Thermal effects and ephaptic entrainment in Hodgkin-Huxley model.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
29 Aug 2024
29 Aug 2024
Historique:
received:
01
04
2024
accepted:
20
08
2024
medline:
31
8
2024
pubmed:
31
8
2024
entrez:
29
8
2024
Statut:
epublish
Résumé
The brain is understood as an intricate biological system composed of numerous elements. It is susceptible to various physical and chemical influences, including temperature. The literature extensively explores the conditions that influence synapses in the context of cellular communication. However, the understanding of how the brain's global physical conditions can modulate ephaptic communication remains limited due to the poorly understood nature of ephapticity. This study proposes an adaptation of the Hodgkin and Huxley (HH) model to investigate the effects of ephaptic entrainment in response to thermal changes (HH-E). The analysis focuses on two distinct neuronal regimes: subthreshold and suprathreshold. In the subthreshold regime, circular statistics are used to demonstrate the dependence of phase differences with temperature. In the suprathreshold regime, the Inter-Spike Interval are employed to estimate phase preferences and changes in the spiking pattern. Temperature influences the model's ephaptic interactions and can modify its preferences for spiking frequency, with the direction of this change depending on specific model conditions and the temperature range under consideration. Furthermore, temperature enhance the anti-phase differences relationship between spikes and the external ephaptic signal. In the suprathreshold regime, ephaptic entrainment is also influenced by temperature, especially at low frequencies. This study reveals the susceptibility of ephaptic entrainment to temperature variations in both subthreshold and suprathreshold regimes and discusses the importance of ephaptic communication in the contexts where temperature may plays a significant role in neural physiology, such as inflammatory processes, fever, and epileptic seizures.
Identifiants
pubmed: 39209942
doi: 10.1038/s41598-024-70655-5
pii: 10.1038/s41598-024-70655-5
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
20075Subventions
Organisme : Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
ID : #88887.900715/2023-00
Organisme : Conselho Nacional de Desenvolvimento Científico e Tecnológico
ID : #140895/2021-3
Organisme : Conselho Nacional de Desenvolvimento Científico e Tecnológico
ID : #309440/2022-0
Informations de copyright
© 2024. The Author(s).
Références
Park, K. S. Nervous system. In Humans and Electricity: Understanding Body Electricity and Applications, pp. 27–51 (Springer, 2023).
Studer-Luethi, B., Jaeggi, S. M., Buschkuehl, M. & Perrig, W. J. Influence of neuroticism and conscientiousness on working memory training outcome. Pers. Individ. Differ. 53, 44–49 (2012).
doi: 10.1016/j.paid.2012.02.012
Gathercole, S. E. The development of memory. J. Child Psychol. Psychiatry Allied Discip. 39, 3–27 (1998).
doi: 10.1111/1469-7610.00301
Kandel, E. R. et al. Principles of neural science Vol. 4 (McGraw-hill, New York, 2000).
dos Santos Lima, G. Z. et al. Hippocampal and cortical communication around micro-arousals in slow-wave sleep. Sci. Rep. 9, 5876 (2019).
pubmed: 30971751
pmcid: 6458146
doi: 10.1038/s41598-019-42100-5
Lima, G. D. S. et al. Mouse activity across time scales: Fractal scenarios. PLoS ONE 9, e105092 (2014).
pubmed: 25275515
pmcid: 4183474
doi: 10.1371/journal.pone.0105092
Katz & Schmitt. Eletric interaction between two adjacent nerve fibers. J. Physiol. 471–488 (1940).
Arvanitaky. Effects evoked in an axon by the activity of a contiguous one. J. Physiol. 91–108 (1942).
Hunt, T. & Jones, M. Fields or firings? Comparing the spike code and the electromagnetic field hypothesis. Front. Psychol. 14 (2023).
