{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,1]],"date-time":"2026-09-01T11:00:04Z","timestamp":1788260404601,"version":"build-2803163510"},"reference-count":76,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2024,8,30]],"date-time":"2024-08-30T00:00:00Z","timestamp":1724976000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["52307259"],"award-info":[{"award-number":["52307259"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["62201519"],"award-info":[{"award-number":["62201519"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["62327805"],"award-info":[{"award-number":["62327805"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Comput. Neurosci."],"abstract":"<jats:sec><jats:title>Introduction<\/jats:title><jats:p>Electrical stimulation of the brain has shown promising prospects in treating various brain diseases. Although biphasic pulse stimulation remains the predominant clinical approach, there has been increasing interest in exploring alternative stimulation waveforms, such as sinusoidal stimulation, to improve the effectiveness of brain stimulation and to expand its application to a wider range of brain disorders. Despite this growing attention, the effects of sinusoidal stimulation on neurons, especially on their nonlinear firing characteristics, remains unclear.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>To address the question, 50\u2009Hz sinusoidal stimulation was applied on Schaffer collaterals of the rat hippocampal CA1 region <jats:italic>in vivo<\/jats:italic>. Single unit activity of both pyramidal cells and interneurons in the downstream CA1 region was recorded and analyzed. Two fractal indexes, namely the Fano factor and Hurst exponent, were used to evaluate changes in the long-range correlations, a manifestation of nonlinear dynamics, in spike sequences of neuronal firing.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>The results demonstrate that sinusoidal electrical stimulation increased the firing rates of both pyramidal cells and interneurons, as well as altered their firing to stimulation-related patterns. Importantly, the sinusoidal stimulation increased, rather than decreased the scaling exponents of both Fano factor and Hurst exponent, indicating an increase in the long-range correlations of both pyramidal cells and interneurons.<\/jats:p><\/jats:sec><jats:sec><jats:title>Discussion<\/jats:title><jats:p>The results firstly reported that periodic sinusoidal stimulation without long-range correlations can increase the long-range correlations of neurons in the downstream post-synaptic area. These results provide new nonlinear mechanisms of brain sinusoidal stimulation and facilitate the development of new stimulation modes.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fncom.2024.1388224","type":"journal-article","created":{"date-parts":[[2024,8,30]],"date-time":"2024-08-30T04:42:17Z","timestamp":1724992937000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":3,"title":["Nonlinear analysis of neuronal firing modulated by sinusoidal stimulation at axons in rat hippocampus"],"prefix":"10.3389","volume":"18","author":[{"given":"Yue","family":"Yuan","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiangyu","family":"Ye","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jian","family":"Cui","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Junyang","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhaoxiang","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2024,8,30]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"329","DOI":"10.1016\/j.tins.2009.01.009","article-title":"The hippocampal rate code: anatomy, physiology and theory","volume":"32","author":"Ahmed","year":"2009","journal-title":"Trends Neurosci."},{"key":"ref2","volume-title":"The Hippocampus Book","author":"Andersen","year":"2007"},{"key":"ref3","doi-asserted-by":"publisher","first-page":"317","DOI":"10.3389\/fnhum.2013.00317","article-title":"Transcranial alternating current stimulation (tACS)","volume":"7","author":"Antal","year":"2013","journal-title":"Front. Hum. Neurosci."},{"key":"ref4","doi-asserted-by":"publisher","first-page":"5216","DOI":"10.1523\/JNEUROSCI.0540-04.2004","article-title":"Neuronal avalanches are diverse and precise activity patterns that are stable for many hours in cortical slice cultures","volume":"24","author":"Beggs","year":"2004","journal-title":"J. Neurosci."