Home LiteratureArticle Details
PMID: 11826103 Published · ppublish English Journal Article

Cell type- and subcellular position-dependent summation of unitary postsynaptic potentials in neocortical neurons.

Tamás G, Szabadics J, Somogyi P

Abstract

Theoretical studies predict that the modes of integration of coincident inputs depend on their location and timing. To test these models experimentally, we simultaneously recorded from three neocortical neurons in vitro and investigated the effect of the subcellular position of two convergent inputs on the response summation in the common postsynaptic cell. When scattered over the somatodendritic surface, combination of two coincident excitatory or inhibitory synaptic potentials summed linearly in layer 2/3 pyramidal cells, as well as in GABAergic interneurons. Slightly sublinear summation with connection specific kinetics was observed when convergent inputs targeted closely placed sites on the postsynaptic cell. The degree of linearity of summation also depended on the type of connection, the relative timing of inputs, and the activation state of I(h). The results suggest that, when few inputs are active, the majority of afferent permutations undergo linear integration, maintaining the importance of individual inputs. However, compartment- and connection-specific nonlinear interactions between synapses located close to each other could increase the computational power of individual neurons in a cell type-specific manner.

MeSH Terms
Animals Cell Compartmentation/physiology Excitatory Postsynaptic Potentials/physiology In Vitro Techniques Interneurons/physiology Neocortex/cytology,physiology Neural Inhibition/physiology Neurons/physiology Patch-Clamp Techniques Pyramidal Cells/physiology Rats Rats, Wistar Reaction Time/physiology Synapses/physiology
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Tamás Gábor
Department of Comparative Physiology, University of Szeged, Szeged H-6726, Hungary.
Szabadics János
Somogyi Peter
References (40)
40 references, click to expand
  1. Spatial integration of local transmitter responses in motoneurones of the turtle spinal cord in vitro.
    J Physiol. 1994 Sep 1;479 ( Pt 2):233-46 PMID: 7799223
  2. 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
  3. High I(h) channel density in the distal apical dendrite of layer V pyramidal cells increases bidirectional attenuation of EPSPs.
    J Neurophysiol. 2001 Feb;85(2):855-68 PMID: 11160518
  4. Electrotonic architecture of hippocampal CA1 pyramidal neurons based on three-dimensional reconstructions.
    J Neurophysiol. 1996 Sep;76(3):1904-23 PMID: 8890303
  5. Neuronal networks for induced '40 Hz' rhythms.
    Trends Neurosci. 1996 May;19(5):202-8 PMID: 8723208
  6. Synaptic integration in an excitable dendritic tree.
    J Neurophysiol. 1993 Sep;70(3):1086-101 PMID: 8229160
  7. Orientation tuning of input conductance, excitation, and inhibition in cat primary visual cortex.
    J Neurophysiol. 2000 Aug;84(2):909-26 PMID: 10938316
  8. Response attenuation during coincident afferent excitatory inputs.
    J Neurophysiol. 1999 Jun;81(6):2945-55 PMID: 10368411
  9. The morphoelectrotonic transform: a graphical approach to dendritic function.
    J Neurosci. 1995 Mar;15(3 Pt 1):1669-82 PMID: 7891127
  10. Effects of inhibition and dendritic saturation in simulated neocortical pyramidal cells.
    J Neurophysiol. 1994 Jun;71(6):2183-93 PMID: 7523612
  11. Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex.
    J Neurophysiol. 1985 Oct;54(4):782-806 PMID: 2999347
  12. Impact of active dendrites and structural plasticity on the memory capacity of neural tissue.
    Neuron. 2001 Mar;29(3):779-96 PMID: 11301036
  13. Differential shunting of EPSPs by action potentials.
    Science. 2001 Jan 5;291(5501):138-41 PMID: 11141567
  14. Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons.
    Nat Neurosci. 2000 Apr;3(4):366-71 PMID: 10725926
  15. Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro.
