Home LiteratureArticle Details
PMID: 9221790 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Contributions of voltage-gated Ca2+ channels in the proximal versus distal dendrites to synaptic integration in prefrontal cortical neurons.

The Journal of neuroscience : the official journal of the Society for Neuroscience ·Vol. 17 ·No. 15 ·1997-08-01 ·Pages 5936-48

Seamans JK, Gorelova NA, Yang CR

Abstract

The electrogenesis of synaptically activated dendritic Ca2+-mediated potentials, which may contribute to synaptic signal integration in pyramidal cells, was examined in rat layers V-VI prefrontal cortical (PFC) neurons in vitro. Intrasomatically recorded suprathreshold synaptic responses evoked by stimulation of the distal dendrites were attenuated by focal Cd2+ application to the proximal apical dendritic stem (100-200 micron from soma), but not to the apical dendritic tuft (>500 micron from soma). With use of intracellular QX-314 and Cs+ to block Na+ and K+ currents, intrasomatic recordings revealed that the Cd2+-induced attenuation of synaptic responses was attributable to the blockade of a dendritic Ca2+-mediated "hump" potential and high-threshold Ca2+ spike activated by NMDA EPSPs. The hump potential was not blocked by bath application of Ni2+ (100 microM) but was blocked by focal application of Cd2+ to the proximal but not distal apical dendrites, suggesting that it was generated by Ca2+ channels located in the proximal dendrites. Direct patch-clamp recordings made from the distal apical tuft of layers V-VI PFC neurons revealed that layers I-II synaptic stimulation or intradendritic depolarizing current pulses evoked tetrodotoxin- and QX-314-sensitive Na+ spikes. Unlike in the stem of the apical dendrite, Ca2+ spikes were not easily evoked in the distal apical tuft when Na+ channels were blocked. When triggered, the Cd2+-sensitive Ca2+ spikes in the dendritic tuft were nonregenerative and had very high activation thresholds (approximately +10 mV). These results suggested that the high voltage-activated Ca2+ potentials that amplify distal EPSPs are primarily generated in the proximal stem of the apical dendrite and not within the fine dendritic branches of the apical tuft of layers V-VI PFC neurons.