Anastassiou, C. A., Perin, R., Markram, H. & Koch, C. Ephaptic coupling of cortical neurons. Nat. Neurosci. 14, 217–223 (2011).
pubmed: 21240273
doi: 10.1038/nn.2727
Cunha, G. M., Corso, G., Miranda, J. G. V. & Dos Santos Lima, G. Z. Ephaptic entrainment in hybrid neuronal model. Sci. Rep. 12, 1–10 (2022).
doi: 10.1038/s41598-022-05343-3
Jefferys, J. Nonsynaptic modulation of neuronal activity in the brain: Electric currents and extracellular ions. Physiol. Rev. 75, 689–723 (1995).
pubmed: 7480159
doi: 10.1152/physrev.1995.75.4.689
Francis, J. T., Gluckman, B. J. & Schiff, S. J. Sensitivity of neurons to weak electric fields. J. Neurosci. 23, 7255–7261 (2003).
pubmed: 12917358
pmcid: 6740448
doi: 10.1523/JNEUROSCI.23-19-07255.2003
Qiu, C., Shivacharan, R. S., Zhang, M. & Durand, D. M. Can neural activity propagate by endogenous electrical field?. J. Neurosci. 35, 15800–15811 (2015).
pubmed: 26631463
pmcid: 4666910
doi: 10.1523/JNEUROSCI.1045-15.2015
Fröhlich, F. & McCormick, D. A. Endogenous electric fields may guide neocortical network activity. Neuron 67, 129–143 (2010).
pubmed: 20624597
pmcid: 3139922
doi: 10.1016/j.neuron.2010.06.005
Anastassiou, C. A. & Koch, C. Ephaptic coupling to endogenous electric field activity: Why bother?. Curr. Opin. Neurobiol. 31, 95–103 (2015).
pubmed: 25265066
doi: 10.1016/j.conb.2014.09.002
Pinotsis, D. A. & Miller, E. K. In vivo ephaptic coupling allows memory network formation. Cereb. Cortex 33, 9877–9895 (2023).
pubmed: 37420330
pmcid: 10472500
doi: 10.1093/cercor/bhad251
Bassett, D. S., Brown, J. A., Deshpande, V., Carlson, J. M. & Grafton, S. T. Conserved and variable architecture of human white matter connectivity. Neuroimage 54, 1262–1279 (2011).
pubmed: 20850551
doi: 10.1016/j.neuroimage.2010.09.006
Han, K.-S. et al. Ephaptic coupling promotes synchronous firing of cerebellar purkinje cells. Neuron 100, 564–578 (2018).
pubmed: 30293822
pmcid: 7513896
doi: 10.1016/j.neuron.2018.09.018
Queenan, B. N., Ryan, T. J., Gazzaniga, M. S. & Gallistel, C. R. On the research of time past: The hunt for the substrate of memory. Ann. N. Y. Acad. Sci. 1396, 108–125 (2017).
pubmed: 28548457
pmcid: 5448307
doi: 10.1111/nyas.13348
Hedrick, T. & Waters, J. Effect of temperature on spiking patterns of neocortical layer 2/3 and layer 6 pyramidal neurons. Front. Neural Circ. 6, 28 (2012).
Yu, Y., Hill, A. P. & McCormick, D. A. Warm body temperature facilitates energy efficient cortical action potentials. PLoS Comput. Biol. 8, e1002456 (2012).
pubmed: 22511855
pmcid: 3325181
doi: 10.1371/journal.pcbi.1002456
Burek, M., Follmann, R. & Rosa, E. Temperature effects on neuronal firing rates and tonic-to-bursting transitions. Biosystems 180, 1–6 (2019).
pubmed: 30862447
doi: 10.1016/j.biosystems.2019.03.003
Hodgkin, A. L. & Huxley, A. F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. 117, 500 (1952).
pubmed: 12991237
pmcid: 1392413
doi: 10.1113/jphysiol.1952.sp004764
Moore, J. Temperature and drug effects on squid axon membrane ion conductances. In Federation proceedings, pp. 113 (Federation Amer Soc Exp Biol 9650 Rockville pike, Bethesda, MD 20814-3998, 1958).
