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PMID: 1666655 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

A functional microcircuit for cat visual cortex.

The Journal of physiology ·Vol. 440 ·1991-00-00 ·Pages 735-69

Douglas RJ, Martin KA

Abstract

1. We have studied in vivo the intracellular responses of neurones in cat visual cortex to electrical pulse stimulation of the cortical afferents and have developed a microcircuit that simulates much of the experimental data. 2. Inhibition and excitation are not separable events, because individual neurones are embedded in microcircuits that contribute strong population effects. Synchronous electrical activation of the cortex inevitably set in motion a sequence of excitation and inhibition in every neurone we recorded. The temporal form of this response depends on the cortical layer in which the neurone is located. Superficial layer (layers 2+3) pyramidal neurones show a more marked polysynaptic excitatory phase than the pyramids of the deep layers (layers 5+6). 3. Excitatory effects on pyramidal neurones, particularly the superficial layer pyramids, are in general not due to monosynaptic input from thalamus, but polysynaptic input from cortical pyramids. Since the thalamic input is transient it does not provide the major, sustained excitation arriving at any cortical neurone. Instead the intracortical excitatory connections provide the major component of the excitation. 4. The polysynaptic excitatory response would be sustained well after the stimulus, were it not for the suppressive effect of intracortical inhibition induced by the pulse stimulation. 5. Intracellular recording combined with ionophoresis of gamma-aminobutyric acid (GABA) agonists and antagonists showed that intracortical inhibition is mediated by GABAA and GABAB receptors. The GABAA component occurs in the early phase of the impulse response. It is reflected in the strong hyperpolarization that follows the excitatory response and lasts about 50 ms. The GABAB component occurs in the late phase of the response, and is reflected in a sustained hyperpolarization that lasts some 200-300 ms. Both components are seen in all cortical pyramidal neurones. However, the GABAA component appears more powerful in deep layer pyramids than superficial layer pyramids. 6. The microcircuit simulates with good fidelity the above data from experiments in vivo and provides a novel explantation for the apparent lack of significant inhibition during visual stimulation. The basic circuit may be common to all cortical areas studied and thus the microcircuit may be a 'canonical' microcircuit for neocortex.

