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

Marcus L. F. Janssen, Yasin Temel, Claire Delaville, Daphne G. M. Zwartjes, Tjitske Heida, Philippe De Deurwaerdère, Veerle Visser-Vandewalle, Abdelhamid Benazzouz
Brain Struct Funct. 2016-12-24; 222(6): 2473-2485
DOI: 10.1007/s00429-016-1351-5

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Janssen MLF(1)(2)(3)(4), Temel Y(3)(5), Delaville C(1)(2), Zwartjes DGM(6), Heida T(6), De Deurwaerdère P(1)(2), Visser-Vandewalle V(7), Benazzouz A(8)(9).

Author information:
(1)Univ. de Bordeaux, Institut des Maladies Neurodégénératives, UMR 5293, 146, Rue Léo-Saignat, 33000, Bordeaux Cedex, France.
(2)CNRS, Institut des Maladies Neurodégénératives, UMR 5293, 33000, Bordeaux, France.
(3)School for Mental Health and Neuroscience, Maastricht University, Maastricht, The Netherlands.
(4)Department of Neurology, Maastricht University Medical Center, 6202 AZ, Maastricht, The Netherlands.
(5)Department of Neurosurgery, Maastricht University Medical Center, 6202 AZ, Maastricht, The Netherlands.
(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.
(7)Department of Stereotactic and Functional Neurosurgery, University of Cologne, Cologne, Germany.
(8)Univ. de Bordeaux, Institut des Maladies Neurodégénératives, UMR 5293, 146, Rue Léo-Saignat, 33000, Bordeaux Cedex, France. .
(9)CNRS, Institut des Maladies Neurodégénératives, UMR 5293, 33000, Bordeaux, France. .

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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