},{"key":"ref5","doi-asserted-by":"publisher","first-page":"263","DOI":"10.1088\/1741-2560\/5\/3\/001","article-title":"Submyelin potassium accumulation may functionally block subsets of local axons during deep brain stimulation: a modeling study","volume":"5","author":"Bellinger","year":"2008","journal-title":"J. Neural Eng."},{"key":"ref6","doi-asserted-by":"publisher","first-page":"1518","DOI":"10.1152\/jn.00198.2020","article-title":"Frequency-dependent spike-pattern changes in motor cortex during thalamic deep brain stimulation","volume":"124","author":"Bello","year":"2020","journal-title":"J. Neurophysiol."},{"key":"ref7","doi-asserted-by":"publisher","first-page":"S440","DOI":"10.1016\/S1353-8020(08)70046-4","article-title":"Stage-dependent patterns of disturbed neural synchrony in Parkinson's disease","volume":"13","author":"Berendse","year":"2007","journal-title":"Parkinsonism Relat. Disord."},{"key":"ref8","doi-asserted-by":"publisher","first-page":"547","DOI":"10.1016\/j.neuroscience.2004.11.013","article-title":"Long-range temporal correlations in the spontaneous spiking of neurons in the hippocampal-amygdala complex of humans","volume":"131","author":"Bhattacharya","year":"2005","journal-title":"Neuroscience"},{"key":"ref9","doi-asserted-by":"publisher","first-page":"181","DOI":"10.1111\/j.1469-7793.2001.0181j.x","article-title":"Suppression of epileptiform activity by high frequency sinusoidal fields in rat hippocampal slices","volume":"531","author":"Bikson","year":"2001","journal-title":"J. Physiol."},{"key":"ref10","doi-asserted-by":"publisher","first-page":"436","DOI":"10.1016\/j.cub.2013.01.068","article-title":"Tremor suppression by rhythmic transcranial current stimulation","volume":"23","author":"Brittain","year":"2013","journal-title":"Curr. Biol."},{"key":"ref11","doi-asserted-by":"publisher","first-page":"205","DOI":"10.1016\/j.chaos.2015.05.026","article-title":"Fractal characterization of acupuncture-induced spike trains of rat WDR neurons","volume":"77","author":"Chen","year":"2015","journal-title":"Chaos, Solitons Fractals"},{"key":"ref12","doi-asserted-by":"publisher","first-page":"84","DOI":"10.1016\/j.brainres.2006.08.027","article-title":"Nonlinear analysis of discharge patterns in monkey basal ganglia","volume":"1118","author":"Darbin","year":"2006","journal-title":"Brain Res."},{"key":"ref13","doi-asserted-by":"publisher","first-page":"833","DOI":"10.1152\/jn.00757.2002","article-title":"Fractal properties of sympathetic nerve discharge","volume":"89","author":"Das","year":"2003","journal-title":"J. Neurophysiol."},{"key":"ref14","doi-asserted-by":"publisher","first-page":"1080","DOI":"10.1111\/j.1460-9568.2010.07413.x","article-title":"Deep brain stimulation mechanisms: beyond the concept of local functional inhibition","volume":"32","author":"Deniau","year":"2010","journal-title":"Eur. J. Neurosci."},{"key":"ref15","doi-asserted-by":"publisher","first-page":"2878","DOI":"10.1016\/j.clinph.2016.05.359","article-title":"Modulation of brain criticality via suppression of EEG long-range temporal correlations (LRTCs) in a closed-loop neurofeedback stimulation","volume":"127","author":"Dimitriadis","year":"2016","journal-title":"Clin. Neurophysiol."},{"key":"ref16","doi-asserted-by":"publisher","first-page":"439","DOI":"10.1016\/0960-0779(93)90029-Z","article-title":"Bifurcations, burstings, chaos and crises in the rose-hindmarsh model for neuronal-activity","volume":"3","author":"Fan","year":"1993","journal-title":"Chaos, Solitons Fractals"},{"key":"ref17","doi-asserted-by":"publisher","first-page":"67","DOI":"10.1016\/j.brainres.2017.02.008","article-title":"High frequency stimulation of afferent fibers generates asynchronous firing in the downstream neurons in hippocampus through partial block of axonal conduction","volume":"1661","author":"Feng","year":"2017","journal-title":"Brain Res."},{"key":"ref18","first-page":"351","article-title":"Selection of filtering frequencies for neuronal spike signals","volume":"46","author":"Feng","year":"2012","journal-title":"J. Zhejiang Univ."},{"key":"ref19","doi-asserted-by":"publisher","first-page":"32","DOI":"10.1016\/j.brainres.2013.02.048","article-title":"Functional disconnection of axonal fibers generated by high frequency stimulation in the hippocampal CA1 region in-vivo","volume":"1509","author":"Feng","year":"2013","journal-title":"Brain Res."