Synaptic determinants of cholinergic interneurons hyperactivity during parkinsonism


Por: Padilla-Orozco, Montserrat, Duhne, Mariana, Fuentes-Serrano, Alejandra, Ortega, Aidan, Galarraga, Elvira, BARGAS, JOSE, Lara-Gonzalez, Esther

Publicada: 6 sep 2022
Resumen:
Parkinson's disease is a neurodegenerative ailment generated by the loss of dopamine in the basal ganglia, mainly in the striatum. The disease courses with increased striatal levels of acetylcholine, disrupting the balance among these modulatory transmitters. These modifications disturb the excitatory and inhibitory balance in the striatal circuitry, as reflected in the activity of projection striatal neurons. In addition, changes in the firing pattern of striatal tonically active interneurons during the disease, including cholinergic interneurons (CINs), are being searched. Dopamine-depleted striatal circuits exhibit pathological hyperactivity as compared to controls. One aim of this study was to show how striatal CINs contribute to this hyperactivity. A second aim was to show the contribution of extrinsic synaptic inputs to striatal CINs hyperactivity. Electrophysiological and calcium imaging recordings in Cre-mice allowed us to evaluate the activity of dozens of identified CINs with single-cell resolution in ex vivo brain slices. CINs show hyperactivity with bursts and silences in the dopamine-depleted striatum. We confirmed that the intrinsic differences between the activity of control and dopamine-depleted CINs are one source of their hyperactivity. We also show that a great part of this hyperactivity and firing pattern change is a product of extrinsic synaptic inputs, targeting CINs. Both glutamatergic and GABAergic inputs are essential to sustain hyperactivity. In addition, cholinergic transmission through nicotinic receptors also participates, suggesting that the joint activity of CINs drives the phenomenon; since striatal CINs express nicotinic receptors, not expressed in striatal projection neurons. Therefore, CINs hyperactivity is the result of changes in intrinsic properties and excitatory and inhibitory inputs, in addition to the modification of local circuitry due to cholinergic nicotinic transmission. We conclude that CINs are the main drivers of the pathological hyperactivity present in the striatum that is depleted of dopamine, and this is, in part, a result of extrinsic synaptic inputs. These results show that CINs may be a main therapeutic target to treat Parkinson's disease by intervening in their synaptic inputs.

Filiaciones:
Padilla-Orozco, Montserrat:
 Univ Nacl Autonoma Mexico, Inst Fisiol Celular, Div Neurociencias, Mexico City, DF, Mexico

Duhne, Mariana:
 Univ Nacl Autonoma Mexico, Inst Fisiol Celular, Div Neurociencias, Mexico City, DF, Mexico

 Univ Calif San Francisco, Dept Neurol, San Francisco, CA USA

Fuentes-Serrano, Alejandra:
 Univ Nacl Autonoma Mexico, Inst Fisiol Celular, Div Neurociencias, Mexico City, DF, Mexico

Ortega, Aidan:
 Univ Nacl Autonoma Mexico, Inst Fisiol Celular, Div Neurociencias, Mexico City, DF, Mexico

Galarraga, Elvira:
 Univ Nacl Autonoma Mexico, Inst Fisiol Celular, Div Neurociencias, Mexico City, DF, Mexico

BARGAS, JOSE:
 Univ Nacl Autonoma Mexico, Inst Fisiol Celular, Div Neurociencias, Mexico City, DF, Mexico

Lara-Gonzalez, Esther:
 Univ Nacl Autonoma Mexico, Inst Fisiol Celular, Div Neurociencias, Mexico City, DF, Mexico

 Northwestern Univ, Dept Neurosci, Feinberg Sch Med, Chicago, IL 60611 USA
ISSN: 16633563
Editorial
Frontiers Research Foundation, EPFL SCIENCE PARK, BLDG D, LAUSANNE, 1015, SWITZERLAND, Suiza
Tipo de documento: Article
Volumen: 14 Número:
Páginas:
WOS Id: 000855839200001
ID de PubMed: 36147730
imagen Green Published, gold, All Open Access; Gold

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