Objective: The present study aimed to identify which neurons in the basal ganglia (BG)  target dopaminergic or GABAergic neurons in SN pars compacta (SNc) or reticulata (SNr), respectively.

Background: Electrophysiological studies in monkeys have shown that dopaminergic neurons respond to the reward prediction error. In addition, striatal neurons alter their responsiveness to cortical or thalamic inputs in response to the dopamine signal, via the mechanism of dopamine-regulated synaptic plasticity. These findings have led to the hypothesis that the striatum exhibits synaptic plasticity under the influence of the reward prediction error and conduct reinforcement learning throughout the basal ganglia circuits.

Methods: In the present study, we generated a novel parvalbumin (PV)-Cre rat model and conducted a detailed morphological and electrophysiological investigation of axons from PV-globus pallidus (GP). For the striatofugal pathways, we performed the single neuron tracing using the recombinant virus.

Results: We initially found that 1) 57% of PV neurons co-expressed Lim-homeobox 6, 2) the PV-GP terminals were preferentially distributed in the ventral part of dorsal tier of SNc, 3) PV-GP neurons formed basket-like appositions with the somata of tyrosine hydroxylase, PV, calretinin and cholecystokinin immunoreactive neurons in the SN, and 4) in vitro whole cell recording during optogenetic photo-stimulation of PV-GP terminals in SNc demonstrated that PV-GP neurons strongly inhibited dopamine neurons via GABAA receptors. For the striatofugal pathways, we found that the neurons in the striosome compartment, but not matrix compartment, projected to SNc.

Conclusions: These results suggest that dopamine neurons receive direct focal inputs from PV-GP prototypic neurons. On the other hand, striatum-SNc inhibition originates from direct pathway MSNs that express the D1 receptor, whereas the D2, D3, D4, and D5 receptors are expressed in the perikarya and dendrites of GP neurons . Therefore, these pathways might exert different modes of dopaminergic modulation; and their timing, plasticity, and functional significance will be investigated further in future.

References: Oh Y-M, Karube F, Takahashi S, Kobayashi K, Takada M, Uchigashima M, Watanabe M, Nishizawa K, Kobayashi K and Fujiyama F. Using a novel PV-Cre rat model to characterize pallidonigral cells and their terminations. Brain Structure and Function, in press

Unzai, T., Kuramoto, E., Kaneko, T., Fujiyama, F. Quantitative Analyses of the Projection of individual Neurons from the Midline Thalamic Nuclei to the Striosome and Matrix Compartments of the Rat Striatum. Cerebral Cortex, In press.

Fujiyama, F., Nakano, T., Matsuda, W., Furuta, T., Udagawa. J., Kaneko, T. A Single-Neuron Tracing Study of Arkypallidal and Prototypic Neurons in Healthy Rats. Brain Structure and Function, In press. doi: 10.1007/s00429-015-1152-2

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MDS Abstracts - https://www.mdsabstracts.org/abstract/basal-ganglia-circuits-for-motor-and-behavioral-emotional-performances/