Skip to main content
SpringerLink
Log in

Firing rhythmicity in the neocortex in vivo and in vitro under sustained iontophoretic excitation

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

Extracellular recordings were made from the cat intact neocortex and guinea-pig neocortical slices during microiontophoretic application of amino acid neurotransmitters. Spike train autocorrelation analysis showed a high stability of firing patterns in the intact neocortex. When excitation of a cell was increased in a step-wise manner with glutamate iontophoresis only an enhancement of the rate of firing was observed. The rhythmic component, which was mainly due to periodic multiple discharges, remained up to the highest firing frequencies. In contrast to the in vivo observation, glutamate, aspartate or K+ iontophoresis in cortical slices resulted in firing pattern alternations (always from bursts or irregular activity to regular spike firing) as well as an increase in firing rate. In slices the periodic component was typically due to single-spike regularity and its frequency rose with an increase of firing rate. The comparison of autocorrelogram alternations in vivo and in vitro suggests that the temporal organization of spike trains in the intact cortex is under tight external control and is defined mainly by neuronal interactions, whereas virtually all the neurons in vitro are very sensitive to the same iontophoretic influences and their individual outputs easily change according to the excitation (depolarization) level. The coincidence of the lowest frequencies of single-spike regularity in the in vitro preparation (5–7 Hz and 8–10 Hz) with theta- and alpha-rhythms in the electroencephalogram (EEG), and with single unit firing rhythmicity in the whole brain, may represent the basis of a unit-circuit resonance and provide a high stability of these EEG-rhythms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

ACF :

autocorrelation function

BFA :

background firing activity

EEG :

electroencephalogram

References

  • Agmon A, Connors BW (1989) Repetitive burst-firing neurons in the deep layers of mouse somatosensory cortex. Neurosci Lett 99: 137–141

    Google Scholar 

  • Agopyan N, Avoli M (1988) Synaptic and non-synaptic mechanism underlying low calcium bursts in the in vitro hippocampal slice. Exp Brain Res 73: 533–540

    Google Scholar 

  • Ahissar E, Vaada E (1990) Oscillatory activity of single unit in a somatosensory cortex of an awake monkey and their possible role in texture analysis. Proc Natl Acad Sci USA 87: 8935–8939

    Google Scholar 

  • Armstrong-James M, Fox K (1983) Effects of ionophoresed noradrenaline on the spontaneous activity of neurons in rat Sm1 cortex. J Physiol Lond 335: 427–447

    Google Scholar 

  • Armstrong-James M, Caan AW, Fox K (1985) Threshold effect of N-methyl-D-asparate (NMDA) and 2-amino-5-phosphonovaleric acid (2-APV) on the spontaneous activity of neocortical single neurones in the urethane anesthetized rat. Exp Brain Res 60: 209–213

    Google Scholar 

  • Ball GJ, Gloor P, Thompson CJ (1977) Computed unit-EEG correlation and laminar profiles of spindle waves in the electroencephalogram of cat. EEG and Clin Neurophysiol 43: 330–345

    Google Scholar 

  • Buzsaki G (1991) The thalamic clock: emergent network properties. Neuroscience 41: 351–364

    Google Scholar 

  • Chagnac-Amitai Y, Connors BW (1989) Synchronized excitation and inhibition driven by intrinsically bursting neurons in neocortex. J Neurophysiol 62: 1149–1162

    Google Scholar 

  • Chagnac-Amitai Y, Luhmann HJ, Prince DA (1990) Burst generating and regular spiking layer 5 pyramidal neurons of rat neocortex have different morphological features. J Comp Neurol 296: 598–613

    Google Scholar 

  • Connors BW, Gutnick MJ (1990) Intrinsic firing patterns of diverse neocortical neurones. Trends Neurosci 13: 99–104

    Google Scholar 

  • Connors BW, Gutnick MJ and Prince DA (1982) Electrophysiological properties of neocortical neurones in vitro. J Neurophysiol 48: 1302–1320

