartjes & Tjitske Heida

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  1. Marcus L. F. Janssen
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Correspondence to Abdelhamid Benazzouz.

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Janssen, M.L.F., Temel, Y., Delaville, C. et al. Cortico-subthalamic inputs from the motor, limbic, and associative areas in normal and dopamine-depleted rats are not fully segregated. Brain Struct Funct 222, 2473–2485 (2017). https://doi.org/10.1007/s00429-016-1351-5

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