    Nature. 1998 Jul 9;394(6689):186-9 PMID: 9671302
  16. Matching dendritic neuron models to experimental data.
    Physiol Rev. 1992 Oct;72(4 Suppl):S159-86 PMID: 1438585
  17. Logic operations are properties of computer-simulated interactions between excitable dendritic spines.
    Neuroscience. 1987 Apr;21(1):151-65 PMID: 3601072
  18. K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons.
    Nature. 1997 Jun 26;387(6636):869-75 PMID: 9202119
  19. Diversity and dynamics of dendritic signaling.
    Science. 2000 Oct 27;290(5492):739-44 PMID: 11052929
  20. Non-linear summation of unit synaptic potentials in spinal motoneurones of the cat.
    J Physiol. 1969 Apr;201(2):465-77 PMID: 5780554
  21. Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons.
    J Neurosci. 1998 Oct 1;18(19):7613-24 PMID: 9742133
  22. Impact of network activity on the integrative properties of neocortical pyramidal neurons in vivo.
    J Neurophysiol. 1999 Apr;81(4):1531-47 PMID: 10200189
  23. Voltage-activated sodium channels amplify inhibition in neocortical pyramidal neurons.
    Nat Neurosci. 1999 Feb;2(2):144-50 PMID: 10195198
  24. Active properties of neuronal dendrites.
    Annu Rev Neurosci. 1996;19:165-86 PMID: 8833440
  25. Direction selectivity of synaptic potentials in simple cells of the cat visual cortex.
    J Neurophysiol. 1997 Nov;78(5):2772-89 PMID: 9356425
  26. Detailed passive cable models of whole-cell recorded CA3 pyramidal neurons in rat hippocampal slices.
    J Neurosci. 1994 Aug;14(8):4613-38 PMID: 8046439
  27. Summation of excitatory postsynaptic potentials in hippocampal pyramidal cells.
    J Neurophysiol. 1983 Dec;50(6):1320-9 PMID: 6663329
  28. Reliability and state dependence of pyramidal cell-interneuron synapses in the hippocampus: an ensemble approach in the behaving rat.
    Neuron. 1998 Jul;21(1):179-89 PMID: 9697862
  29. Differential signaling via the same axon of neocortical pyramidal neurons.
    Proc Natl Acad Sci U S A. 1998 Apr 28;95(9):5323-8 PMID: 9560274
  30. Selective responses of visual cortical cells do not depend on shunting inhibition.
    Nature. 1988 Apr 14;332(6165):642-4 PMID: 3357519
  31. Submillisecond AMPA receptor-mediated signaling at a principal neuron-interneuron synapse.
    Neuron. 1997 Jun;18(6):1009-23 PMID: 9208867
  32. Salient features of synaptic organisation in the cerebral cortex.
    Brain Res Brain Res Rev. 1998 May;26(2-3):113-35 PMID: 9651498
  33. Linear summation of excitatory inputs by CA1 pyramidal neurons.
    Neuron. 1999 Feb;22(2):383-94 PMID: 10069343
  34. Amplification of EPSPs by low Ni(2+)- and amiloride-sensitive Ca2+ channels in apical dendrites of rat CA1 pyramidal neurons.
    J Neurophysiol. 1997 Mar;77(3):1639-43 PMID: 9084628
  35. Visual input evokes transient and strong shunting inhibition in visual cortical neurons.
    Nature. 1998 May 28;393(6683):369-73 PMID: 9620800
  36. Target-cell-specific facilitation and depression in neocortical circuits.
    Nat Neurosci. 1998 Aug;1(4):279-85 PMID: 10195160
  37. Linearity of summation of synaptic potentials underlying direction selectivity in simple cells of the cat visual cortex.
    Science. 1993 Dec 17;262(5141):1901-4 PMID: 8266083
  38. Site independence of EPSP time course is mediated by dendritic I(h) in neocortical pyramidal neurons.
    J Neurophysiol. 2000 May;83(5):3177-82 PMID: 10805715
  39. Synaptic integration in striate cortical simple cells.
    J Neurosci. 1998 Nov 15;18(22):9517-28 PMID: 9801388
  40. Total number and ratio of excitatory and inhibitory synapses converging onto single interneurons of different types in the CA1 area of the rat hippocampus.
    J Neurosci. 1999 Nov 15;19(22):10082-97 PMID: 10559416
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2002-02-01
Pages
740-7
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6758512
Subset
IM
Grants
Wellcome Trust · United Kingdom
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