Cao, X.-J. & Oertel, D. Temperature affects voltage-sensitive conductances differentially in octopus cells of the mammalian cochlear nucleus. J. Neurophysiol. 94, 821–832 (2005).
pubmed: 15800074
doi: 10.1152/jn.01049.2004
Forrest, M. D. Can the thermodynamic Hodgkin–Huxley model of voltage-dependent conductance extrapolate for temperature?. Computation 2, 47–60 (2014).
doi: 10.3390/computation2020047
Tiwari, J. & Sikdar, S. Temperature-dependent conformational changes in a voltage-gated potassium channel. Eur. Biophys. J. 28, 338–345 (1999).
pubmed: 10394625
doi: 10.1007/s002490050216
Carpenter, D. O. Temperature effects on pacemaker generation, membrane potential, and critical firing threshold in aplysia neurons. J. Gen. Physiol. 50, 1469–1484 (1967).
pubmed: 6034753
pmcid: 2225722
doi: 10.1085/jgp.50.6.1469
Ishiko, N. & Loewenstein, W. R. Effects of temperature on the generator and action potentials of a sense organ. J. Gen. Physiol. 45, 105–124 (1961).
pubmed: 13718006
pmcid: 2195154
doi: 10.1085/jgp.45.1.105
Ritchie, M. E. Reaction and diffusion thermodynamics explain optimal temperatures of biochemical reactions. Sci. Rep. 8, 11105 (2018).
pubmed: 30038415
pmcid: 6056565
doi: 10.1038/s41598-018-28833-9
Rodríguez, B. M., Sigg, D. & Bezanilla, F. Voltage gating of shaker k+ channels: The effect of temperature on ionic and gating currents. J. Gen. Physiol. 112, 223–242 (1998).
pubmed: 9689029
pmcid: 2525751
doi: 10.1085/jgp.112.2.223
Liang, S. et al. Temperature-dependent activation of neurons by continuous near-infrared laser. Cell Biochem. Biophys. 53, 33–42 (2009).
pubmed: 19034696
doi: 10.1007/s12013-008-9035-2
Hodgkin, A. L. & Huxley, A. F. Currents carried by sodium and potassium ions through the membrane of the giant axon of loligo. J. Physiol. 116, 449–472 (1952).
pubmed: 14946713
pmcid: 1392213
doi: 10.1113/jphysiol.1952.sp004717
Sjodin, R. & Mullins, L. Oscillatory behavior of the squid axon membrane potential. J. Gen. Physiol. 42, 39–47 (1958).
pubmed: 13575773
pmcid: 2194897
doi: 10.1085/jgp.42.1.39
Guttman, R. & with the technical assistance of Robert Barnhill. Temperature characteristics of excitation in space-clamped squid axons. J. Gen. Physiol. 49, 1007–1018 (1966).
Hodgkin, A. & Huxley, A. Current and its application to conduction. J. Physiol. 117, 500–544 (1952).
pubmed: 12991237
pmcid: 1392413
doi: 10.1113/jphysiol.1952.sp004764
Anastassiou, C. A., Perin, R., Markram, H. & Koch, C. Ephaptic coupling of cortical neurons. Nat. Neurosci. 14, 217 (2011).
pubmed: 21240273
doi: 10.1038/nn.2727
Robertson, R. M. & Money, T. G. Temperature and neuronal circuit function: Compensation, tuning and tolerance. Curr. Opin. Neurobiol. 22, 724–734 (2012).
pubmed: 22326854
doi: 10.1016/j.conb.2012.01.008
Peleg, M., Normand, M. D. & Corradini, M. G. The arrhenius equation revisited. Crit. Rev. Food Sci. Nutr. 52, 830–851 (2012).
pubmed: 22698273
doi: 10.1080/10408398.2012.667460
Hodgkin, A. L. & Huxley, A. F. The components of membrane conductance in the giant axon of loligo. J. Physiol. 116, 473–496 (1952).
pubmed: 14946714
pmcid: 1392209
doi: 10.1113/jphysiol.1952.sp004718
Hodgkin, A. L., Huxley, A. F. & Katz, B. Measurement of current-voltage relations in the membrane of the giant axon of loligo. J. Physiol. 116, 424–448 (1952).
pubmed: 14946712
pmcid: 1392219
doi: 10.1113/jphysiol.1952.sp004716
Izhikevich, E. M. Dynamical systems in neuroscience (MIT press, London, 2007).
