Synaptic-like axo-axonal transmission from striatal cholinergic interneurons onto dopaminergic fibers

被引:55
作者
Kramer, Paul F. [1 ]
-Weil, Samuel G. Brill [1 ]
Cummins, Alex C. [2 ]
Zhang, Renshu [1 ]
Camacho-Hernandez, Gisela A. [3 ]
Newman, Amy H. [3 ]
Eldridge, Mark A. G. [2 ]
Averbeck, Bruno B. [2 ]
Khaliq, Zayd M. [1 ]
机构
[1] Natl Inst Neurol Disorders & Stroke Intramural Res, NIH, Cellular Neurophysiol Sect, Bethesda, MD 20892 USA
[2] Natl Inst Mental Hlth Intramural Res Program, NIH, Lab Neuropsychol, Bethesda, MD 20892 USA
[3] Natl Inst Drug Abuse Intramural Res Program, NIH, Med Chem Sect, MD21224, Baltimore, MD USA
关键词
NICOTINIC ACETYLCHOLINE-RECEPTORS; TONICALLY ACTIVE NEURONS; ALPHA-CONOTOXIN-MII; SUBSTANTIA-NIGRA; RELEASE; NEUROTRANSMISSION; INNERVATION; ENHANCEMENT; MODULATION; ACTIVATION;
D O I
10.1016/j.neuron.2022.07.011
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
Transmission from striatal cholinergic interneurons (CINs) controls dopamine release through nicotinic acetylcholine receptors (nAChRs) on dopaminergic axons. Anatomical studies suggest that cholinergic ter-minals signal predominantly through non-synaptic volume transmission. However, the influence of cholin-ergic transmission on electrical signaling in axons remains unclear. We examined axo-axonal transmission from CINs onto dopaminergic axons using perforated-patch recordings, which revealed rapid spontaneous EPSPs with properties characteristic of fast synapses. Pharmacology showed that axonal EPSPs (axEPSPs) were mediated primarily by high-affinity a6-containing receptors. Remarkably, axEPSPs triggered sponta-neous action potentials, suggesting that these axons perform integration to convert synaptic input into spiking, a function associated with somatodendritic compartments. We investigated the cross-species val-idity of cholinergic axo-axonal transmission by recording dopaminergic axons in macaque putamen and found similar axEPSPs. Thus, we reveal that synaptic-like neurotransmission underlies cholinergic signaling onto dopaminergic axons, supporting the idea that striatal dopamine release can occur independently of somatic firing to provide distinct signaling.
引用
收藏
页码:2949 / +
页数:17
相关论文
共 75 条
[1]   Prefrontal Cortex-Driven Dopamine Signals in the Striatum Show Unique Spatial and Pharmacological Properties [J].
Adrover, Martin F. ;
Shin, Jung Hoon ;
Quiroz, Cesar ;
Ferre, Sergi ;
Lemos, Julia C. ;
Alvarez, Veronica A. .
JOURNAL OF NEUROSCIENCE, 2020, 40 (39) :7510-7522
[2]  
AOSAKI T, 1994, J NEUROSCI, V14, P3969
[3]   Responses of tonically discharging neurons in the monkey striatum to primary rewards delivered during different behavioral states [J].
Apicella, P ;
Legallet, E ;
Trouche, E .
EXPERIMENTAL BRAIN RESEARCH, 1997, 116 (03) :456-466
[4]   Fine structural features of the acetylcholine innervation in the developing neostriatum of rat [J].
Aznavour, N ;
Mechawar, N ;
Watkins, KC ;
Descarries, L .
JOURNAL OF COMPARATIVE NEUROLOGY, 2003, 460 (02) :280-291
[5]   Vesicular dopamine release elicits an inhibitory postsynaptic current in midbrain dopamine neurons [J].
Beckstead, MJ ;
Grandy, DK ;
Wickman, K ;
Williams, JT .
NEURON, 2004, 42 (06) :939-946
[6]   Mechanisms Generating Dual-Component Nicotinic EPSCs in Cortical Interneurons [J].
Bennett, Corbett ;
Arroyo, Sergio ;
Berns, Dominic ;
Hestrin, Shaul .
JOURNAL OF NEUROSCIENCE, 2012, 32 (48) :17287-17296
[7]   α-Conotoxin MII-Sensitive Nicotinic Acetylcholine Receptors in the Nucleus Accumbens Shell Regulate Progressive Ratio Responding Maintained by Nicotine [J].
Brunzell, Darlene H. ;
Boschen, Karen E. ;
Hendrick, Elizabeth S. ;
Beardsley, Patrick M. ;
McIntosh, J. Michael .
NEUROPSYCHOPHARMACOLOGY, 2010, 35 (03) :665-673
[8]   Selective Activation of Cholinergic Interneurons Enhances Accumbal Phasic Dopamine Release: Setting the Tone for Reward Processing [J].
Cachope, Roger ;
Mateo, Yolanda ;
Mathur, Brian N. ;
Irving, James ;
Wang, Hui-Ling ;
Morales, Marisela ;
Lovinger, David M. ;
Cheer, Joseph F. .
CELL REPORTS, 2012, 2 (01) :33-41
[10]   Pharmacological and functional comparisons of α6/α3β2β3-nAChRs and α4β2-nAChRs heterologously expressed in the human epithelial SH-EP1 cell line [J].
Chen, De-jie ;
Gao, Fen-fei ;
Ma, Xiao-kuang ;
Shi, Gang-gang ;
Huang, Yuan-bing ;
Su, Quang-xi ;
Sud-Weeks, Sterling ;
Gao, Ming ;
Dharshaun, Turner ;
Eaton, Jason Brek ;
Chang, Yong-chang ;
Mcintosh, J. Michael ;
Lukas, Ronald J. ;
Whiteaker, Paul ;
Steffensen, Scott C. ;
Wu, Jie .
ACTA PHARMACOLOGICA SINICA, 2018, 39 (10) :1571-1581