Theory article Special Issues

Gamma Oscillations and Neural Field DCMs Can Reveal Cortical Excitability and Microstructure

  • Received: 24 February 2014 Accepted: 17 April 2014 Published: 10 May 2014
  • This paper shows how gamma oscillations can be combined with neural population models and dynamic causal modeling (DCM) to distinguish among alternative hypotheses regarding cortical excitability and microstructure. This approach exploits inter-subject variability and trial-specific effects associated with modulations in the peak frequency of gamma oscillations. Neural field models are used to evaluate model evidence and obtain parameter estimates using invasive and non-invasive gamma recordings. Our overview comprises two parts: in the first part, we use neural fields to simulate neural activity and distinguish the effects of post synaptic filtering on predicted responses in terms of synaptic rate constants that correspond to different timescales and distinct neurotransmitters. We focus on model predictions of conductance and convolution based field models and show that these can yield spectral responses that are sensitive to biophysical properties of local cortical circuits like synaptic kinetics and filtering; we also consider two different mechanisms for this filtering: a nonlinear mechanism involving specific conductances and a linear convolution of afferent firing rates producing post synaptic potentials. In the second part of this paper, we use neural fields quantitatively—to fit empirical data recorded during visual stimulation. We present two studies of spectral responses obtained from the visual cortex during visual perception experiments: in the first study, MEG data were acquired during a task designed to show how activity in the gamma band is related to visual perception, while in the second study, we exploited high density electrocorticographic (ECoG) data to study the effect of varying stimulus contrast on cortical excitability and gamma peak frequency.

    Citation: Dimitris Pinotsis, Karl Friston. Gamma Oscillations and Neural Field DCMs Can Reveal Cortical Excitability and Microstructure[J]. AIMS Neuroscience, 2014, 1(1): 18-38. doi: 10.3934/Neuroscience.2014.1.18

    Related Papers:

  • This paper shows how gamma oscillations can be combined with neural population models and dynamic causal modeling (DCM) to distinguish among alternative hypotheses regarding cortical excitability and microstructure. This approach exploits inter-subject variability and trial-specific effects associated with modulations in the peak frequency of gamma oscillations. Neural field models are used to evaluate model evidence and obtain parameter estimates using invasive and non-invasive gamma recordings. Our overview comprises two parts: in the first part, we use neural fields to simulate neural activity and distinguish the effects of post synaptic filtering on predicted responses in terms of synaptic rate constants that correspond to different timescales and distinct neurotransmitters. We focus on model predictions of conductance and convolution based field models and show that these can yield spectral responses that are sensitive to biophysical properties of local cortical circuits like synaptic kinetics and filtering; we also consider two different mechanisms for this filtering: a nonlinear mechanism involving specific conductances and a linear convolution of afferent firing rates producing post synaptic potentials. In the second part of this paper, we use neural fields quantitatively—to fit empirical data recorded during visual stimulation. We present two studies of spectral responses obtained from the visual cortex during visual perception experiments: in the first study, MEG data were acquired during a task designed to show how activity in the gamma band is related to visual perception, while in the second study, we exploited high density electrocorticographic (ECoG) data to study the effect of varying stimulus contrast on cortical excitability and gamma peak frequency.


