×

Comparison between an exact and a heuristic neural mass model with second-order synapses. (English) Zbl 1521.92027

Summary: Neural mass models (NMMs) are designed to reproduce the collective dynamics of neuronal populations. A common framework for NMMs assumes heuristically that the output firing rate of a neural population can be described by a static nonlinear transfer function (NMM1). However, a recent exact mean-field theory for quadratic integrate-and-fire (QIF) neurons challenges this view by showing that the mean firing rate is not a static function of the neuronal state but follows two coupled nonlinear differential equations (NMM2). Here we analyze and compare these two descriptions in the presence of second-order synaptic dynamics. First, we derive the mathematical equivalence between the two models in the infinitely slow synapse limit, i.e., we show that NMM1 is an approximation of NMM2 in this regime. Next, we evaluate the applicability of this limit in the context of realistic physiological parameter values by analyzing the dynamics of models with inhibitory or excitatory synapses. We show that NMM1 fails to reproduce important dynamical features of the exact model, such as the self-sustained oscillations of an inhibitory interneuron QIF network. Furthermore, in the exact model but not in the limit one, stimulation of a pyramidal cell population induces resonant oscillatory activity whose peak frequency and amplitude increase with the self-coupling gain and the external excitatory input. This may play a role in the enhanced response of densely connected networks to weak uniform inputs, such as the electric fields produced by noninvasive brain stimulation.

MSC:

92C20 Neural biology
34A34 Nonlinear ordinary differential equations and systems

Software:

AUTO; AUTO-07P

References:

[1] Aberra AS, Peterchev AV, Grill WM (2018) Biophysically realistic neuron models for simulation of cortical stimulation. J Neural Eng 15(6):066-023. doi:10.1088/1741-2552/aadbb1 (http://stacks.iop.org/1741-2552/15/i=6/a=066023?key=crossref.c24583b2463818cf852344f5de358599)
[2] Agmon-Snir H, Segev I (1993) Signal delay and input synchronization in passive dendritic structures. J Neurophysiol 70(5):5556
[3] Augustin M, Ladenbauer J, Baumann F et al (2017) Low-dimensional spike rate models derived from networks of adaptive integrate-and-fire neurons: comparison and implementation. PLoS Comput Biol 13(6):e1005-545. doi:10.1371/journal.pcbi.1005545
[4] Avermann M, Tomm C, Mateo C et al (2012) Microcircuits of excitatory and inhibitory neurons in layer 2/3 of mouse barrel cortex. J Neurophysiol 107(11):3116-34. doi:10.1152/jn.00917.2011
[5] Avitabile D, Desroches M, Ermentrout GB (2022) Cross-scale excitability in networks of synaptically-coupled quadratic integrate-and-fire neurons. doi:10.48550/ARXIV.2203.08634, https://arxiv.org/abs/2203.08634
[6] Bacci, A.; Rudolph, U.; Huguenard, JR, Major differences in inhibitory synaptic transmission onto two neocortical interneuron subclasses, J Neurosci, 23, 29, 9664-74 (2003) · doi:10.1523/JNEUROSCI.23-29-09664.2003
[7] Bartos, M.; Vida, I.; Frotscher, M., Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks, Proc Natl Acad Sci, 99, 20, 13222-13227 (2002) · doi:10.1073/pnas.192233099
[8] Bartos, M.; Vida, I.; Jonas, P., Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks, Nat Rev Neurosci, 8, 1, 45-56 (2007) · doi:10.1038/nrn2044