    Google Scholar 

  • Corner MA, Mirmiran M (1990) Spontaneous neuronal firing patterns in the occipital cortex of developing rats. Int J Devel Neurosci 8: 309–316

    Google Scholar 

  • Creutzfeldt O, Houchin J (1974) Neuronal basis of EEG waves. In: Handbook of electroencephalography and clinical neurophysiology, vol 2 (part c, sect 1). Elsiever, Amsterdam, pp 2C5–2C54

    Google Scholar 

  • Creutzfeldt OD, Watanade S, Lux HD (1966) Relation between EEG phenomena and potentials of single cortical cells. II. Spontaneous and convulsoid activity. EEG and Clin Neurophysiol 20: 19–37

    Google Scholar 

  • Eckhorn R, Obermuller A (1993) Single neurons are differently involved in stimulus-specific oscillations in cat visual cortex. Exp Brain Res 95: 177–182

    Google Scholar 

  • Eckhorn R, Baner R, Jordon W, Brosch M, Kruse W, Munk M, Reinboeck HJ (1988) Coherent oscillations: a mechanism of feature linking in the arosal cortex? Biol Cybern 60: 121–130

    Google Scholar 

  • Giaretta D, Avoli M, Gloor P (1987) Intracellular recordings in pericruciate neurons during spike and wave discharges of feline generalized penicillin epilepsy. Brain Res 405: 68–79

    Google Scholar 

  • Gilbey MP, Wooster MJ (1979) Mono and multi-synaptic origin of the early surface-negative wave recorded from guinea-pig olfactory cortex in vitro. J Physiol Lond 293: 153–172

    Google Scholar 

  • Gray CM, Konig P, Engel AK, Singer W (1989) Oscillatory responses on cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338: 334–337

    Google Scholar 

  • Gruneis F, Nakao M, Jamamoto M, Musha T, Nakahama H (1989) An interpretation of I/f fluctuations in neuronal spike trains during dreamsleep. Biol Cyberns 60: 161–169

    Google Scholar 

  • Gutnick MJ, Connors BW, Prince DA (1982) Mechanisms of neocortical epileptogenesis in vitro. J Neurophysiol 48: 1321–1335

    Google Scholar 

  • Jones RSG, Heinemann U (1989) Spontaneous activity mediated by NMDA receptors in immature rat entorhinal cortex in vitro. Neurosci Lett 104: 93–98

    Google Scholar 

  • Karnup SV (1978) Correlation of the surface and deep cortical potentials with the unit activity at an orienting reflex. Sechenov Physiol J USSR 64: 1475–1478 (in Russian)

    Google Scholar 

  • Karnup SV (1980) Comparative analysis of statistical dependence forms between background spike activity of cortical neurons and EEG in different functional states of the brain. Jhurnal Vyssh Nervn Deyat 30: 105–112 (in Russian)

    Google Scholar 

  • Karnup SV (1992) Background firing activity in guinea-pig neocortex in vitro. Neuroscience 48: 915–924

    Google Scholar 

  • Karnup SV, Zhadin MN (1980) Autocorrelation analysis of spontaneous discharges of cortical neurons during learning. Jhurnal Vyssh Nervn Deyat 30: 738–745 (in Russian)/(1983) Neurosci Behav Physiol 13: 55–62 (in English)

    Google Scholar 

  • Kavaguchi Y (1993) Grouping of nonpyramidal and pyramidal cells with specific physiological and morphological characteristics in rat frontal cortex. J Neurophysiol 69: 416–431

    Google Scholar 

  • Klink R, Alonso A (1993) Ionic mechanisms for the subthreshold oscillations and differential electroresponsiveness of medial entorhinal cortex layer II neurons. J Neurophysiol 70: 144–157

    Google Scholar 

  • Koch UT, Bassler U, Brunner M (1989) Non-spiking neurons suppress fluctuations in small networks. Biol Cybern 62: 75–81

    Google Scholar 

  • Llinas RR (1988) The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. Science 242: 1654–1664