    加载中
    [1] Pinotsis DA, Friston KJ. (2014). Neural fields, neural masses and Bayesian modelling. In Neural Fields: Theory and Applications. S. Coombes, P. beimGraben, R. Potthast, J. Wright (Eds. ). Berlin: Springer-Verlag.
    [2] Deco G, Jirsa VK, Robinson PA, Breakspear M, Friston K. (2008) The Dynamic Brain: From Spiking Neurons to Neural Masses and Cortical Fields. PLoS Comput Biol 4(8): e1000092. doi:10. 1371/journal. pcbi. 1000092.
    [3] Jirsa VK. (2004). Connectivity and dynamics of neural information processing. Neuroinformatics2: 183-204.
    [4] Coombes S, Venkov NA, Shiau L, Bojak I, Liley DTJ, Laing CR. (2007) Modeling electrocortical activity through improved local approximations of integral neural field equations. Phys Rev E76(5 Pt 1): 051901.
    [5] Robinson PA, Loxley PN, O'Connor SC, Rennie CJ. (2001) Modal analysis of corticothalamic dynamics, electroencephalographic spectra, and evoked potentials. Phys Rev E 63(4 Pt 1):041909.
    [6] Breakspear M, Roberts JA, Terry JR, Rodrigues S, Mahant N, Robinson PA. (2006) A unifying explanation of primary generalized seizures through nonlinear brain modeling and bifurcation analysis. Cereb Cortex 16: 1296-1313.
    [7] Rodrigues S, Barton D, Szalai R, Benjamin O, Richardson MP, Terry JR. (2009) Transitions to spike-wave oscillations and epileptic dynamics in a human cortico-thalamic mean-field model. J comput neurosci 27: 507-526. doi: 10.1007/s10827-009-0166-2
    [8] Pinotsis DA, Hansen E, Friston KJ, Jirsa VK. (2013) Anatomical connectivity and the resting state activity of large cortical networks. NeuroImage 65: 127-138. doi: 10.1016/j.neuroimage.2012.10.016
    [9] Pinotsis DA, Schwarzkopf DS, Litvak V, Rees G, Barnes G, Friston KJ. (2013) Dynamic causal modelling of lateral interactions in the visual cortex. NeuroImage 66: 563-576. doi: 10.1016/j.neuroimage.2012.10.078
    [10] Pinotsis DA, Brunet N, Bastos A, Bosman CA, Litvak V, Fries P, Friston KJ. (2014) Contrast gain-control and horizontal interactions in V1: A DCM study. NeuroImage 92C: 143-155
    [11] Riera JJ, Jimenez JC, Wan X, Kawashima R, Ozaki T. (2007) Nonlinear local electrovascular coupling. II: From data to neuronal masses. Hum brain mapp 28: 335-354.
    [12] Schiff S, Sauer T. (2008) Kalman filter control of a model of spatiotemporal cortical dynamics. BMC Neurosci 5(1): 1-8.
    [13] Angelucci A, Bressloff PC. (2006) Contribution of feedforward, lateral and feedback connections to the classical receptive field center and extra-classical receptive field surround of primate V1 Neurons. Prog Brain Res 154: 93-120. doi: 10.1016/S0079-6123(06)54005-1
    [14] Burkhalter A, Bernardo KL. (1989) Organization of corticocortical connections in human visual cortex. Proc Natl Acad Sci USA 86(3): 1071-5.
    [15] Wallace MN, Bajwa S. ( 1991) Patchy intrinsic connections of the ferret primary auditory cortex. Neuroreport 2(8): 417-20.
    [16] Stettler DD, Das A, Bennett J, Gilbert CD. (2002) Lateral connectivity and contextual interactions in macaque primary visual cortex. Neuron 36: 739-750. doi: 10.1016/S0896-6273(02)01029-2
    [17] Baker TI, Cowan JD. (2009) Spontaneous pattern formation and pinning in the primary visual cortex. J Physio Paris 103: 52-68. doi: 10.1016/j.jphysparis.2009.05.011
    [18] Wen Q, Chklovskii DB. (2008) A cost–benefit analysis of neuronal morphology. J neurophysiol99: 2320-2328.
    [19] Cherniak C. (1994) Component placement optimization in the brain. J neurosci 14: 2418-2427.