[9] Benayoun, M.; Cowan, JD; van Drongelen, W., Avalanches in a Stochastic Model of Spiking Neurons, PLoS Comput Biol, 6, 7, e1000-846 (2010) · doi:10.1371/journal.pcbi.1000846
[10] Bi, H.; di Volo, M.; Torcini, A., Asynchronous and coherent dynamics in balanced excitatory-inhibitory spiking networks, Front Syst Neurosci, 15, 609 (2021) · doi:10.3389/fnsys.2021.752261
[11] Bikson, M.; Inoue, M.; Akiyama, H., Effects of uniform extracellular DC electric fields on excitability in rat hippocampal slices in vitro, J Physiol, 557, Pt 1, 175-90 (2004) · doi:10.1113/jphysiol.2003.055772
[12] Brunel, N.; Hakim, V., Sparsely synchronized neuronal oscillations, Chaos Interdiscip J Nonlinear Sci, 18, 1, 015-113 (2008) · doi:10.1063/1.2779858
[13] Buice, MA; Cowan, JD; Chow, CC, Systematic fluctuation expansion for neural network activity equations, Neural Comput, 22, 2, 377-426 (2010) · Zbl 1183.92013 · doi:10.1162/neco.2009.02-09-960
[14] Buzsáki, G.; Wang, XJ, Mechanisms of gamma oscillations, Annu Rev Neurosci, 35, 1, 203-225 (2012) · doi:10.1146/annurev-neuro-062111-150444
[15] Byrne, Á.; óDea, RD; Forrester, M., Next-generation neural mass and field modeling, J Neurophysiol, 123, 2, 726-742 (2020) · doi:10.1152/jn.00406.2019
[16] Byrne, Á.; Ross, J.; Nicks, R., Mean-field models for EEG/MEG: from oscillations to waves, Brain Topogr, 35, 1, 36-53 (2022) · doi:10.1007/s10548-021-00842-4
[17] Camera, GL; Rauch, A.; Lüscher, HR, Minimal models of adapted neuronal response to in vivo –like input currents, Neural Comput, 16, 10, 2101-2124 (2004) · Zbl 1055.92011 · doi:10.1162/0899766041732468
[18] Cardin, JA; Carlén, M.; Meletis, K., Driving fast-spiking cells induces gamma rhythm and controls sensory responses, Nature, 459, 7247, 663-667 (2009) · doi:10.1038/nature08002
[19] Carhart-Harris, RL, The entropic brain-revisited, Neuropharmacology (2018) · doi:10.1016/j.neuropharm.2018.03.010
[20] Carlu, M.; Chehab, O.; Dalla Porta, L., A mean-field approach to the dynamics of networks of complex neurons, from nonlinear Integrate-and-Fire to Hodgkin-Huxley models, J Neurophysiol, 123, 3, 1042-1051 (2020) · doi:10.1152/jn.00399.2019
[21] Chialvo, DR, Critical brain networks, Physica A, 340, 4, 756-765 (2004) · doi:10.1016/j.physa.2004.05.064
[22] Clusella P, Montbrió E (2022) Regular and sparse neuronal synchronization are described by identical mean field dynamics. doi:10.48550/ARXIV.2208.05515, https://arxiv.org/abs/2208.05515
[23] Coombes S, Byrne Á (2019) Next generation neural mass models. In: Nonlinear dynamics in computational neuroscience. Springer, pp 1-16
[24] da Silva, FL; Vr, A.; Barts, P., Model of neuronal populations: the basic mechanism of rhythmicity, Prog Brain Res, 3, 45 (1976)
[25] Deleuze, C.; Bhumbra, GS; Pazienti, A., Strong preference for autaptic self-connectivity of neocortical pv interneurons facilitates their tuning to \(\gamma \)-oscillations, PLoS Biol, 17, 9, e3000-419 (2019) · doi:10.1371/journal.pbio.3000419
[26] Destexhe, A.; Mainen, ZF; Sejnowski, TJ; Koch, C.; Segev, I., Kinetic models of synaptic transmission, Methods in neuronal modeling, 1-25 (1998), Cambridge: MIT Press, Cambridge
[27] Devalle, F.; Roxin, A.; Montbrió, E., Firing rate equations require a spike synchrony mechanism to correctly describe fast oscillations in inhibitory networks, PLOS Comput Biol, 13, 12, 7008 (2017) · doi:10.1371/journal.pcbi.1005881