    Google Scholar 

  • Llinás RR, Grace AA, Yarom J (1991) In vitro neurons in mammalian cortical layer 4 exhibit intrinsic oscillatory activity in the 10- to 50-Hz frequency range. Proc Natl Acad Sci USA 88: 897–901

    Google Scholar 

  • Lopes-da-Silva F (1991) Neural mechanisms underlying brain waves: from neuronal membranes to networks. EEG Clin Neurophysiol 79: 81–93

    Google Scholar 

  • Mason A, Larkman A (1990) Correlation between morphology and electrophysiology of pyramidal neurons in series of rat visual cortex. II. Electrophysiology. J Neurosci 10: 1415–1428

    Google Scholar 

  • McCormick DA, Connors BW, Lighthall JW, Prince DA (1985) Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol 54: 782–806

    Google Scholar 

  • Neuman RS, Cherubini E, Ben-Ari Y (1989) Endogenous and network bursts induced by N-methyl-D-aspartate and magnesium free medium in the CA3 region of the hippocampal slice. Neuroscience 28: 393–399

    Google Scholar 

  • Schneidermann JH (1986) Low concentrations of penicillin reveal rhythmic, synchronous synaptic potentials in hippocampal slice. Brain Res 398: 231–241

    Google Scholar 

  • Schuster HG, Wagner P (1990) A model for neuronal oscillations in the visual cortex. 1. Mean-field theory and derivations of the phase equations. Biol Cybern 64: 77–82

    Google Scholar 

  • Silva LR, Amitai Y, Connors BW (1991) Intrinsic oscillations of neocortex generated by layer 5 pyramidal neurons. Science 251: 432–435

    Google Scholar 

  • Singer W (1993) Synchronization of cortical activity and its putative role on information processing and learning. Annu Rev Physiol 55: 349–374

    Google Scholar 

  • Steriade M, Dossi RC, Nunez A (1991) Network modulation of a slow intrinsic oscillation of cat thalamocortical neurons implicated in sleep delta waves: cortically-induced synchronization and brainstem cholinergic suppression. J Neurosci 11: 3200–3217

    Google Scholar 

  • Steriade M, Nunez A, Amzica F (1993) Intracellular analysis of relations between the slow (< 1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. J Neurocsi 13: 3266–3283

    Google Scholar 

  • Szentagothai J (1978) The neuron network of the cerebral cortex: A functional interpretation. Proc R Soc Lond B 201: 219–248

    Google Scholar 

  • Traub RD, Miles R, Wong RKS, Schulman LS, Schneiderman JH (1987) Models of synchronized bursts in the presence of inhibition, II. Ongoing spontaneous population events. J Neurophysiol 58: 752–764

    Google Scholar 

  • Tasu Y, Chen P-X (1989) Normalized power spectrum density function analysis on spike trains. II. Rhythms of unit activities in the somatosensory cortex of cats. Int J Neurosci 49: 123–131

    Google Scholar 

  • Vinogradova OS, Brazhnik ES, Stafekhina VS, Kitchigina VF (1993) Acetylcholine, theta-rhythm and activity of hippocampal neurons in the rabbit-II. Septal input. Neuroscience. 53: 971–979

    Google Scholar 

  • Zhadin MN (1984) In: Supin AJ (ed) Biophysical meachanisms of the electroencephalogram forming. Nauka, Moscow (in Russian)

    Google Scholar 

Download references

Author information

Author notes

  1. S. V. Karnup

    Present address: SUNY Health Science Center at Brooklyn, 450 Clarkson Ave., Box 29, 11203, Brooklyn, NY, USA

Authors and Affiliations

  1. Institute of Theoretical and Experimental Biophysics, 142292, Pushchino, Russia

    S. V. Karnup

Authors
  1. S. V. Karnup
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Karnup, S.V. Firing rhythmicity in the neocortex in vivo and in vitro under sustained iontophoretic excitation. J Comp Physiol A 178, 63–74 (1996). https://doi.org/10.1007/BF00189591

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00189591

Key words

Search

Navigation