MeSH Terms
Animals Baclofen/pharmacology Bicuculline/pharmacology Cats Computer Simulation Electric Stimulation Evoked Potentials, Visual/drug effects Models, Neurological Neural Inhibition/physiology Neurons, Afferent/physiology Receptors, GABA-A/physiology Visual Cortex/physiology
Chemicals
Receptors, GABA-A Baclofen Bicuculline
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Douglas R J
MRC Anatomical Neuropharmacology Unit, Department of Pharmacology, Oxford.
Martin K A
References (64)
64 references, click to expand
  1. Laminar differences in receptive field properties of cells in cat primary visual cortex.
    J Physiol. 1977 Jun;268(2):391-421 PMID: 874916
  2. An electron microscopic study of the types and proportions of neurons in the cortex of the motor and visual areas of the cat and rat.
    Brain. 1980 Jun;103(2):245-58 PMID: 6772267
  3. Antidromic identification of association, commissural and corticofugal efferent cells in cat visual cortex.
    Brain Res. 1969 Jul;14(2):513-7 PMID: 5794921
  4. Postsynaptic potentials in the cat's visual cortex following electrical stimulation of afferent pathways.
    Exp Brain Res. 1966;1(3):272-83 PMID: 5920554
  5. Responses to visual contours: spatio-temporal aspects of excitation in the receptive fields of simple striate neurones.
    J Physiol. 1971 Dec;219(3):625-57 PMID: 5157596
  6. Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex.
    J Neurophysiol. 1985 Oct;54(4):782-806 PMID: 2999347
  7. Excitation by geniculocortical synapses is not 'vetoed' at the level of dendritic spines in cat visual cortex.
    J Physiol. 1991;440:723-34 PMID: 1804984
  8. Targets and Quantitative Distribution of GABAergic Synapses in the Visual Cortex of the Cat.
    Eur J Neurosci. 1990;2(4):296-303 PMID: 12106036
  9. Visibility of synaptically induced conductance changes: theory and simulations of anatomically characterized cortical pyramidal cells.
    J Neurosci. 1990 Jun;10(6):1728-44 PMID: 2355247
  10. Cortical inhibition and gamma-aminobutyric acid.
    Exp Brain Res. 1969;9(2):137-54 PMID: 5346460
  11. Direction selectivity of simple striate cells: properties and mechanism.
    J Neurophysiol. 1975 Nov;38(6):1500-23 PMID: 1221086
  12. Inhibitory mechanisms influencing complex cell orientation selectivity and their modification at high resting discharge levels.
    J Physiol. 1979 Apr;289:33-53 PMID: 458666
  13. Modification of orientation sensitivity of cat visual cortex neurons by removal of GABA-mediated inhibition.
    Exp Brain Res. 1979 Jan 15;34(2):351-63 PMID: 421752
  14. Slow conductances in neurons from cat sensorimotor cortex in vitro and their role in slow excitability changes.
    J Neurophysiol. 1988 Feb;59(2):450-67 PMID: 3351570
  15. Innervation of cat visual areas 17 and 18 by physiologically identified X- and Y- type thalamic afferents. I. Arborization patterns and quantitative distribution of postsynaptic elements.
    J Comp Neurol. 1985 Dec 8;242(2):263-74 PMID: 4086666
  16. Anatomical organization of the primary visual cortex (area 17) of the cat. A comparison with area 17 of the macaque monkey.
    J Comp Neurol. 1979 Apr 15;184(4):599-618 PMID: 106072
  17. An intracellular analysis of geniculo-cortical connectivity in area 17 of the cat.
    J Physiol. 1983 Sep;342:181-215 PMID: 6631731
  18. Multiple potassium conductances and their functions in neurons from cat sensorimotor cortex in vitro.
    J Neurophysiol. 1988 Feb;59(2):424-49 PMID: 3351569
  19. Direction-selective cells in complex family in cat striate cortex.
    J Neurophysiol. 1980 May;43(5):1266-83 PMID: 7373366
  20. Form, function and intracortical projections of spiny neurones in the striate visual cortex of the cat.
    J Physiol. 1984 Aug;353:463-504 PMID: 6481629
  21. The afferent connections and laminar distribution of cells in the cat striate cortex.
    J Comp Neurol. 1979 Oct 15;187(4):725-44 PMID: 489798
  22. Orientation selectivity of synaptic potentials in neurons of cat primary visual cortex.
    J Neurosci. 1986 May;6(5):1284-301 PMID: 3711980
  23. 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
  24. Morphology and intracortical projections of functionally characterised neurones in the cat visual cortex.
    Nature. 1979 Jul 12;280(5718):120-5 PMID: 552600
  25. The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat.
    J Physiol. 1975 Sep;250(2):305-29 PMID: 1177144
  26. Two inhibitory postsynaptic potentials, and GABAA and GABAB receptor-mediated responses in neocortex of rat and cat.
    J Physiol. 1988 Dec;406:443-68 PMID: 2855437
  27. Comparison of the action of baclofen with gamma-aminobutyric acid on rat hippocampal pyramidal cells in vitro.
    J Physiol. 1985 Mar;360:161-85 PMID: 3989713
  28. Ordinal position of neurons in cat striate cortex.
    J Neurophysiol. 1979 Sep;42(5):1251-63 PMID: 226663
  29. Synaptic targets of HRP-filled layer III pyramidal cells in the cat striate cortex.
    Exp Brain Res. 1986;64(3):541-52 PMID: 3803491
  30. Quantitative distribution of GABA-immunoreactive neurons in the visual cortex (area 17) of the cat.
    Exp Brain Res. 1986;61(2):323-31 PMID: 3005016
  31. Physiological, morphological, and cytochemical characteristics of a layer 1 neuron in cat striate cortex.
    J Comp Neurol. 1989 Apr 15;282(3):404-14 PMID: 2715389