[28] Devalle, F.; Montbrió, E.; Pazó, D., Dynamics of a large system of spiking neurons with synaptic delay, Phys Rev E, 98, 42, 214 (2018) · doi:10.1103/PhysRevE.98.042214
[29] di Volo, M.; Torcini, A., Transition from asynchronous to oscillatory dynamics in balanced spiking networks with instantaneous synapses, Phys Rev Lett, 121, 128, 301 (2018) · doi:10.1103/PhysRevLett.121.128301
[30] Doedel, EJ; Champneys, AR; Dercole, F., Auto-07p: continuation and bifurcation software for ordinary differential equations, Science, 6, 9330 (2007)
[31] Dumont, G.; Gutkin, B., Macroscopic phase resetting-curves determine oscillatory coherence and signal transfer in inter-coupled neural circuits, PLoS Comput Biol, 15, 6, 39 (2019)
[32] Eeckman, FH; Jaas, FW, Asymmetric sigmoid non-linearity in the rat olfactory system, Brain Res, 557, 1-2, 13-21 (1991) · doi:10.1016/0006-8993(91)90110-H
[33] Ermentrout, B., Reduction of conductance-based models with slow synapses to neural nets, Neural Comput, 6, 4, 679-695 (1994) · doi:10.1162/neco.1994.6.4.679
[34] Ermentrout, GB; Terman, DH, Mathematical foundations of neuroscience (2010), New York: Springer, New York · Zbl 1320.92002 · doi:10.1007/978-0-387-87708-2
[35] Eyal, G.; Verhoog, MB; Testa-Silva, G., Human cortical pyramidal neurons: From spines to spikes via models, Front Cell Neurosci, 2, 12 (2018) · doi:10.3389/fncel.2018.00181
[36] Forrester, M.; Crofts, JJ; Sotiropoulos, SN, The role of node dynamics in shaping emergent functional connectivity patterns in the brain, Netw Neurosci, 4, 2, 467-483 (2020) · doi:10.1162/netn\_a_00130
[37] Fourcaud-Trocmé, N.; Hansel, D.; van Vreeswijk, C., How spike generation mechanisms determine the neuronal response to fluctuating inputs, J Neurosci, 23, 37, 11628-11640 (2003) · doi:10.1523/JNEUROSCI.23-37-11628.2003
[38] Freeman, WJ, Linear analysis of the dynamics of neural masses, Annu Rev Biophys Bioeng, 1, 1, 225-256 (1972) · doi:10.1146/annurev.bb.01.060172.001301
[39] Freeman, WJ, Mass action in the nervous system (1975), New York: Academic Press, New York
[40] Freeman, WJ, Simulation of chaotic EEG patterns with a dynamic model of the olfactory system, Biol Cybern, 56, 2-3, 139-50 (1987) · doi:10.1007/BF00317988
[41] Galan A (2021) Realistic modeling of neocortical neurons and electric field effects under direct current stimulation. MSc thesis, Elite Master Program in Neuroengineering, Department of Electrical and Computer Engineering, Technical University of Munich
[42] Gast, R.; Schmidt, H.; Knösche, TR, A mean-field description of bursting dynamics in spiking neural networks with short-term adaptation, Neural Comput, 32, 9, 1615-1634 (2020) · Zbl 1453.92013 · doi:10.1162/neco\_a\_01300
[43] Gerstner, W., Time structure of the activity in neural network models, Phys Rev E, 51, 1, 738-758 (1995) · doi:10.1103/PhysRevE.51.738
[44] Goldobin, DS; di Volo, M.; Torcini, A., Reduction methodology for fluctuation driven population dynamics, Phys Rev Lett, 127, 38, 301 (2021) · doi:10.1103/PhysRevLett.127.038301
[45] Grimbert, F.; Faugeras, O., Analysis of Jansen’s model of a single cortical column, INRIA RR, 5597, 34 (2006)
[46] Jang, HJ; Cho, KH; Park, SW, The development of phasic and tonic inhibition in the rat visual cortex, Korean J Physiol Pharmacol, 14, 299-405 (2010) · doi:10.4196/kjpp.2010.14.6.399