MeSH Terms
Animals Calcium Channels/physiology Dendrites/physiology Male Patch-Clamp Techniques Prefrontal Cortex/physiology Rats Rats, Sprague-Dawley Synaptic Transmission/physiology
Chemicals
Calcium Channels
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Seamans J K
Department of Psychology, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada.
Gorelova N A
Yang C R
References (63)
63 references, click to expand
  1. Amplification of EPSPs by axosomatic sodium channels in neocortical pyramidal neurons.
    Neuron. 1995 Nov;15(5):1065-76 PMID: 7576650
  2. Dopaminergic innervation of the cerebral cortex: unexpected differences between rodents and primates.
    Trends Neurosci. 1991 Jan;14(1):21-7 PMID: 1709528
  3. EPSPs in rat neocortical neurons in vitro. II. Involvement of N-methyl-D-aspartate receptors in the generation of EPSPs.
    J Neurophysiol. 1989 Mar;61(3):621-34 PMID: 2565379
  4. Biochemical properties and subcellular distribution of an N-type calcium channel alpha 1 subunit.
    Neuron. 1992 Dec;9(6):1099-115 PMID: 1334419
  5. Nonlinear interactions in a dendritic tree: localization, timing, and role in information processing.
    Proc Natl Acad Sci U S A. 1983 May;80(9):2799-802 PMID: 6573680
  6. Synaptic physiology of horizontal connections in the cat's visual cortex.
    J Neurosci. 1991 Jun;11(6):1800-9 PMID: 1675266
  7. Calcium transients in dendrites of neocortical neurons evoked by single subthreshold excitatory postsynaptic potentials via low-voltage-activated calcium channels.
    Proc Natl Acad Sci U S A. 1994 May 24;91(11):5207-11 PMID: 8197208
  8. Magnesium gates glutamate-activated channels in mouse central neurones.
    Nature. 1984 Feb 2-8;307(5950):462-5 PMID: 6320006
  9. Apical dendrites of the neocortex: correlation between sodium- and calcium-dependent spiking and pyramidal cell morphology.
    J Neurosci. 1993 Dec;13(12):5301-11 PMID: 8254376
  10. Expression of N-methyl-D-aspartate glutamate receptor subunits in the prefrontal cortex of the rat.
    Neuroscience. 1996 Jul;73(2):417-27 PMID: 8783259
  11. Spatial profile of dendritic calcium transients evoked by action potentials in rat neocortical pyramidal neurones.
    J Physiol. 1995 Sep 15;487 ( Pt 3):583-600 PMID: 8544123
  12. Dendritic Na+ channels amplify EPSPs in hippocampal CA1 pyramidal cells.
    J Neurophysiol. 1996 Oct;76(4):2181-91 PMID: 8899593
  13. Negative slope conductance due to a persistent subthreshold sodium current in cat neocortical neurons in vitro.
    Brain Res. 1982 Mar 18;236(1):221-6 PMID: 6279236
  14. Electrophysiological properties of neocortical neurons in vitro.
    J Neurophysiol. 1982 Dec;48(6):1302-20 PMID: 6296328
  15. Amplification and linearization of distal synaptic input to cortical pyramidal cells.
    J Neurophysiol. 1994 Dec;72(6):2743-53 PMID: 7897486
  16. Dendritic glutamate receptor channels in rat hippocampal CA3 and CA1 pyramidal neurons.
    J Physiol. 1995 Jan 15;482 ( Pt 2):325-52 PMID: 7536248
  17. Afferent connections of the medial frontal cortex of the rat. II. Cortical and subcortical afferents.
    J Comp Neurol. 1995 Feb 20;352(4):567-93 PMID: 7722001
  18. Multiple types of neuronal calcium channels and their selective modulation.
    Trends Neurosci. 1988 Oct;11(10):431-8 PMID: 2469160
  19. Interpretation of voltage-clamp measurements in hippocampal neurons.
    J Neurophysiol. 1983 Aug;50(2):464-86 PMID: 6310063
  20. The spread of Na+ spikes determines the pattern of dendritic Ca2+ entry into hippocampal neurons.
    Nature. 1992 May 21;357(6375):244-6 PMID: 1350327
  21. Synaptic activation of voltage-gated channels in the dendrites of hippocampal pyramidal neurons.
    Science. 1995 Apr 14;268(5208):301-4 PMID: 7716525
  22. Ca2+ accumulations in dendrites of neocortical pyramidal neurons: an apical band and evidence for two functional compartments.
    Neuron. 1994 Jul;13(1):23-43 PMID: 8043278
  23. Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices.
    J Physiol. 1980 Aug;305:197-213 PMID: 7441553
  24. Synaptic physiology of horizontal afferents to layer I in slices of rat SI neocortex.
    J Neurosci. 1994 Feb;14(2):751-62 PMID: 7905516
  25. Intradendritic recordings from hippocampal neurons.
    Proc Natl Acad Sci U S A. 1979 Feb;76(2):986-90 PMID: 284423
  26. Mechanisms generating the time course of dual component excitatory synaptic currents recorded in hippocampal slices.
    Neuron. 1990 Sep;5(3):247-53 PMID: 1976014
  27. Effects of uniform and non-uniform synaptic 'activation-distributions' on the cable properties of modeled cortical pyramidal neurons.
    Brain Res. 1989 Dec 25;505(1):12-22 PMID: 2611664
  28. Branch input resistance and steady attenuation for input to one branch of a dendritic neuron model.
    Biophys J. 1973 Jul;13(7):648-87 PMID: 4715583
  29. Inhibitory control of excitable dendrites in neocortex.
    J Neurophysiol. 1995 Oct;74(4):1810-4 PMID: 8989418
  30. Synaptically activated increases in Ca2+ concentration in hippocampal CA1 pyramidal cells are primarily due to voltage-gated Ca2+ channels.
    Neuron. 1992 Dec;9(6):1163-73 PMID: 1361128
  31. Electrophysiology of GABA-mediated synaptic transmission and possible roles in epilepsy.
    Neurochem Res. 1991 Mar;16(3):251-62 PMID: 1664056