    [20] Bassett DS, Greenfield DL, Meyer-Lindenberg A, Weinberger DR, Moore SW, Bullmore ET. (2010) Efficient physical embedding of topologically complex information processing networks in brains and computer circuits. PLoS comput biol 6(4): e1000748. doi:10. 1371/journal. pcbi. 1000748
    [21] Grindrod P, Pinotsis DA. (2011) On the spectra of certain integro-differential-delay problems with applications in neurodynamics. Physica D 240: 13-20. doi: 10.1016/j.physd.2010.08.002
    [22] Pinotsis DA, Friston KJ. (2011) Neural fields, spectral responses and lateral connections. Neuroimage 55: 39-48. doi: 10.1016/j.neuroimage.2010.11.081
    [23] Sceniak MP, Hawken MJ, Shapley R. (2001). Visual spatial characterization of macaque V1 neurons. J Neurophysiol 85: 1873-1887.
    [24] Sceniak MP, Chatterjee S, Callaway EM. (2006) Visual spatial summation in macaque geniculocortical afferents. J Neurophysiol 96: 3474-3484. doi: 10.1152/jn.00734.2006
    [25] Sceniak MP, Ringach DL, Hawken MJ, Shapley R. (1999) Contrast's effect on spatial summation by macaque V1 neurons. Nat neurosci 2: 733-739. doi: 10.1038/11197
    [26] Kapadia MK, Westheimer G, Gilbert CD. (1999) Dynamics of spatial summation in primary visual cortex of alert monkeys. Proc Natl Acad Sci USA 96: 12073-12078. doi: 10.1073/pnas.96.21.12073
    [27] Ray S, Maunsell JH. (2010) Differences in gamma frequencies across visual cortex restrict their possible use in computation. Neuron 67(5): 885-896.
    [28] Hodgkin AL, Huxley AF. (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J physiol 117(4): 500-544.
    [29] Traub RD, Kopell N, Bibbig A, Buhl EH, LeBeau FE, Whittington MA. (2001) Gap junctions between interneuron dendrites can enhance synchrony of gamma oscillations in distributed networks. J Neurosci 21: 9478-9486.
    [30] Moran RJ, Stephan KE, Kiebel SJ, Rombach N, O'Connor WT, Murphy KJ, Reilly RB, Friston KJ. (2008) Bayesian estimation of synaptic physiology from the spectral responses of neural masses. Neuroimage 42: 272-84. doi: 10.1016/j.neuroimage.2008.01.025
    [31] Moran RJ, Stephan KE, Dolan RJ, Friston KJ. (2011) Consistent spectral predictors for dynamic causal models of steady-state responses. Neuroimage 55: 1694-1708. doi: 10.1016/j.neuroimage.2011.01.012
    [32] Goldstein SS, Rall W. (1974) Changes of action potential shape and velocity for changing core conductor geometry. Biophys J 14: 731-757. doi: 10.1016/S0006-3495(74)85947-3
    [33] Ellias SA, Grossberg S. (1975) Pattern formation, contrast control, and oscillations in the short term memory of shunting on-center off-surround networks. Biol Cybern 20: 69-98. doi: 10.1007/BF00327046
    [34] Somers DC, Nelson SB, Sur M. (1995) An emergent model of orientation selectivity in cat visual cortical simple cells. J neurosci 15: 5448-5465.
    [35] Ermentrout B. (1998) Neural networks as spatio-temporal pattern-forming systems. Rep progin phys 61: 353. doi: 10.1088/0034-4885/61/4/002
    [36] Jansen BH, Rit VG. (1995) Electroencephalogram and visual evoked potential generation in a mathematical model of coupled cortical columns. Biol Cybern 73: 357-66. doi: 10.1007/BF00199471
    [37] Pinotsis D, Leite M, Friston K. (2013) On conductance-based neural field models. Front. Comput. Neurosci 7: 158. doi: 10. 3389/fncom. 2013. 00158.
    [38] Pinotsis DA, Moran RJ, Friston KJ. (2012) Dynamic causal modeling with neural fields. Neuroimage 59: 1261-1274. doi: 10.1016/j.neuroimage.2011.08.020