[47] Jansen, BH; Rit, VG, Electroencephalogram and visual evoked potential generation in a mathematical model of coupled cortical columns, Biol Cybern, 73, 4, 357-66 (1995) · Zbl 0827.92010 · doi:10.1007/BF00199471
[48] Jansen, BH; Zouridakis, G.; Brandt, ME, A neurophysiologically-based mathematical model of flash visual evoked potentials, Biol Cybern, 68, 3, 275-83 (1993) · doi:10.1007/BF00224863
[49] Jedynak, M.; Pons, AJ; Garcia-Ojalvo, J., Temporally correlated fluctuations drive epileptiform dynamics, Neuroimage, 146, 188-196 (2017) · doi:10.1016/j.neuroimage.2016.11.034
[50] Karnani, MM; Jackson, J.; Ayzenshtat, I., Cooperative subnetworks of molecularly similar interneurons in mouse neocortex, Neuron, 90, 1, 86-100 (2016) · doi:10.1016/j.neuron.2016.02.037
[51] Kay, LM, The physiological foresight in Freeman’s work, J Conscious Stud, 25, 1-2, 50-63 (2018)
[52] Koch, C.; Segev, I., Methods in neuronal modeling (2003), Cambridge: Bradford Books, Cambridge
[53] Kōksal Ersōz E, Wendling F (2021) Canard solutions in neural mass models: consequences on critical regimes. J Math Neurosc 11(11). doi:10.1186/s13408-021-00109-z · Zbl 1486.92010
[54] Kunze, T.; Hunold, A.; Haueisen, J., Transcranial direct current stimulation changes resting state functional connectivity: a large-scale brain network modeling study, Neuroimage, 140, 174-187 (2016) · doi:10.1016/j.neuroimage.2016.02.015
[55] Laing, CR, Exact neural fields incorporating gap junctions, SIAM J Appl Dyn Syst, 14, 4, 1899-1929 (2015) · Zbl 1369.92020 · doi:10.1137/15M1011287
[56] Latham, PE; Richmond, BJ; Nelson, PG, Intrinsic dynamics in neuronal networks. I. Theory, J Neurophysiol, 83, 2, 808-827 (2000) · doi:10.1152/jn.2000.83.2.808
[57] Lopes da Silva, F.; Hoek, A.; Smits, H., Model of brain rhythmic activity: the alpha rhythm of the thalamus, Kybernetik, 15, 1, 27-37 (1974) · doi:10.1007/BF00270757
[58] Lopez-Sola, E.; Sanchez-Todo, R.; Lleal, È., A personalizable autonomous neural mass model of epileptic seizures, J Neural Eng, 19, 55, 002 (2022) · doi:10.1088/1741-2552/ac8ba8
[59] Mensi, S.; Naud, R.; Pozzorini, C., Parameter extraction and classification of three cortical neuron types reveals two distinct adaptation mechanisms, J Neurophysiol, 107, 6, 1756-1775 (2012) · doi:10.1152/jn.00408.2011
[60] Merlet, I.; Birot, G.; Salvador, R., From oscillatory transcranial current stimulation to scalp EEG changes: a biophysical and physiological modeling study, PLoS ONE, 8, 2, 1-12 (2013) · doi:10.1371/journal.pone.0057330
[61] Molaee-Ardekani, B.; Benquet, P.; Bartolomei, F., Computational modeling of high-frequency oscillations at the onset of neocortical partial seizures: from ‘altered structure’ to ‘dysfunction’, Neuroimage, 52, 3, 1109-22 (2010) · doi:10.1016/j.neuroimage.2009.12.049
[62] Montbrió, E.; Pazó, D., Exact mean-field theory explains the dual role of electrical synapses in collective synchronization, Phys Rev Lett, 125, 248, 101 (2020) · doi:10.1103/PhysRevLett.125.248101
[63] Montbrió, E.; Pazó, D.; Roxin, A., Macroscopic description for networks of spiking neurons, Phys Rev X, 2, 021028 (2015)
[64] Neske, GT; Patrick, SL; Connors, BW, Contributions of diverse excitatory and inhibitory neurons to recurrent network activity in cerebral cortex, J Neurosci, 35, 3, 1089-1105 (2015) · doi:10.1523/JNEUROSCI.2279-14.2015