Han, K.-S. et al. Ephaptic coupling promotes synchronous firing of cerebellar purkinje cells. Neuron 100, 564–578 (2018).
pubmed: 30293822
pmcid: 7513896
doi: 10.1016/j.neuron.2018.09.018
Schmidt, H., Hahn, G., Deco, G. & Knösche, T. R. Ephaptic coupling in white matter fibre bundles modulates axonal transmission delays. PLoS Comput. Biol. 17, e1007858 (2021).
pubmed: 33556058
pmcid: 7895385
doi: 10.1371/journal.pcbi.1007858
Cunha, G. M., Corso, G., Lima, M. M. & dos Santos Lima, G. Z. Electrophysiological damage to neuronal membrane alters ephaptic entrainment. Sci. Rep. 13, 11974 (2023).
pubmed: 37488148
pmcid: 10366241
doi: 10.1038/s41598-023-38738-x
Binczak, S., Eilbeck, J. & Scott, A. C. Ephaptic coupling of myelinated nerve fibers. Phys. D 148, 159–174 (2001).
doi: 10.1016/S0167-2789(00)00173-1
Holt, G. R. & Koch, C. Electrical interactions via the extracellular potential near cell bodies. J. Comput. Neurosci. 6, 169–184 (1999).
pubmed: 10333161
doi: 10.1023/A:1008832702585
Goldwyn, J. H. & Rinzel, J. Neuronal coupling by endogenous electric fields: cable theory and applications to coincidence detector neurons in the auditory brain stem. J. Neurophysiol. 115, 2033–2051 (2016).
pubmed: 26823512
pmcid: 4869512
doi: 10.1152/jn.00780.2015
Mechler, F. & Victor, J. D. Dipole characterization of single neurons from their extracellular action potentials. J. Comput. Neurosci. 32, 73–100 (2012).
pubmed: 21667156
doi: 10.1007/s10827-011-0341-0
Hodgkin, A. & Katz, B. The effect of temperature on the electrical activity of the giant axon of the squid. J. Physiol. 109, 240 (1949).
pubmed: 15394322
pmcid: 1392577
doi: 10.1113/jphysiol.1949.sp004388
Fohlmeister, J. F. Voltage gating by molecular subunits of na+ and k+ ion channels: higher-dimensional cubic kinetics, rate constants, and temperature. J. Neurophysiol. 113, 3759–3777 (2015).
pubmed: 25867741
pmcid: 4468971
doi: 10.1152/jn.00551.2014
Rosen, A. D. Nonlinear temperature modulation of sodium channel kinetics in gh3 cells. Biochim. Biophys. Acta (BBA) Biomembranes 1511, 391–396. https://doi.org/10.1016/S0005-2736(01)00301-7 (2001).
doi: 10.1016/S0005-2736(01)00301-7
pubmed: 11286982
Pahlavan, B., Buitrago, N. & Santamaria, F. Macromolecular rate theory explains the temperature dependence of membrane conductance kinetics. Biophys. J . 122, 522–532 (2023).
pubmed: 36567527
doi: 10.1016/j.bpj.2022.12.033
Arrhenius, S. Über die dissociationswärme und den einfluss der temperatur auf den dissociationsgrad der elektrolyte. Z. Phys. Chem. 4, 96–116 (1889).
doi: 10.1515/zpch-1889-0408
Laidler, K. J. & King, M. C. The development of transition-state theory. J. Phys. Chem. 87, 2657–2664 (1983).
doi: 10.1021/j100238a002
Mardia, K. V. Statistics of directional data (Academic press, USA, 1972).
Berens, P. et al. Circstat: A matlab toolbox for circular statistics. J. Stat. Softw. 31, 1–21 (2009).
doi: 10.18637/jss.v031.i10
Georgopoulos, A. P., Kalaska, J. F., Caminiti, R. & Massey, J. T. On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex. J. Neurosci. 2, 1527–1537 (1982).
pubmed: 7143039
pmcid: 6564361
doi: 10.1523/JNEUROSCI.02-11-01527.1982
Georgopoulos, A. P., Schwartz, A. B. & Kettner, R. E. Neuronal population coding of movement direction. Science 233, 1416–1419 (1986).
pubmed: 3749885
doi: 10.1126/science.3749885
Oppenheim, A. V. Discrete-time signal processing (Pearson Education, India, 1999).
