Home LiteratureArticle Details
PMID: 15930382 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, P.H.S.

Stimulus-dependent gamma (30-50 Hz) oscillations in simple and complex fast rhythmic bursting cells in primary visual cortex.

Cardin JA, Palmer LA, Contreras D

Abstract

Oscillatory activity is generated by many neural systems. gamma band (approximately 40 Hz) oscillations in the thalamus and cortex occur spontaneously and in response to sensory stimuli. Fast rhythmic bursting (FRB) cells (also called chattering cells) comprise a unique class of cortical neurons that, during depolarization by current injection, intrinsically generate bursts of high-frequency action potentials with an interburst frequency between 30 and 50 Hz. In the present study, we show for the first time that FRB cells in the primary visual cortex can be either simple or complex and are distributed throughout all cortical layers. Strikingly, both simple and complex FRB cells generate spike bursts at gamma frequencies in response to depolarizing current pulses, but only simple FRB cells exhibit a selective, stimulus feature-dependent increase in gamma oscillations in response to visual stimulation. In addition, we find that hyperpolarization does not reduce the relative power of visually evoked gamma oscillations in the V(m) response of FRB cells. Our results thus indicate that visually evoked gamma activity in individual simple and complex FRB cells is generated in large part by rhythmic synaptic input, rather than by depolarization-dependent activation of intrinsic properties. Finally, the presence of FRB cells in layer 6 suggests a role for corticothalamic feedback in potentiating thalamic oscillations and facilitating the generation of a corticothalamocortical oscillatory loop. We propose that rather than functioning as pacemakers, FRB cells amplify and distribute stimulus-driven gamma oscillations in the neocortex.