[65] Oláh, S.; Komlósi, G.; Szabadics, J., Output of neurogliaform cells to various neuron types in the human and rat cerebral cortex, Front Neural Circuits (2007) · doi:10.3389/neuro.04.004.2007
[66] Ostojic, S.; Brunel, N., From spiking neuron models to linear-nonlinear models, PLoS Comput Biol, 7, 1, e1001-056 (2011) · doi:10.1371/journal.pcbi.1001056
[67] Pazó, D.; Montbrió, E., From quasiperiodic partial synchronization to collective chaos in populations of inhibitory neurons with delay, Phys Rev Lett, 116, 238, 101 (2016) · doi:10.1103/PhysRevLett.116.238101
[68] Pereira, U.; Brunel, N., Attractor dynamics in networks with learning rules inferred from in vivo data, Neuron, 99, 1, 227-238.e4 (2018) · doi:10.1016/j.neuron.2018.05.038
[69] Pietras, B.; Devalle, F.; Roxin, A., Exact firing rate model reveals the differential effects of chemical versus electrical synapses in spiking networks, Phys Rev E, 100, 42, 412 (2019)
[70] Pods, J.; Schönke, J.; Bastian, P., Electrodiffusion models of neurons and extracellular space using the poisson-nernst-planck equations-numerical simulation of the intra- and extracellular potential for an axon model, Biophys J, 105, 242-254 (2013) · doi:10.1016/j.bpj.2013.05.041
[71] Pons, AJ; Cantero, JL; Atienza, M., Relating structural and functional anomalous connectivity in the aging brain via neural mass modeling, Neuroimage, 52, 3, 848-861 (2010) · doi:10.1016/j.neuroimage.2009.12.105
[72] Povysheva, NV; Zaitsev, AV; Kröner, S., Electrophysiological differences between neurogliaform cells from monkey and rat prefrontal cortex, J Neurophysiol (2007) · doi:10.1152/jn.00794.2006
[73] Ratas, I.; Pyragas, K., Macroscopic self-oscillations and aging transition in a network of synaptically coupled quadratic integrate-and-fire neurons, Phys Rev E, 94, 3, 032-215 (2016) · doi:10.1103/PhysRevE.94.032215
[74] Ratas, I.; Pyragas, K., Macroscopic oscillations of a quadratic integrate-and-fire neuron network with global distributed-delay coupling, Phys Rev E, 98, 52, 224 (2018) · doi:10.1103/PhysRevE.98.052224
[75] Ratas, I.; Pyragas, K., Noise-induced macroscopic oscillations in a network of synaptically coupled quadratic integrate-and-fire neurons, Phys Rev E, 100, 5, 052-211 (2019) · doi:10.1103/PhysRevE.100.052211
[76] Rauch, A.; Camera, GL; Lüscher, HR, Neocortical pyramidal cells respond as integrate-and-fire neurons to in vivo-like input currents, J Neurphysiol, 90, 1598-1612 (2003) · doi:10.1152/jn.00293.2003
[77] Ruffini, G.; Wendling, F.; Merlet, I., Transcranial current brain stimulation (tCS): models and technologies, IEEE Trans Neural Syst Rehabil Eng, 21, 3, 333-345 (2013) · doi:10.1109/TNSRE.2012.2200046
[78] Ruffini, G.; Wendling, F.; Sanchez-Todo, R., Targeting brain networks with multichannel transcranial current stimulation (tcs), Curr Opin Biomed Eng, 2, 996 (2018)
[79] Ruffini, G.; Salvador, R.; Tadayon, E., Realistic modeling of mesoscopic ephaptic coupling in the human brain, PLoS Comput Biol, 2, 855 (2020)
[80] Ruffini G, Lopez-Sola E (2022) AIT foundations of structured experience
[81] Sanchez-Todo, R.; Salvador, R.; Santarnecchi, E., Personalization of hybrid brain models from neuroimaging and electrophysiology data, BioRxiv, 00, 1-35 (2018) · doi:10.1101/461350
