Functional Properties of AMPA and NMDA Receptors Expressed in Identified Types of Basal Ganglia Neurons

Overview

Journal J Neurosci

Specialty Neurology

Date 1997 Jan 1

PMID 8987749

Citations 65

Authors

T Gotz

U Kraushaar

J Geiger

J Lubke

T Berger

P Jonas

Affiliations

Soon will be listed here.

Abstract

AMPA- and NMDA-type glutamate receptors (AMPARs and NMDARs) mediate excitatory synaptic transmission in the basal ganglia and may contribute to excitotoxic injury. We investigated the functional properties of AMPARs and NMDARs expressed by six main types of basal ganglia neurons in acute rat brain slices (principal neurons and cholinergic interneurons of striatum, GABAergic and dopaminergic neurons of substantia nigra, globus pallidus neurons, and subthalamic nucleus neurons) using fast application of glutamate to nucleated and outside-out membrane patches. AMPARs in different types of basal ganglia neurons were functionally distinct. Those expressed in striatal principal neurons exhibited the slowest gating (desensitization time constant tau = 11.5 msec, 1 mM glutamate, 22 degrees C), whereas those in striatal cholinergic interneurons showed the fastest gating (desensitization time constant tau = 3.6 msec). The lowest Ca2+ permeability of AMPARs was observed in nigral dopaminergic neurons (PCa/PNa = 0.10), whereas the highest Ca2+ permeability was found in subthalamic nucleus neurons (PCa/PNa = 1.17). NMDARs of different types of basal ganglia neurons were less variable in their functional properties; those expressed in nigral dopaminergic neurons exhibited the slowest gating (deactivation time constant of predominant fast component tau1 = 150 msec, 100 microM glutamate), and those of globus pallidus neurons showed the fastest gating (tau1 = 67 msec). The Mg2+ block of NMDARs was similar; the average chord conductance ratio g-60mV/g+40mV was 0.18-0.22 in 100 microM external Mg2+. Hence, AMPARs expressed in different types of basal ganglia neurons are markedly diverse, whereas NMDARs are less variable in functional properties that are relevant for excitatory synaptic transmission and neuronal vulnerability.

Citing Articles

Extrinsic and intrinsic control of striatal cholinergic interneuron activity.

Ratna D, Francis T Front Mol Neurosci. 2025; 18:1528419.

PMID: 40018010 PMC: 11865219. DOI: 10.3389/fnmol.2025.1528419.

Break-up and recovery of harmony between direct and indirect pathways in the basal ganglia: Huntington's disease and treatment.

Kim S, Lim W Cogn Neurodyn. 2024; 18(5):2909-2924.

PMID: 39555304 PMC: 11564723. DOI: 10.1007/s11571-024-10125-w.

Quantifying harmony between direct and indirect pathways in the basal ganglia: healthy and Parkinsonian states.

Kim S, Lim W Cogn Neurodyn. 2024; 18(5):2809-2829.

PMID: 39555274 PMC: 11564607. DOI: 10.1007/s11571-024-10119-8.

The diversity of AMPA receptor inhibition mechanisms among amidine-containing compounds.

Zhigulin A, Dron M, Barygin O, Tikhonov D Front Pharmacol. 2024; 15:1467266.

PMID: 39444609 PMC: 11496081. DOI: 10.3389/fphar.2024.1467266.

The Pentameric Ligand-Gated Ion Channel Family: A New Member of the Voltage Gated Ion Channel Superfamily?.

Dubey A, Baxter M, Hendargo K, Medrano-Soto A, Saier Jr M Int J Mol Sci. 2024; 25(9).

PMID: 38732224 PMC: 11084639. DOI: 10.3390/ijms25095005.