MeSH Terms
Action Potentials Animals Cats Evoked Potentials, Visual Periodicity Photic Stimulation Visual Cortex/cytology,physiology
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Cardin Jessica A
Department of Neuroscience, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19106-6074, USA.
Palmer Larry A
Contreras Diego
References (62)
62 references, click to expand
  1. Single-column thalamocortical network model exhibiting gamma oscillations, sleep spindles, and epileptogenic bursts.
    J Neurophysiol. 2005 Apr;93(4):2194-232 PMID: 15525801
  2. Intrinsic firing patterns of diverse neocortical neurons.
    Trends Neurosci. 1990 Mar;13(3):99-104 PMID: 1691879
  3. Neocortical cell classes are flexible entities.
    Nat Rev Neurosci. 2004 Feb;5(2):121-34 PMID: 14735115
  4. Gamma frequency-range abnormalities to auditory stimulation in schizophrenia.
    Arch Gen Psychiatry. 1999 Nov;56(11):1001-5 PMID: 10565499
  5. Resonance, oscillation and the intrinsic frequency preferences of neurons.
    Trends Neurosci. 2000 May;23(5):216-22 PMID: 10782127
  6. Ionic mechanisms underlying repetitive high-frequency burst firing in supragranular cortical neurons.
    J Neurosci. 2000 Jul 1;20(13):4829-43 PMID: 10864940
  7. Synaptic interactions between thalamic inputs to simple cells in cat visual cortex.
    J Neurosci. 2000 Jul 15;20(14):5461-7 PMID: 10884329
  8. Diversity and dynamics of dendritic signaling.
    Science. 2000 Oct 27;290(5492):739-44 PMID: 11052929
  9. Oscillatory gamma activity in humans: a possible role for object representation.
    Int J Psychophysiol. 2000 Dec 1;38(3):211-23 PMID: 11102663
  10. Rules of connectivity between geniculate cells and simple cells in cat primary visual cortex.
    J Neurosci. 2001 Jun 1;21(11):4002-15 PMID: 11356887
  11. Construction of complex receptive fields in cat primary visual cortex.
    Neuron. 2001 Nov 8;32(3):515-25 PMID: 11709161
  12. Synaptic physiology and receptive field structure in the early visual pathway of the cat.
    Cereb Cortex. 2003 Jan;13(1):63-9 PMID: 12466216
  13. The spatial receptive field of thalamic inputs to single cortical simple cells revealed by the interaction of visual and electrical stimulation.
    Proc Natl Acad Sci U S A. 2002 Dec 10;99(25):16261-6 PMID: 12461179
  14. Electrophysiological classes of cat primary visual cortical neurons in vivo as revealed by quantitative analyses.
    J Neurophysiol. 2003 Mar;89(3):1541-66 PMID: 12626627
  15. A role for fast rhythmic bursting neurons in cortical gamma oscillations in vitro.
    Proc Natl Acad Sci U S A. 2004 May 4;101(18):7152-7 PMID: 15103017
  16. The action of antidromic impulses on the cerebellar Purkinje cells.
    J Physiol. 1966 Jan;182(2):316-45 PMID: 5942032
  17. Dynamic characteristics of visual evoked potentials in the dog. II. Beta frequency selectivity in evoked potentials and background activity.
    Electroencephalogr Clin Neurophysiol. 1970 Sep;29(3):260-8 PMID: 4195648
  18. Correlation analysis of units recorded in the cat dorsal lateral geniculate nucleus.
    Exp Brain Res. 1975 Dec 22;24(2):111-30 PMID: 1218547
  19. Spatial summation in the receptive fields of simple cells in the cat's striate cortex.
    J Physiol. 1978 Oct;283:53-77 PMID: 722589
  20. Fast fronto-parietal rhythms during combined focused attentive behaviour and immobility in cat: cortical and thalamic localizations.
    Electroencephalogr Clin Neurophysiol. 1981 Mar;51(3):244-52 PMID: 6163613
  21. In vitro neurons in mammalian cortical layer 4 exhibit intrinsic oscillatory activity in the 10- to 50-Hz frequency range.
    Proc Natl Acad Sci U S A. 1991 Feb 1;88(3):897-901 PMID: 1992481
  22. Fast oscillations (20-40 Hz) in thalamocortical systems and their potentiation by mesopontine cholinergic nuclei in the cat.
    Proc Natl Acad Sci U S A. 1991 May 15;88(10):4396-400 PMID: 2034679
  23. Classifying simple and complex cells on the basis of response modulation.
    Vision Res. 1991;31(7-8):1079-86 PMID: 1909826
  24. Human auditory evoked gamma-band magnetic fields.
    Proc Natl Acad Sci U S A. 1991 Oct 15;88(20):8996-9000 PMID: 1924362
  25. Magnetic field tomography of coherent thalamocortical 40-Hz oscillations in humans.
    Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11037-41 PMID: 1763020
  26. Coherent 25- to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys.
    Proc Natl Acad Sci U S A. 1992 Jun 15;89(12):5670-4 PMID: 1608977
  27. Visually evoked oscillations of membrane potential in cells of cat visual cortex.
    Science. 1992 Jul 24;257(5069):552-4 PMID: 1636094
  28. Voltage-dependent fast (20-40 Hz) oscillations in long-axoned neocortical neurons.
    Neuroscience. 1992 Nov;51(1):7-10 PMID: 1465188
  29. Voltage-dependent 40-Hz oscillations in rat reticular thalamic neurons in vivo.
    Neuroscience. 1992 Nov;51(2):245-58 PMID: 1465191
  30. Oscillatory discharge in the visual system: does it have a functional role?
    J Neurophysiol. 1992 Nov;68(5):1558-74 PMID: 1479430