[82] Seay, M.; Natan, RG; Geffen, MN, Differential short-term plasticity of PV and SST neurons accounts for adaptation and facilitation of cortical neurons to auditory tones, J Neurosci, 40, 48, 9224-9235 (2020) · doi:10.1523/JNEUROSCI.0686-20.2020
[83] Stefanovski, L.; Triebkorn, P.; Spiegler, A., Linking molecular pathways and large-scale computational modeling to assess candidate disease mechanisms and pharmacodynamics in alzheimer’s disease, Front Comput Neurosci, 3, 4500 (2019)
[84] Taher, H.; Torcini, A.; Olmi, S., Exact neural mass model for synaptic-based working memory, PLoS Comput Biol, 16, 12, 1-42 (2020) · doi:10.1371/journal.pcbi.1008533
[85] Taher, H.; Avitabile, D.; Desroches, M., Bursting in a next generation neural mass model with synaptic dynamics: a slow-fast approach, Nonlinear Dyn (2022) · doi:10.1007/s11071-022-07406-6
[86] Tiesinga, P.; Sejnowski, TJ, Cortical enlightenment: are attentional gamma oscillations driven by ING or PING?, Neuron, 63, 6, 727-732 (2009) · doi:10.1016/j.neuron.2009.09.009
[87] Traub RD, Spruston N, Soltesz I et al (1998) Gamma-frequency oscillations: a neuronal population phenomenon, regulated by synaptic and intrinsic cellular processes, and inducing synaptic plasticity. Prog Neurobiol 55(6):563-575. doi:10.1016/S0301-0082(98)00020-3
[88] Van Vreeswijk, C.; Abbott, LF; Bard Ermentrout, G., When inhibition not excitation synchronizes neural firing, J Comput Neurosci, 1, 4, 313-321 (1994) · doi:10.1007/BF00961879
[89] Vázquez-Rodríguez B, Avena-Koenigsberger A, Sporns O et al (2017) Stochastic resonance at criticality in a network model of the human cortex. Sci Rep. doi:10.1038/s41598-017-13400-5
[90] Wendling F, Chauvel P (2008) Transition to ictal activity in temporal lobe epilepsy: insights from macroscopic models. Comput Neurosci Epilepsy. doi:10.1016/B978-012373649-9.50026-0
[91] Wendling, F.; Bartolomei, F.; Bellanger, JJ, Epileptic fast activity can be explained by a model of impaired GABAergic dendritic inhibition, Eur J Neurosci, 15, 9, 1499-508 (2002) · doi:10.1046/j.1460-9568.2002.01985.x
[92] Whittington MA, Traub RD, Jefferys JGR (1995) Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373(6515):612-615. doi:10.1038/373612a0
[93] Whittington, M.; Traub, R.; Kopell, N., Inhibition-based rhythms: experimental and mathematical observations on network dynamics, Int J Psychophysiol, 38, 3, 315-336 (2000) · doi:10.1016/S0167-8760(00)00173-2
[94] Wilson, HR; Cowan, JD, Excitatory and Inhibitory interactions in localized populations of model neurons, Biophys J, 12, 1, 1-24 (1972) · doi:10.1016/S0006-3495(72)86068-5
[95] Zaitsev, AV; Povysheva, NV; Gonzalez-Burgos, G., Electrophysiological classes of layer 2/3 pyramidal cells in monkey prefrontal cortex, J Neurophysiol, 108, 2, 595-609 (2012) · doi:10.1152/jn.00859.2011
[96] Zimmern, V., Why brain criticality is clinically relevant: a scoping review, Front Neural Circuits, 2, 14 (2020)
This reference list is based on information provided by the publisher or from digital mathematics libraries. Its items are heuristically matched to zbMATH identifiers and may contain data conversion errors. In some cases that data have been complemented/enhanced by data from zbMATH Open. This attempts to reflect the references listed in the original paper as accurately as possible without claiming completeness or a perfect matching.