Skip to main content
SpringerLink
Log in

Analysis of State-Dependent Transitions in Frequency and Long-Distance Coordination in a Model Oscillatory Cortical Circuit

  • Published:
Journal of Computational Neuroscience Aims and scope Submit manuscript

Abstract

Changes in behavioral state are typically accompanied by changes in the frequency and spatial coordination of rhythmic activity in the neocortex. In this article, we analyze the effects of neuromodulation on ionic conductances in an oscillating cortical circuit model. The model consists of synaptically-coupled excitatory and inhibitory neurons and supports rhythmic activity in the alpha, beta, and gamma ranges. We find that the effects of neuromodulation on ionic conductances are, by themselves, sufficient to induce transitions between synchronous gamma and beta rhythms and asynchronous alpha rhythms. Moreover, these changes are consistent with changes in behavioral state, with the rhythm transitioning from the slower alpha to the faster gamma and beta as arousal increases. We also observe that it is the same set of underlying intrinsic and network mechanisms that appear to be simultaneously responsible for both the observed transitions between the rhythm types and between their synchronization properties. Spike time response curves (STRCs) are used to study the relationship between the transitions in rhythm and the underlying biophysics.

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

References

  • Acker CD, White JA, Kopell N (2002) Synchronization of strongly coupled excitatory neurons: Relating network behavior to biophysics. J. Comput. Neurosci. (submitted).

  • Bibbig A, Faulkner HJ, Whittington MA, Traub RD (2001) Selforganized synaptic plasticity contributes to the shaping of gamma and beta oscillations in vitro. J. Neurosci. 21(22): 9053-9067.

    PubMed  Google Scholar 

  • Buzsaki G, Bickford RG, Ponomareff G, Thal LJ, Mandel RJ, Gage FH (1988) Nucleus basalis and thalamic control of neocortical activity in the freely moving rat. J. Neurosci. 8(11): 4007-4026.

    PubMed  Google Scholar 

  • Cape EG, Jones BE (1998) Differential modulation of high-frequency ?-electroencephalogram activity and sleep-wake state by noradrenaline and serotonin microinjections into the region of cholinergic basalis neurons. J. Neurosci. 18(7): 2653-2666.

    PubMed  Google Scholar 

  • Cape EG, Jones BE (2000) Effects of glutamate agonist versus procaine microinjections into the basal forebrain cholinergic cell area upon gamma and theta EEG activity and sleep-wake state. Eur. J. Neurosci. 12: 2166-2184.

    Article  PubMed  Google Scholar 

  • Castro-Alamancos MA, Connors BW (1996a) Short-term plasticity of a thalamocortical pathway dynamically modulated by behavioral state. Science 272: 274-277.

    PubMed  Google Scholar 

  • Castro-Alamancos MA, Connors BW (1996b) Cellular mechanisms of the augmenting response: Short-term plasticity in a thalamocortical pathway. J. Neurosci. 16(23): 7742-7756.

    PubMed  Google Scholar 

  • Celesia GG, Jasper HH (1966) Acetylcholine released from cerebral cortex in relation to state of activation. Neurologist 16: 1053-1064.

    Google Scholar 

  • Chow CC, White JA, Ritt J, Kopell N (1998) Frequency control in synchronized networks of inhibitory neurons. J. Comput. Neurosci. 5: 407-420.

    Article  PubMed  Google Scholar 

  • Connors BW, Amitai Y (1997) Making waves in the neocortex. Neuron 18: 347-349.

    Article  PubMed  Google Scholar 

  • da Silva LF (1991) Neural mechanisms underlying brain waves: From neural membranes to networks. Electroenceph. Clin. Neurophysiol. 79: 81-93.

    Article  PubMed  Google Scholar 

  • De La Pena E, Geijo-Barrientos E (1996) Laminar localization, morphlogy, and physiological properties of pyramidal neurons that have low-threshold calcium current in the guinea-pig medial frontal cortex. J. Neurosci. 16: 5301-5311.

    PubMed  Google Scholar 

  • Destexhe A, Babloyantz A, Sejnowski TJ (1993) Ionic mechanisms for intrinsic slow oscillations in thalamic relay neurons. Biophys. J. 65: 1538-1552.

    PubMed  Google Scholar 

  • Destexhe A, Bal T, McCormick D, Sejnowski TJ (1996) Ionic mechanisms underlying synchronized oscillations and propagating waves in a model of ferret thalamic slices. J. Neurophysiol. 76: 2049-2070.

    PubMed  Google Scholar 

  • Destexhe A, Mainen ZF, Sejnowski TJ (1998) Kinetic models of synaptic transmission. In: C. Koch, I. Segev, eds. Methods in Neuronal Modeling, 2nd ed. MIT Press, Cambridge.

    Google Scholar 

  • Detari L, Rasmusson DD, Semba K (1999) The role of basal forebrain neurons in tonic and phasic activation of the cerebral cortex. Prog. Neurobiol. 58: 249-277.

    Article  PubMed  Google Scholar 

  • Devaney RL (1992) A First Course in Chaotic Dynamical Systems: Theory and Experiment. Addison-Wesley, Reading, MA.