  32. A model of spike initiation in neocortical pyramidal neurons.
    Neuron. 1995 Dec;15(6):1427-39 PMID: 8845165
  33. Synaptic background activity influences spatiotemporal integration in single pyramidal cells.
    Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11569-73 PMID: 1763072
  34. Expression of the NMDA R1 receptor in selected human brain regions.
    Neuroreport. 1994 Apr 14;5(8):965-9 PMID: 8061305
  35. Electrophysiological and morphological properties of layers V-VI principal pyramidal cells in rat prefrontal cortex in vitro.
    J Neurosci. 1996 Mar 1;16(5):1904-21 PMID: 8774458
  36. Criteria for distinguishing between monosynaptic and polysynaptic transmission.
    Brain Res. 1976 Mar 19;105(1):1-20 PMID: 175886
  37. Active properties of neuronal dendrites.
    Annu Rev Neurosci. 1996;19:165-86 PMID: 8833440
  38. NMDA receptors in layers II and III of rat cerebral cortex.
    Brain Res. 1994 Oct 31;662(1-2):103-8 PMID: 7859061
  39. Active propagation of somatic action potentials into neocortical pyramidal cell dendrites.
    Nature. 1994 Jan 6;367(6458):69-72 PMID: 8107777
  40. Qualitative and quantitative comparison of the prefrontal cortex in rat and in primates, including humans.
    Prog Brain Res. 1990;85:31-62 PMID: 2094901
  41. D1 receptor activation enhances evoked discharge in neostriatal medium spiny neurons by modulating an L-type Ca2+ conductance.
    J Neurosci. 1997 May 1;17(9):3334-42 PMID: 9096166
  42. ELECTROPHYSIOLOGY OF HIPPOCAMPAL NEURONS: IV. FAST PREPOTENTIALS.
    J Neurophysiol. 1961 May 1;24(3):272-85 PMID: 25286477
  43. Signal enhancement in distal cortical dendrites by means of interactions between active dendritic spines.
    Proc Natl Acad Sci U S A. 1985 Apr;82(7):2192-5 PMID: 3856892
  44. Amplification of synaptic current by persistent sodium conductance in apical dendrite of neocortical neurons.
    J Neurophysiol. 1995 Nov;74(5):2220-4 PMID: 8592214
  45. Properties of persistent sodium conductance and calcium conductance of layer V neurons from cat sensorimotor cortex in vitro.
    J Neurophysiol. 1985 Jan;53(1):153-70 PMID: 2579215
  46. Clustering of L-type Ca2+ channels at the base of major dendrites in hippocampal pyramidal neurons.
    Nature. 1990 Sep 20;347(6290):281-4 PMID: 2169591
  47. Regenerative activity in apical dendrites of pyramidal cells in neocortex.
    Cereb Cortex. 1993 Jan-Feb;3(1):26-38 PMID: 8439739
  48. Subthreshold synaptic activation of voltage-gated Ca2+ channels mediates a localized Ca2+ influx into the dendrites of hippocampal pyramidal neurons.
    J Neurophysiol. 1995 Sep;74(3):1335-42 PMID: 7500154
  49. Dopamine D1 receptor actions in layers V-VI rat prefrontal cortex neurons in vitro: modulation of dendritic-somatic signal integration.
    J Neurosci. 1996 Mar 1;16(5):1922-35 PMID: 8774459
  50. In vivo dendritic calcium dynamics in neocortical pyramidal neurons.
    Nature. 1997 Jan 9;385(6612):161-5 PMID: 8990119
  51. Giant synaptic potential hypothesis for epileptiform activity.
    Science. 1981 Jan 16;211(4479):294-7 PMID: 7444469
  52. Dendritic integration in mammalian neurons, a century after Cajal.
    Neuron. 1996 Apr;16(4):701-16 PMID: 8607989
  53. Electrophysiology of isolated hippocampal pyramidal dendrites.
    J Neurosci. 1982 Nov;2(11):1614-22 PMID: 6292377
  54. Voltage- and space-clamp errors associated with the measurement of electrotonically remote synaptic events.
    J Neurophysiol. 1993 Aug;70(2):781-802 PMID: 8410172
  55. Distribution and synaptic localization of immunocytochemically identified NMDA receptor subunit proteins in sensory-motor and visual cortices of monkey and human.
    J Neurosci. 1994 Jun;14(6):3603-19 PMID: 8207475
  56. Stepwise repolarization from Ca2+ plateaus in neocortical pyramidal cells: evidence for nonhomogeneous distribution of HVA Ca2+ channels in dendrites.
    J Neurosci. 1993 Nov;13(11):4609-21 PMID: 8229187
  57. Calcium concentration dynamics produced by synaptic activation of CA1 hippocampal pyramidal cells.
    J Neurosci. 1992 Nov;12(11):4202-23 PMID: 1359030
  58. Differences between somatic and dendritic inhibition in the hippocampus.
    Neuron. 1996 Apr;16(4):815-23 PMID: 8607999
  59. Characterization of single voltage-gated Na+ and Ca2+ channels in apical dendrites of rat CA1 pyramidal neurons.
    J Physiol. 1995 Aug 15;487(1):67-90 PMID: 7473260
  60. Ca2+ signalling in postsynaptic dendrites and spines of mammalian neurons in brain slice.
    J Physiol Paris. 1992;86(1-3):57-66 PMID: 1343597
  61. Dendritic attenuation of synaptic potentials and currents: the role of passive membrane properties.
    Trends Neurosci. 1994 Apr;17(4):161-6 PMID: 7517596
  62. Synaptic control of excitability in isolated dendrites of hippocampal neurons.
    J Neurosci. 1984 Jan;4(1):217-27 PMID: 6693938
  63. Excitatory postsynaptic potentials recorded from regular-spiking cells in layers II/III of rat sensorimotor cortex.
    J Neurophysiol. 1992 Mar;67(3):728-37 PMID: 1349636
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
0270-6474
Published
1997-08-01
Pages
5936-48
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6573188
Subset
IM
External Links
PubMed source PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2