  32. Receptive field organization of simple cells in cat striate cortex.
    Exp Brain Res. 1981;42(1):89-98 PMID: 7215513
  33. Origin of orientation-selective EPSPs in simple cells of cat visual cortex.
    J Neurosci. 1987 Jun;7(6):1780-91 PMID: 3598648
  34. Selective responses of visual cortical cells do not depend on shunting inhibition.
    Nature. 1988 Apr 14;332(6165):642-4 PMID: 3357519
  35. Innervation of cat visual areas 17 and 18 by physiologically identified X- and Y- type thalamic afferents. II. Identification of postsynaptic targets by GABA immunocytochemistry and Golgi impregnation.
    J Comp Neurol. 1985 Dec 8;242(2):275-91 PMID: 2418072
  36. Response to movement of neurons in areas 17 and 18 of the cat: direction selectivity.
    J Neurophysiol. 1981 Jun;45(6):1059-73 PMID: 7252530
  37. Connections between pyramidal neurons in layer 5 of cat visual cortex (area 17).
    J Comp Neurol. 1987 May 15;259(3):364-81 PMID: 3584561
  38. Glutamate decarboxylase-immunoreactive terminals of Golgi-impregnated axoaxonic cells and of presumed basket cells in synaptic contact with pyramidal neurons of the cat's visual cortex.
    J Comp Neurol. 1983 Dec 10;221(3):263-78 PMID: 6655085
  39. Synaptic connections of intracellularly filled clutch cells: a type of small basket cell in the visual cortex of the cat.
    J Comp Neurol. 1985 Nov 8;241(2):111-37 PMID: 4067011
  40. Projection patterns of individual X- and Y-cell axons from the lateral geniculate nucleus to cortical area 17 in the cat.
    J Comp Neurol. 1985 Mar 8;233(2):159-89 PMID: 3973100
  41. Evidence that the different classes of relay cells of the cat's lateral geniculate nucleus terminate in different layers of the striate cortex.
    Exp Brain Res. 1979 Oct;37(2):349-72 PMID: 499392
  42. An intracellular analysis of the visual responses of neurones in cat visual cortex.
    J Physiol. 1991;440:659-96 PMID: 1804981
  43. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex.
    J Physiol. 1962 Jan;160:106-54 PMID: 14449617
  44. A theoretical analysis of electrical properties of spines.
    Proc R Soc Lond B Biol Sci. 1983 Jul 22;218(1213):455-77 PMID: 6136978
  45. Cortical intracellular potentials in response to stimulation to lateral geniculate body.
    J Neurophysiol. 1960 Nov;23:592-601 PMID: 13761815
  46. The action of glycine on cortical neurones.
    Exp Brain Res. 1969;9(2):155-63 PMID: 4310329
  47. Direction selectivity of complex cells in a comparison with simple cells.
    J Neurophysiol. 1975 Nov;38(6):1524-40 PMID: 1221087
  48. Conduction velocity of afferents to cat visual cortex: a correlation with cortical receptive field properties.
    Brain Res. 1971 Sep 24;32(2):460-6 PMID: 5134590
  49. Physiological and morphological properties of identified basket cells in the cat's visual cortex.
    Exp Brain Res. 1983;50(2-3):193-200 PMID: 6641854
  50. Mechanisms of inhibition in cat visual cortex.
    J Physiol. 1991;440:697-722 PMID: 1804983
  51. A simple algorithm for solving the cable equation in dendritic trees of arbitrary geometry.
    J Neurosci Methods. 1985 Feb;12(4):303-15 PMID: 3838780
  52. Receptive fields of single neurones in the cat's striate cortex.
    J Physiol. 1959 Oct;148:574-91 PMID: 14403679
  53. Evidence for interlaminar inhibitory circuits in the striate cortex of the cat.
    J Comp Neurol. 1987 Jun 1;260(1):1-19 PMID: 3597830
  54. Cortical intracellular synaptic potentials and direct cortical stimulation.
    J Cell Comp Physiol. 1962 Aug;60:1-16 PMID: 14464979
  55. A reassessment of the forms of nonpyramidal neurons in area 17 of cat visual cortex.
    J Comp Neurol. 1981 Dec 20;203(4):685-716 PMID: 7035507
  56. Mechanism of directional selectivity in simple neurons of the cat's visual cortex analyzed with stationary flash sequences.
    J Neurophysiol. 1984 Feb;51(2):294-324 PMID: 6707723
  57. Transient response in a dendritic neuron model for current injected at one branch.
    Biophys J. 1974 Oct;14(10):759-90 PMID: 4424185
  58. Immunogold demonstration of GABA in synaptic terminals of intracellularly recorded, horseradish peroxidase-filled basket cells and clutch cells in the cat's visual cortex.
    Neuroscience. 1986 Dec;19(4):1051-65 PMID: 3029623
  59. Synaptic connections of morphologically identified and physiologically characterized large basket cells in the striate cortex of cat.
    Neuroscience. 1983 Oct;10(2):261-94 PMID: 6633861
  60. Electrophysiological properties of neocortical neurons in vitro.
    J Neurophysiol. 1982 Dec;48(6):1302-20 PMID: 6296328
  61. Patterns of synaptic input to layer 4 of cat striate cortex.
    J Neurosci. 1984 Dec;4(12):3021-33 PMID: 6502220
  62. The basic uniformity in structure of the neocortex.
    Brain. 1980 Jun;103(2):221-44 PMID: 6772266
  63. The Wellcome Prize lecture. From single cells to simple circuits in the cerebral cortex.
    Q J Exp Physiol. 1988 Sep;73(5):637-702 PMID: 3068702
  64. Spatially opponent excitation and inhibition in simple cells of the cat visual cortex.
    J Neurosci. 1988 Apr;8(4):1172-80 PMID: 3357015
Article Info
Journal
The Journal of physiology
Abbr.
J Physiol
ISSN
0022-3751
Published
1991-00-00
Pages
735-69
Language
English
Region
England
NLM ID
0266262
PMCID
PMC1180177
Subset
IM
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