Dayan, P. & Abbott, L. F. Theoretical neuroscience: Computational and mathematical modeling of neural systems (MIT press, London, 2005).
Takens, F. Detecting strange attractors in turbulence. In Dynamical Systems and Turbulence, Warwick 1980: proceedings of a symposium held at the University of Warwick 1979/80, pp. 366–381 (Springer, 2006).
Sauer, T. Interspike interval embedding of chaotic signals. Chaos Interdiscip. J. Nonlinear Sci. 5, 127–132 (1995).
doi: 10.1063/1.166094
Snider, R., Kabara, J., Roig, B. & Bonds, A. Burst firing and modulation of functional connectivity in cat striate cortex. J. Neurophysiol. 80, 730–744 (1998).
pubmed: 9705464
doi: 10.1152/jn.1998.80.2.730
Reich, D. S., Mechler, F., Purpura, K. P. & Victor, J. D. Interspike intervals, receptive fields, and information encoding in primary visual cortex. J. Neurosci. 20, 1964–1974 (2000).
pubmed: 10684897
pmcid: 6772912
doi: 10.1523/JNEUROSCI.20-05-01964.2000
Kim, Y. & Panda, P. Visual explanations from spiking neural networks using inter-spike intervals. Sci. Rep. 11, 19037 (2021).
pubmed: 34561513
pmcid: 8463578
doi: 10.1038/s41598-021-98448-0
Thompson, S. M., Masukawa, L. M. & Prince, D. A. Temperature dependence of intrinsic membrane properties and synaptic potentials in hippocampal ca1 neurons in vitro. J. Neurosci. 5, 817–824 (1985).
pubmed: 3973697
pmcid: 6565032
doi: 10.1523/JNEUROSCI.05-03-00817.1985
Ito, E., Ikemoto, Y. & Yoshioka, T. Thermodynamic implications of high q10 of thermotrp channels in living cells. Biophysics 11, 33–38 (2015).
pubmed: 27493512
pmcid: 4736789
doi: 10.2142/biophysics.11.33
Patapoutian, A., Peier, A. M., Story, G. M. & Viswanath, V. Thermotrp channels and beyond: mechanisms of temperature sensation. Nat. Rev. Neurosci. 4, 529–539 (2003).
pubmed: 12838328
doi: 10.1038/nrn1141
Kashio, M. & Tominaga, M. Trp channels in thermosensation. Curr. Opin. Neurobiol. 75, 102591 (2022).
pubmed: 35728275
doi: 10.1016/j.conb.2022.102591
Avila, J., Lucas, J. J., Perez, M. & Hernandez, F. Role of tau protein in both physiological and pathological conditions. Physiol. Rev. (2004).
dos Santos Lima, G. Z. et al. Disruption of neocortical synchronisation during slow-wave sleep in the rotenone model of Parkinson’s disease. J. Sleep Res. e13170 (2020).
Lima, M. M., Targa, A. D., dos Santos Lima, G. Z., Cavarsan, C. F. & Torterolo, P. Macro and micro-sleep dysfunctions as translational biomarkers for parkinson’s disease. Int. Rev. Neurobiol. (2023).
Kandel, E. R. & al. et. Princípios de Neurociências (artmed, Porto Alegre, 2014), 5 edn.
Ruffini, G. et al. Realistic modeling of mesoscopic ephaptic coupling in the human brain. PLoS Comput. Biol. 16, e1007923 (2020).
pubmed: 32479496
pmcid: 7289436
doi: 10.1371/journal.pcbi.1007923
Vroman, R., Klaassen, L. J. & Kamermans, M. Ephaptic communication in the vertebrate retina. Front. Hum. Neurosci. 7, 612 (2013).
pubmed: 24068997
pmcid: 3780359
doi: 10.3389/fnhum.2013.00612