    Google Scholar 

  • Dringenberg HC, Vanderwolf CH (1997) Neocortical activation: Modulation by multiple pathways acting on central cholinergic and serotonergic systems. Exp. Brain Res. 116: 160-174.

    PubMed  Google Scholar 

  • Ermentrout GB, Kopell N (1998) Fine structure of neural spiking and synchronization in the presence of conduction delays. PNAS 95: 1259-1264.

    Article  PubMed  Google Scholar 

  • Fanselow EE, Nicolelis MAL (1999) Behavioral modulation of tactile responses in the rat somatosensory system. J. Neurosci. 19: 7603-7616.

    PubMed  Google Scholar 

  • Farmer SF (1998) Rhythmicity, synchronization and binding in human and primate motor systems. J. Physiol. 509(1): 3-14.

    Article  PubMed  Google Scholar 

  • Fuchs EC, Doheny H, Faulkner H, Caputi A, Traub RD, Bibbig A, Kopell N, Whittington MA, Monyer H (2000) Genetically altered AMPA-type glutamate receptor kinetics in interneurons disrupt long-range synchrony of gamma oscillation. PNAS 96(6): 3571-3576.

    Google Scholar 

  • Gray CM, McCormick DA (1996) Chattering cells: Superficial pyramidal neurons contributing to the generation of synchronous oscillations in the visual cortex. Science 274(5284): 109-113.

    Article  PubMed  Google Scholar 

  • Haenschel C, Baldeweg T, Croft RJ, Whittington M, Gruzelier J (2000) Gamma and beta frequency oscillations in response to novel auditory stimuli: A comparison of human electroencephalogram (EEG) data with in vitro models. PNAS 97: 7645-7650.

    Article  PubMed  Google Scholar 

  • Hasselmo ME (1995) Neuromodulation and cortical function: Modeling the physiological basis of behavior. Behav. Brain Res. 67: 1-27.

    Article  PubMed  Google Scholar 

  • Jones SR, Pinto DJ, Kaper TJ, Kopell N (2000) Alpha-frequency rhythms desynchronize over long cortical distances: A modeling study. J. Comput. Neurosci. 9: 271-291.

    Article  PubMed  Google Scholar 

  • Karbowski J, Kopell N (2000) Multispikes and synchronization in a large neural network with temporal delays. Neural Comp. 12: 1573-1606.

    Article  Google Scholar 

  • Keil A, Gruber T, Muller MM (2001) Functional correlates of macroscopic high-frequency brain activity in the human visual system. Neurosci. and Biobehavioral Rev. 25: 527-534.

    Article  Google Scholar 

  • Kisvarday ZF, Kim DS, Eysel UT, Bonhoeffer T (1994) Relationship between lateral inhibitory connections and the topography of the orientation map in cat visual corex. Eur. J. Neurosci. 6(10): 1619-1632.

    PubMed  Google Scholar 

  • Kristiansen K, Courtois G (1949) Rhythmic electrical activity from isolated cerebral cortex. EEG Clin. Neurophysiol. 1: 265-272.

    Google Scholar 

  • Kopell N, Ermentrout GB, Whittington MA, Traub RD (2000) Gamma rhythms and beta rhythms have different synchronization properties. PNAS 97(4): 1867-1872.

    Article  PubMed  Google Scholar 

  • Lo Conte G, Casamenti F, Bigi V, Milaneshi E, Pepeu G (1982) Effect of magnocellular forebrain lesions on acetylcholine output from the cerebral cortex, electrocorticogam and behavior. Arch. Ital. Biol. 120: 176-188.

    PubMed  Google Scholar 

  • Lund J, Yoshioka T, Levitt J (1993) Comparison of intrinsic connectivity in different areas of macaque monkey cerebral-cortex. Cerebral Cortex 3: 148-162.

    PubMed  Google Scholar 

  • Marrufo MV, Vaquero E, Cardoso MJ, Gomez CM (2001) Temporal evolution of á and â bands during visual spatial attention. Cog. Brain Res. 12: 315-320.

    Article  Google Scholar 

  • McCormick DA(1992) Neurotransmitter actions in the thalamus and cerebral cortex. J. Clin. Neurophysiol. 9(21): 212-223.

  • Muller MM (2000) Oscillatory cortical activities in the gamma band in the human EEG induced by visual stimuli-representation of the stimulus? Acta Neurobiol. Exp. 60: 49-65.

    Google Scholar 

  • Nicolelis MAL, Fanselow EE (2002) Thalamocortical optimization of tactile processing according to behavioral state. Nature Neurosci. 5(6): 517-523.

    Article  PubMed  Google Scholar 

  • Nunez PL, Wingeier BM, Silberstein RB (2001) Spatial-temporal structures of human alpha rhythms: Theory, microcurrent sources, multiscale measurements, and global binding of local networks. Human Brain Mapping 13(3): 125-164.

    Article  PubMed  Google Scholar 

  • Pantev C (1995) Evoked and induced gamma band activity of the human cortex. Brain Topog. 7: 321-330.