References

Albin R, Young A, Penney J . The functional anatomy of basal ganglia disorders. Trends Neurosci. 1989; 12(10):366-75. DOI: 10.1016/0166-2236(89)90074-x. View

Stuart G, Dodt H, Sakmann B . Patch-clamp recordings from the soma and dendrites of neurons in brain slices using infrared video microscopy. Pflugers Arch. 1993; 423(5-6):511-8. DOI: 10.1007/BF00374949. View

Jonas P, Burnashev N . Molecular mechanisms controlling calcium entry through AMPA-type glutamate receptor channels. Neuron. 1995; 15(5):987-90. DOI: 10.1016/0896-6273(95)90087-x. View

Monyer H, Burnashev N, Laurie D, Sakmann B, Seeburg P . Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron. 1994; 12(3):529-40. DOI: 10.1016/0896-6273(94)90210-0. View

Parent A, Hazrati L . Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain Res Brain Res Rev. 1995; 20(1):91-127. DOI: 10.1016/0165-0173(94)00007-c. View

Standaert D, Testa C, Young A, Penney Jr J . Organization of N-methyl-D-aspartate glutamate receptor gene expression in the basal ganglia of the rat. J Comp Neurol. 1994; 343(1):1-16. DOI: 10.1002/cne.903430102. View

Silver R, Colquhoun D, Cull-Candy S, Edmonds B . Deactivation and desensitization of non-NMDA receptors in patches and the time course of EPSCs in rat cerebellar granule cells. J Physiol. 1996; 493 ( Pt 1):167-73. PMC: 1158958. DOI: 10.1113/jphysiol.1996.sp021372. View

Chen Q, Harris C, Brown C, Howe A, Surmeier D, Reiner A . Glutamate-mediated excitotoxic death of cultured striatal neurons is mediated by non-NMDA receptors. Exp Neurol. 1995; 136(2):212-24. DOI: 10.1006/exnr.1995.1098. View

Choi D . Glutamate neurotoxicity and diseases of the nervous system. Neuron. 1988; 1(8):623-34. DOI: 10.1016/0896-6273(88)90162-6. View

10.

Calabresi P, Maj R, Pisani A, Mercuri N, Bernardi G . Long-term synaptic depression in the striatum: physiological and pharmacological characterization. J Neurosci. 1992; 12(11):4224-33. PMC: 6576009. View

11.

RINVIK E, Ottersen O . Terminals of subthalamonigral fibres are enriched with glutamate-like immunoreactivity: an electron microscopic, immunogold analysis in the cat. J Chem Neuroanat. 1993; 6(1):19-30. DOI: 10.1016/0891-0618(93)90004-n. View

12.

Nowak L, Bregestovski P, Ascher P, Herbet A, Prochiantz A . Magnesium gates glutamate-activated channels in mouse central neurones. Nature. 1984; 307(5950):462-5. DOI: 10.1038/307462a0. View

13.

Celio M . Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience. 1990; 35(2):375-475. DOI: 10.1016/0306-4522(90)90091-h. View

14.

Petralia R, Wenthold R . Light and electron immunocytochemical localization of AMPA-selective glutamate receptors in the rat brain. J Comp Neurol. 1992; 318(3):329-54. DOI: 10.1002/cne.903180309. View

15.

Beal M, Ferrante R, Swartz K, Kowall N . Chronic quinolinic acid lesions in rats closely resemble Huntington's disease. J Neurosci. 1991; 11(6):1649-59. PMC: 6575424. View

16.

HESTRIN S . Different glutamate receptor channels mediate fast excitatory synaptic currents in inhibitory and excitatory cortical neurons. Neuron. 1993; 11(6):1083-91. DOI: 10.1016/0896-6273(93)90221-c. View

17.

Patneau D, Mayer M . Kinetic analysis of interactions between kainate and AMPA: evidence for activation of a single receptor in mouse hippocampal neurons. Neuron. 1991; 6(5):785-98. DOI: 10.1016/0896-6273(91)90175-y. View

18.

Koh D, Geiger J, Jonas P, Sakmann B . Ca(2+)-permeable AMPA and NMDA receptor channels in basket cells of rat hippocampal dentate gyrus. J Physiol. 1995; 485 ( Pt 2):383-402. PMC: 1158000. DOI: 10.1113/jphysiol.1995.sp020737. View

19.

Mori A, Takahashi T, Miyashita Y, Kasai H . Two distinct glutamatergic synaptic inputs to striatal medium spiny neurones of neonatal rats and paired-pulse depression. J Physiol. 1994; 476(2):217-28. PMC: 1160435. DOI: 10.1113/jphysiol.1994.sp020125. View

20.

Mosbacher J, Schoepfer R, Monyer H, Burnashev N, Seeburg P, Ruppersberg J . A molecular determinant for submillisecond desensitization in glutamate receptors. Science. 1994; 266(5187):1059-62. DOI: 10.1126/science.7973663. View