    [39] Faulkner HJ, Traub RD, Whittington MA. (2009) Disruption of synchronous gamma oscillations in the rat hippocampal slice: A common mechanism of anaesthetic drug action. Brit pharmacol125: 483-492.
    [40] Moran RJ, Jung F, Kumagai T, Endepols H, Graf R, Dolan RJ, Friston KJ, Stephan KE, Tittgemeyer M. (2011) Dynamic causal models and physiological inference: a validation study using isoflurane anaesthesia in rodents. PloS one 6: e22790. doi: 10.1371/journal.pone.0022790
    [41] Pinotsis DA, Moran RJ, Friston KJ. (2012) Dynamic causal modeling with neural fields. NeuroImage 59: 1261-1274. doi: 10.1016/j.neuroimage.2011.08.020
    [42] Bastos AM, Usrey WM, Adams RA, Mangun GR, Fries P, Friston KJ. (2012) Canonical microcircuits for predictive coding. Neuron 76: 695-711. doi: 10.1016/j.neuron.2012.10.038
    [43] Buffalo EA, Fries P, Landman R, Buschman TJ, Desimone R. (2011) Laminar differences in gamma and alpha coherence in the ventral stream. Proc Natl Acad Sci USA 108: 11262. doi: 10.1073/pnas.1011284108
    [44] Haider B, Duque A, Hasenstaub AR, McCormick DA. (2006) Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition. J neurosci 26:4535-4545. doi: 10.1523/JNEUROSCI.5297-05.2006
    [45] Jansen BH, Rit VG. (1995) Electroencephalogram and visual evoked potential generation in a mathematical model of coupled cortical columns. Biol Cybern 73:357-66. doi: 10.1007/BF00199471
    [46] Friston K, Mattout J, Trujillo-Barreto N, Ashburner J, Penny W. (2007). Variational free energy and the Laplace approximation. Neuroimage 34: 220-234. doi: 10.1016/j.neuroimage.2006.08.035
    [47] Wilson HR, Cowan JD. (1973) Mathematical Theory of Functional Dynamics of Cortical and Thalamic Nervous-Tissue. Kybernetik 13: 55-80. doi: 10.1007/BF00288786
    [48] Pelinovsky DE, Yakhno VG. (1996) Generation of collective-activity structures in a homogeneous neuron-like medium. I. Bifurcation analysis of static structures. Int J Bifurcat Chaos 6: 81-88.
    [49] Pinto DJ, Brumberg JC, Simons DJ, Ermentrout GB. (1996) A quantitative population model of whisker barrels: re-examining the Wilson-Cowan equations. J Comput Neurosci 3: 247-64. doi: 10.1007/BF00161134
    [50] Robinson PA, Rennie CJ, Rowe DL, O'Connor SC, Gordon E. (2005) Multiscale brain modelling. Philos T Roy Soc B 360: 1043-1050. doi: 10.1098/rstb.2005.1638
    [51] Coombes S. (2005) Waves, bumps, and patterns in neural field theories. Biol Cybern 93: 91-108. doi: 10.1007/s00422-005-0574-y
    [52] Valdes PA, Jimenez JC, Riera J, Biscay R, Ozaki T. (1999) Nonlinear EEG analysis based on a neural mass model. Biol cybern 81: 415-424. doi: 10.1007/s004220050572
    [53] Robinson PA, Loxley PN, O'Connor SC, Rennie CJ. (2001) Modal analysis of corticothalamic dynamics, electroencephalographic spectra, and evoked potentials. Phys Rev E 63(4 Pt 1):041909
    [54] Kopell N, Ermentrout GB, Whittington MA, Traub RD. (2000) Gamma rhythms and beta rhythms have different synchronization properties. Proc Natl Acad Sci USA 97: 1867-72. doi: 10.1073/pnas.97.4.1867
    [55] Jia X, Xing D, Kohn A. (2013) No consistent relationship between gamma power and peak frequency in macaque primary visual cortex. J Neurosci 33: 17-25. doi: 10.1523/JNEUROSCI.1687-12.2013
    [56] Chambers JD, Bethwaite B, Diamond NT, Peachey T, Abramson D, Petrou S, Thomas EA. (2012) Parametric computation predicts a multiplicative interaction between synaptic strength parameters that control gamma oscillations. Front Comput Neurosci 6:53 doi:10. 3389/fncom. 2012. 00053.
