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.
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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.
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.
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.
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.
Castro-Alamancos MA, Connors BW (1996a) Short-term plasticity of a thalamocortical pathway dynamically modulated by behavioral state. Science 272: 274-277.
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.
Celesia GG, Jasper HH (1966) Acetylcholine released from cerebral cortex in relation to state of activation. Neurologist 16: 1053-1064.
Chow CC, White JA, Ritt J, Kopell N (1998) Frequency control in synchronized networks of inhibitory neurons. J. Comput. Neurosci. 5: 407-420.
Connors BW, Amitai Y (1997) Making waves in the neocortex. Neuron 18: 347-349.
da Silva LF (1991) Neural mechanisms underlying brain waves: From neural membranes to networks. Electroenceph. Clin. Neurophysiol. 79: 81-93.
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.
Destexhe A, Babloyantz A, Sejnowski TJ (1993) Ionic mechanisms for intrinsic slow oscillations in thalamic relay neurons. Biophys. J. 65: 1538-1552.
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.
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.
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.
Devaney RL (1992) A First Course in Chaotic Dynamical Systems: Theory and Experiment. Addison-Wesley, Reading, MA.
Dringenberg HC, Vanderwolf CH (1997) Neocortical activation: Modulation by multiple pathways acting on central cholinergic and serotonergic systems. Exp. Brain Res. 116: 160-174.
Ermentrout GB, Kopell N (1998) Fine structure of neural spiking and synchronization in the presence of conduction delays. PNAS 95: 1259-1264.
Fanselow EE, Nicolelis MAL (1999) Behavioral modulation of tactile responses in the rat somatosensory system. J. Neurosci. 19: 7603-7616.
Farmer SF (1998) Rhythmicity, synchronization and binding in human and primate motor systems. J. Physiol. 509(1): 3-14.
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.
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.
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.
Hasselmo ME (1995) Neuromodulation and cortical function: Modeling the physiological basis of behavior. Behav. Brain Res. 67: 1-27.
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.
Karbowski J, Kopell N (2000) Multispikes and synchronization in a large neural network with temporal delays. Neural Comp. 12: 1573-1606.
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.
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.
Kristiansen K, Courtois G (1949) Rhythmic electrical activity from isolated cerebral cortex. EEG Clin. Neurophysiol. 1: 265-272.
Kopell N, Ermentrout GB, Whittington MA, Traub RD (2000) Gamma rhythms and beta rhythms have different synchronization properties. PNAS 97(4): 1867-1872.
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.
Lund J, Yoshioka T, Levitt J (1993) Comparison of intrinsic connectivity in different areas of macaque monkey cerebral-cortex. Cerebral Cortex 3: 148-162.
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.
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.
Nicolelis MAL, Fanselow EE (2002) Thalamocortical optimization of tactile processing according to behavioral state. Nature Neurosci. 5(6): 517-523.
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.
Pantev C (1995) Evoked and induced gamma band activity of the human cortex. Brain Topog. 7: 321-330.
Pare D, Lang EJ (1998) Calcium electrogenesis in neocortical pyramidal neurons in vivo. Eur. J. Neuosci. 10: 3164-3170.
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.
Sherman SM (2001) Tonic and burst firing: Dual modes of thalamocortical relay. Trends Neurosci. 24(2): 122-126.
Silva LR, Amitai Y, Connors BW (1991) Intrinsic oscillations of neocortex generated by layer 5 pyramidal neurons. Science 251: 432-435.
Steriade M, McCormick DA, Sejnowski TJ (1993) Thalamocortical oscillations in the sleeping and aroused brain. Science 262: 679-685.
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.
Tallon-Baudry C, Bertrand O (1999) Oscillatory gamma activity in humans and its role in object representation. Trends Cog. Sci. 3(4): 151-162.
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.
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.
Traub RD, Jefferys JGR, Whittington MA (1999) Fast Oscillations in Cortical Circuits. MIT Press, Cambridge.
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.
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.
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.
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.
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.
White EL (1989) Cortical Circuits: Synaptic Organization of the Cerebral Cortex. Structure, Function, and Theory. Birkhauser, Boston, MA.
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.
Whittington MA, Traub RD, Jefferys JGR (1995) Synchronized osillations in interneuron networks driven by metabotropic glutamatereceptor activation. Nature 373(6515): 612-615.
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.
Winfree AT (1980) The Geometry of Biological Time. Springer, New York.
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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
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DOI: https://doi.org/10.1023/A:1025825102620