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PMID: 11356859 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Presynaptic Ca2+ channels and neurotransmitter release at the terminal of a mouse cortical neuron.

Qian J, Noebels JL

Abstract

Regional variation in synaptic efficacy is an important determinant of associative processing as information flows through major circuits of the brain. The perforant path is the principal route of entry from cortex to the hippocampus and contains the first synapse in the cortical-hippocampal projection pathway. We used optical imaging techniques to analyze presynaptic Ca(2+) entry and neurotransmitter release at synapses in the medial perforant path linking stellate neurons located in layer II of the entorhinal cortex to granule cells in the dentate gyrus. Similar to other excitatory central synapses, the relationship between neurotransmitter release and the amount of Ca(2+) influx can be best described by a Hill equation with a Hill coefficient of 3.5. Our Ca(2+) channel toxin studies indicate that P/Q-type channels are the predominant Ca(2+) source triggering neurotransmitter release in this pathway, as shown by a potent inhibition of Ca(2+) entry and synaptic transmission by the P/Q-type channel blocker omega-agatoxin IVA. However, compared with the downstream hippocampal pyramidal neuron CA3-CA1 synapse, neurotransmitter release was less sensitive to the N-type Ca(2+) channel blocker omega-conotoxin GVIA, although the amount of N-type Ca(2+) current is comparable. The contribution of N-type channels to neurotransmitter release approximates that found at the CA3-CA1 synapse when tested under lower [Ca(2+)](o), which effectively reduces the size of the Ca(2+) microdomain surrounding each channel. These results suggest that P/Q-type channels are more closely associated with release machinery then N-type channels at this synapse and that cooperativity differences for each channel subtype may characterize variations in signaling at central synapses.

MeSH Terms
Animals Calcium/metabolism Calcium Channel Blockers/pharmacology Calcium Channels/classification,metabolism Calcium Channels, N-Type/metabolism Calcium Channels, P-Type/metabolism Calcium Channels, Q-Type/metabolism Dentate Gyrus/cytology,physiology Entorhinal Cortex/cytology,drug effects,metabolism Excitatory Postsynaptic Potentials/drug effects,physiology Fluorescent Dyes In Vitro Techniques Mice Models, Neurological Neurons/drug effects,metabolism Neurotransmitter Agents/metabolism Perforant Pathway/cytology,drug effects,metabolism Presynaptic Terminals/drug effects,metabolism Pyramidal Cells/drug effects,metabolism
Chemicals
Calcium Channel Blockers Calcium Channels Calcium Channels, N-Type Calcium Channels, P-Type Calcium Channels, Q-Type Fluorescent Dyes Neurotransmitter Agents Calcium
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Qian J
Department of Neurology, Baylor College of Medicine, Houston, Texas 77030, USA.
Noebels J L
References (24)
24 references, click to expand
  1. Pharmacological identification of two types of presynaptic voltage-dependent calcium channels at CA3-CA1 synapses of the hippocampus.
    J Neurosci. 1994 Sep;14(9):5613-22 PMID: 8083757
  2. Subunit interaction sites in voltage-dependent Ca2+ channels: role in channel function.
    Trends Neurosci. 1998 Apr;21(4):148-54 PMID: 9554724
  3. Roles of N-type and Q-type Ca2+ channels in supporting hippocampal synaptic transmission.
    Science. 1994 Apr 1;264(5155):107-11 PMID: 7832825
  4. Calcium channel types with distinct presynaptic localization couple differentially to transmitter release in single calyx-type synapses.
    J Neurosci. 1999 Jan 15;19(2):726-36 PMID: 9880593
  5. Modeling study of the effects of overlapping Ca2+ microdomains on neurotransmitter release.
    Biophys J. 1999 Feb;76(2):735-50 PMID: 9929478
  6. Inhibition of synaptic transmission by neuropeptide Y in rat hippocampal area CA1: modulation of presynaptic Ca2+ entry.
    J Neurosci. 1997 Nov 1;17(21):8169-77 PMID: 9334392
  7. Coincidence detection and changes of synaptic efficacy in spiny stellate neurons in rat barrel cortex.
    Nat Neurosci. 1999 Dec;2(12):1098-105 PMID: 10570487
  8. Calcium influx and transmitter release in a fast CNS synapse.
    Nature. 1996 Oct 3;383(6599):431-4 PMID: 8837774
  9. Properties of Q-type calcium channels in neostriatal and cortical neurons are correlated with beta subunit expression.
    J Neurosci. 1999 Sep 1;19(17):7268-77 PMID: 10460233
  10. Mouse SmI cortex: qualitative and quantitative classification of golgi-impregnated barrel neurons.
    Proc Natl Acad Sci U S A. 1975 Jun;72(6):2165-9 PMID: 1056021
  11. Modulation of transmitter release by action potential duration at the hippocampal CA3-CA1 synapse.
    J Neurophysiol. 1999 Jan;81(1):288-98 PMID: 9914289
  12. Differential electroresponsiveness of stellate and pyramidal-like cells of medial entorhinal cortex layer II.
    J Neurophysiol. 1993 Jul;70(1):128-43 PMID: 8395571
  13. Evidence for two physiologically distinct perforant pathways to the fascia dentata.
    Brain Res. 1980 Oct 13;199(1):1-19 PMID: 7407615
  14. Morphological characteristics of layer II projection neurons in the rat medial entorhinal cortex.
    Hippocampus. 1997;7(5):571-83 PMID: 9347353
  15. Presynaptic Ca(2+) influx at a mouse central synapse with Ca(2+) channel subunit mutations.
    J Neurosci. 2000 Jan 1;20(1):163-70 PMID: 10627593
  16. Splicing of alpha 1A subunit gene generates phenotypic variants of P- and Q-type calcium channels.
    Nat Neurosci. 1999 May;2(5):407-15 PMID: 10321243
  17. Changes in action potential duration alter reliance of excitatory synaptic transmission on multiple types of Ca2+ channels in rat hippocampus.
    J Neurosci. 1996 Apr 1;16(7):2226-37 PMID: 8601803
  18. The forms of non-pyramidal neurons in the visual cortex of the rat.
    J Comp Neurol. 1978 Jun 15;179(4):761-93 PMID: 346619
  19. Calcium control of transmitter release at a cerebellar synapse.
    Neuron. 1995 Sep;15(3):675-88 PMID: 7546746
  20. Mutation of the Ca2+ channel beta subunit gene Cchb4 is associated with ataxia and seizures in the lethargic (lh) mouse.
    Cell. 1997 Feb 7;88(3):385-92 PMID: 9039265
  21. Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat.
    J Comp Neurol. 1976 Oct 1;169(3):347-70 PMID: 972204
  22. Reliable synaptic connections between pairs of excitatory layer 4 neurones within a single 'barrel' of developing rat somatosensory cortex.
    J Physiol. 1999 Nov 15;521 Pt 1:169-90 PMID: 10562343
  23. Presynaptic calcium is increased during normal synaptic transmission and paired-pulse facilitation, but not in long-term potentiation in area CA1 of hippocampus.
    J Neurosci. 1994 Feb;14(2):645-54 PMID: 7905515
  24. Synaptic efficacy and reliability of excitatory connections between the principal neurones of the input (layer 4) and output layer (layer 5) of the neocortex.
    J Physiol. 2000 May 15;525 Pt 1:31-9 PMID: 10811722
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2001-06-01
Pages
3721-8
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6762720
Subset
IM
Grants
NINDS NIH HHS · R01 NS029709 · United States
NINDS NIH HHS · NS29709 · United States
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