    Google Scholar 

  • Pare D, Lang EJ (1998) Calcium electrogenesis in neocortical pyramidal neurons in vivo. Eur. J. Neuosci. 10: 3164-3170.

    Article  Google Scholar 

  • Roelfsema PR, Engel AK, KÖnig P, Singer W (1997) Visuomotor integration is associated with zero time-lag synchronization among cortical areas. Nature 385: 157-161.

    Article  PubMed  Google Scholar 

  • Sherman SM (2001) Tonic and burst firing: Dual modes of thalamocortical relay. Trends Neurosci. 24(2): 122-126.

    Article  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Steriade M, McCormick DA, Sejnowski TJ (1993) Thalamocortical oscillations in the sleeping and aroused brain. Science 262: 679-685.

    PubMed  Google Scholar 

  • Steriade M, Timofeev I, Grenier F, Durmuller N (1998) Role of thalamic and cortical neurons in augmenting responses and selfsustaining activity: Dual intracellular recordings in vivo. J Neurosci. 18: 6425-6443.

    PubMed  Google Scholar 

  • Tallon-Baudry C, Bertrand O (1999) Oscillatory gamma activity in humans and its role in object representation. Trends Cog. Sci. 3(4): 151-162.

    Article  Google Scholar 

  • Timofeev I, Grenier F, Bazhenov M, Houweling AR, Sejnowski TJ, Steriade M (2002) Short-and medium-term plasticity associated with augmenting responses in cortical slabs and spindles in intact cortex of cats in vivo. J. Physiol. 542(2): 583-598.

    Article  PubMed  Google Scholar 

  • Traub RD, Jefferys JGR, Whittington MA (1997) Simulation of gamma rhythms in networks of interneurons and pyramidal cells. J. Comput. Neurosci. 4(2): 141-150.

    Article  PubMed  Google Scholar 

  • Traub RD, Jefferys JGR, Whittington MA (1999) Fast Oscillations in Cortical Circuits. MIT Press, Cambridge.

    Google Scholar 

  • Traub RD, Whittington MA, Buhl EH, Jefferys JGR, Faulkner HJ (1999) On the mechanism of the γ → β frequency shift in neuronal oscillations induced in rat hippocampal slices by tetanic stimulation. J. Neurosci. 19(3): 1088-1105.

    PubMed  Google Scholar 

  • Traub RD, Whittington MA, Colling SB (1996) Analysis of gamma rhythms in the rat hippocampus in vitro and in vivo. J. Physiol. London 493(2): 471-484.

    PubMed  Google Scholar 

  • von Stein A, Rappelsberger P, Sarnthein J, Petsche H (1999) Synchronization between temporal and parietal cortex during multimodal object processing in man. Cerebral Cortex 9(2): 137-150.

    Article  PubMed  Google Scholar 

  • von Stein A, Sarnthein J (2000) Different frequencies for different scales of cortical integration: From local gamma to long range alpha/theta synchronization. Int. J. Psychophysiol. 38(3): 301-313.

    Article  PubMed  Google Scholar 

  • Wang XJ, Golomb D, Rinzel J (1995) Emergent spindle oscillations and intermittent burst firing in a thalamic model: Specific neuronal mechanisms. PNAS 92: 5577-5581.

    PubMed  Google Scholar 

  • White EL (1989) Cortical Circuits: Synaptic Organization of the Cerebral Cortex. Structure, Function, and Theory. Birkhauser, Boston, MA.

    Google Scholar 

  • Whittington MA, Traub RD, Faulkner HJ, Stanford IM, Jefferys JGR (1997) Recurrent excitatory postsynaptic potentials induced by synchronized fast cortical oscillations. PNAS 94: 12198-12203.

    Article  PubMed  Google Scholar 

  • Whittington MA, Traub RD, Jefferys JGR (1995) Synchronized osillations in interneuron networks driven by metabotropic glutamatereceptor activation. Nature 373(6515): 612-615.

    Article  PubMed  Google Scholar 

  • Whittington MA, Traub RD, Kopell N, Ermentrout GB, Buhl EH (2000) Inhibition-based rhythms: Experimental and mathematical observations on network dynamics. Int. J. Psychophysiol. 38: 315-336.

    Article  PubMed  Google Scholar 

  • Winfree AT (1980) The Geometry of Biological Time. Springer, New York.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Neuroscience, Brown University, Box 1953, Providence, RI, 02912, USA

    David J. Pinto

  2. Harvard Medical School, NMR Center, Massachusetts General Hospital, Charlestown, MA, 02129, USA

    Stephanie R. Jones

  3. Department of Mathematics and Center for Biodynamics, Boston University, Boston, MA, 02215, USA

    Tasso J. Kaper & Nancy Kopell

Authors
  1. David J. Pinto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stephanie R. Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tasso J. Kaper
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nancy Kopell
    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

Pinto, D.J., Jones, S.R., Kaper, T.J. et al. Analysis of State-Dependent Transitions in Frequency and Long-Distance Coordination in a Model Oscillatory Cortical Circuit. J Comput Neurosci 15, 283–298 (2003). https://doi.org/10.1023/A:1025825102620

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1025825102620

Search

Navigation