    [57] Schwarzkopf DS, Robertson DJ, Song C, Barnes GR, Rees G. (2012) The Frequency of Visually Induced Gamma-Band Oscillations Depends on the Size of Early Human Visual Cortex. J Neurosci 32: 1507-1512. doi: 10.1523/JNEUROSCI.4771-11.2012
    [58] Schwarzkopf DS, Robertson DJ, Song C, Barnes GR, Rees G. (2012) The Frequency of Visually Induced Gamma-Band Oscillations Depends on the Size of Early Human Visual Cortex. J Neurosci 32: 1507-1512. doi: 10.1523/JNEUROSCI.4771-11.2012
    [59] Muthukumaraswamy SD, Edden RA. , Jones DK, Swettenham JB, Singh KD. (2009) Resting GABA concentration predicts peak gamma frequency and fMRI amplitude in response to visual stimulation in humans. Proc Natl Acad Sci 106: 8356-8361. doi: 10.1073/pnas.0900728106
    [60] Pinotsis DA, Friston KJ. (2011) Neural fields, spectral responses and lateral connections. Neuroimage 55: 39-48. doi: 10.1016/j.neuroimage.2010.11.081
    [61] Gaetz W, Roberts TP. , Singh KD, Muthukumaraswamy SD. (2011) Functional and structural correlates of the aging brain: Relating visual cortex (V1) gamma band responses to age ‐related structural change. Hum Brain Mapp 33(9): 2035-46.
    [62] Muthukumaraswamy SD, Edden RA. , Jones DK, Swettenham JB, Singh KD. (2009) Resting GABA concentration predicts peak gamma frequency and fMRI amplitude in response to visual stimulation in humans. Proc Natl Acad Sci 106: 8356-8361. doi: 10.1073/pnas.0900728106
    [63] Rubehn B, Bosman C, Oostenveld R, Fries P, Stieglitz T: A MEMS-based flexible multichannel ECoG-electrode array. J. Neural Eng 6 036003 doi:10. 1088/1741-2560/6/3/036003.
    [64] Bosman CA, Schoffelen J-M, Brunet N, Oostenveld R, Bastos AM, Womelsdorf T, Rubehn B, Stieglitz T, De Weerd P, Fries P. (2009) Attentional stimulus selection through selective synchronization between monkey visual areas. Neuron 75: 875-888.
    [65] Feldman H, Friston KJ. (2010) Attention, uncertainty, and free-energy. Front Hum Neurosci 4:215. doi: 10. 3389/fnhum. 2010. 00215.
    [66] Kang K, Shelley M, Henrie JA, Shapley R. (2010) LFP spectral peaks in V1 cortex: network resonance and cortico-cortical feedback. J computat neurosci 29: 495-507. doi: 10.1007/s10827-009-0190-2
    [67] Brunel N, Wang X-J. (2003) What determines the frequency of fast network oscillations with irregular neural discharges? I. Synaptic dynamics and excitation-inhibition balance. J Neurophysiol 90: 415-430.
    [68] Traub RD, Jefferys JG, Whittington MA. (1997) Simulation of gamma rhythms in networks of interneurons and pyramidal cells. J comput neurosci 4: 141-150. doi: 10.1023/A:1008839312043
    [69] Schwarzkopf DS, Song C, Rees G. (2011) Linking perceptual experience with the functional architecture of the visual cortex. J Vis 11: 844-844. doi: 10.1167/11.11.844
    [70] Harvey BM, Dumoulin SO. (2011) The Relationship between Cortical Magnification Factor and Population Receptive Field Size in Human Visual Cortex: Constancies in Cortical Architecture. J Neurosci 31: 13604-13612. doi: 10.1523/JNEUROSCI.2572-11.2011
  • Reader Comments
  • © 2014 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0)
通讯作者: 陈斌, bchen63@163.com
  • 1. 

    沈阳化工大学材料科学与工程学院 沈阳 110142

  1. 本站搜索
  2. 百度学术搜索
  3. 万方数据库搜索
  4. CNKI搜索

Metrics

Article views(5674) PDF downloads(1230) Cited by(5)

Article outline

Figures and Tables

Figures(5)

Other Articles By Authors

/

DownLoad:  Full-Size Img  PowerPoint
Return
Return

Catalog