  31. Electrophysiological properties of intralaminar thalamocortical cells discharging rhythmic (approximately 40 HZ) spike-bursts at approximately 1000 HZ during waking and rapid eye movement sleep.
    Neuroscience. 1993 Sep;56(1):1-9 PMID: 8232908
  32. Mechanisms of oscillatory activity in guinea-pig nucleus reticularis thalami in vitro: a mammalian pacemaker.
    J Physiol. 1993 Aug;468:669-91 PMID: 8254530
  33. Electrophysiological properties of cat reticular thalamic neurones in vivo.
    J Physiol. 1993 Oct;470:273-94 PMID: 8308730
  34. Human oscillatory brain activity near 40 Hz coexists with cognitive temporal binding.
    Proc Natl Acad Sci U S A. 1994 Nov 22;91(24):11748-51 PMID: 7972135
  35. Relation between oscillatory activity and long-range synchronization in cat visual cortex.
    Proc Natl Acad Sci U S A. 1995 Jan 3;92(1):290-4 PMID: 7816836
  36. Visual feature integration and the temporal correlation hypothesis.
    Annu Rev Neurosci. 1995;18:555-86 PMID: 7605074
  37. Synchronization of fast (30-40 Hz) spontaneous cortical rhythms during brain activation.
    J Neurosci. 1996 Jan;16(1):392-417 PMID: 8613806
  38. Long-range synchronization of oscillatory light responses in the cat retina and lateral geniculate nucleus.
    Nature. 1996 Feb 22;379(6567):728-32 PMID: 8602219
  39. Intracortical and corticothalamic coherency of fast spontaneous oscillations.
    Proc Natl Acad Sci U S A. 1996 Mar 19;93(6):2533-8 PMID: 8637909
  40. Stimulus specificity of phase-locked and non-phase-locked 40 Hz visual responses in human.
    J Neurosci. 1996 Jul 1;16(13):4240-9 PMID: 8753885
  41. Excitatory synaptic inputs to spiny stellate cells in cat visual cortex.
    Nature. 1996 Jul 18;382(6588):258-61 PMID: 8717041
  42. Chattering cells: superficial pyramidal neurons contributing to the generation of synchronous oscillations in the visual cortex.
    Science. 1996 Oct 4;274(5284):109-13 PMID: 8810245
  43. Odour encoding by temporal sequences of firing in oscillating neural assemblies.
    Nature. 1996 Nov 14;384(6605):162-6 PMID: 8906790
  44. Dendritic calcium conductances generate high-frequency oscillation in thalamocortical neurons.
    Proc Natl Acad Sci U S A. 1997 Jan 21;94(2):724-8 PMID: 9012852
  45. Sensory-evoked high-frequency (gamma-band) oscillating potentials in somatosensory cortex of the unanesthetized rat.
    Brain Res. 1997 Sep 12;768(1-2):167-76 PMID: 9369313
  46. Dynamic properties of corticothalamic neurons and local cortical interneurons generating fast rhythmic (30-40 Hz) spike bursts.
    J Neurophysiol. 1998 Jan;79(1):483-90 PMID: 9425218
  47. Synchronization of visual responses between the cortex, lateral geniculate nucleus, and retina in the anesthetized cat.
    J Neurosci. 1998 Aug 15;18(16):6395-410 PMID: 9698331
  48. Mechanisms underlying burst and regular spiking evoked by dendritic depolarization in layer 5 cortical pyramidal neurons.
    J Neurophysiol. 1999 Mar;81(3):1341-54 PMID: 10085360
  49. Functional connectivity between simple cells and complex cells in cat striate cortex.
    Nat Neurosci. 1998 Sep;1(5):395-403 PMID: 10196530
  50. Cerebral and cerebellar potentials.
    Physiol Rev. 1958 Jul;38(3):357-88 PMID: 13567040
  51. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex.
    J Physiol. 1962 Jan;160:106-54 PMID: 14449617
  52. STATISTICAL ANALYSIS OF THE DARK DISCHARGE OF LATERAL GENICULATE NEURONES.
    J Physiol. 1964 Apr;170:598-612 PMID: 14165698
  53. Persistent gamma oscillations in superficial layers of rat auditory neocortex: experiment and model.
    J Physiol. 2005 Jan 1;562(Pt 1):3-8 PMID: 15489250
  54. Receptive-field structure in cat striate cortex.
    J Neurophysiol. 1981 Aug;46(2):260-76 PMID: 6267213
  55. Electrophysiological properties of neocortical neurons in vitro.
    J Neurophysiol. 1982 Dec;48(6):1302-20 PMID: 6296328
  56. Statistical features of impulse trains in cat's lateral geniculate neurons.
    Biol Cybern. 1984;50(3):167-72 PMID: 6466733
  57. 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
  58. Spatial patterns of visual cortical fast EEG during conditioned reflex in a rhesus monkey.
    Brain Res. 1987 Oct 6;422(2):267-76 PMID: 3676788
  59. Spatially opponent excitation and inhibition in simple cells of the cat visual cortex.
    J Neurosci. 1988 Apr;8(4):1172-80 PMID: 3357015
  60. The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function.
    Science. 1988 Dec 23;242(4886):1654-64 PMID: 3059497
  61. Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex.
    Proc Natl Acad Sci U S A. 1989 Mar;86(5):1698-702 PMID: 2922407
  62. A model of thalamocortical relay cells.
    J Physiol. 2005 Jun 15;565(Pt 3):765-81 PMID: 15613378
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2005-06-01
Pages
5339-50
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC3034157
Subset
IM
Grants
NIMH NIH HHS · P50 MH064045 · United States
NIMH NIH HHS · P50 MH064045-10 · United States
NEI NIH HHS · R01 EY016430-02 · United States
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: [email protected]