},{"key":"ref20","doi-asserted-by":"crossref","DOI":"10.1201\/9781003479970-10","article-title":"Detecting dementia using EEG signal processing and machine learning","volume-title":"Artificial Intelligence Enabled Signal Processing Based Models for Neural Information Processing","author":"Ferdowsi","year":"2024"},{"key":"ref21","doi-asserted-by":"publisher","first-page":"261","DOI":"10.1038\/nrneurol.2014.59","article-title":"Electrical brain stimulation for epilepsy","volume":"10","author":"Fisher","year":"2014","journal-title":"Nat. Rev. Neurol."},{"key":"ref22","doi-asserted-by":"publisher","first-page":"066008","DOI":"10.1088\/1741-2560\/7\/6\/066008","article-title":"Evaluation of novel stimulus waveforms for deep brain stimulation","volume":"7","author":"Foutz","year":"2010","journal-title":"J. Neural Eng."},{"key":"ref23","doi-asserted-by":"publisher","first-page":"7255","DOI":"10.1523\/JNEUROSCI.23-19-07255.2003","article-title":"Sensitivity of neurons to weak electric fields","volume":"23","author":"Francis","year":"2003","journal-title":"J. Neurosci."},{"key":"ref24","doi-asserted-by":"publisher","first-page":"1176","DOI":"10.1152\/jn.01021.2005","article-title":"Fractal noises and motions in time series of presympathetic and sympathetic neural activities","volume":"95","author":"Gebber","year":"2006","journal-title":"J. Neurophysiol."},{"key":"ref25","doi-asserted-by":"publisher","first-page":"1312","DOI":"10.1016\/S0140-6736(96)90948-4","article-title":"Non-linear dynamics for clinicians: Chaos theory, fractals, and complexity at the bedside","volume":"347","author":"Goldberger","year":"1996","journal-title":"Lancet"},{"key":"ref26","doi-asserted-by":"publisher","first-page":"2466","DOI":"10.1073\/pnas.012579499","article-title":"Fractal dynamics in physiology: alterations with disease and aging","volume":"99","author":"Goldberger","year":"2002","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref27","doi-asserted-by":"publisher","first-page":"858","DOI":"10.3389\/fnins.2018.00858","article-title":"Simulation study of intermittent axonal block and desynchronization effect induced by high-frequency stimulation of electrical pulses","volume":"12","author":"Guo","year":"2018","journal-title":"Front. Neurosci."},{"key":"ref28","doi-asserted-by":"publisher","first-page":"5817","DOI":"10.1109\/EMBC.2016.7592050","article-title":"Sinusoidal stimulation trains suppress epileptiform spikes induced by 4-AP in the rat hippocampal CA1 region in-vivo","author":"Guo","year":"2016","journal-title":"Annu. Int. Conf. IEEE Eng. Med. Biol. Soc."},{"key":"ref29","doi-asserted-by":"publisher","first-page":"500","DOI":"10.1113\/jphysiol.1952.sp004764","article-title":"A quantitative description of membrane current and its application to conduction and excitation in nerve","volume":"117","author":"Hodgkin","year":"1952","journal-title":"J. Physiol."},{"key":"ref30","doi-asserted-by":"publisher","first-page":"751","DOI":"10.1097\/WNR.0b013e328364c1a1","article-title":"Modulation of cortical neural dynamics during thalamic deep brain stimulation in patients with essential tremor","volume":"24","author":"Hohlefeld","year":"2013","journal-title":"Neuroreport"},{"key":"ref31","doi-asserted-by":"publisher","first-page":"2812","DOI":"10.1111\/j.1460-9568.2012.08198.x","article-title":"Long-range temporal correlations in the subthalamic nucleus of patients with Parkinson's disease","volume":"36","author":"Hohlefeld","year":"2012","journal-title":"Eur. J. Neurosci."},{"key":"ref32","doi-asserted-by":"publisher","first-page":"770","DOI":"10.1061\/TACEAT.0006518","article-title":"Long-term storage capacity of reservoirs","volume":"116","author":"Hurst","year":"1951","journal-title":"Trans Am Soc Civil Eng"},{"key":"ref33","doi-asserted-by":"publisher","first-page":"2125","DOI":"10.1162\/0899766041732413","article-title":"Including long-range dependence in integrate-and-fire models of the high interspike-interval variability of cortical neurons","volume":"16","author":"Jackson","year":"2004","journal-title":"Neural Comput."},{"key":"ref34","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1088\/1741-2560\/4\/2\/001","article-title":"Suppression of axonal conduction by sinusoidal stimulation in rat hippocampus in vitro","volume":"4","author":"Jensen","year":"2007","journal-title":"J. Neural Eng."},{"key":"ref35","doi-asserted-by":"publisher","first-page":"223","DOI":"10.1016\/j.tics.2010.02.005","article-title":"Scaling laws in cognitive sciences","volume":"14","author":"Kello","year":"2010","journal-title":"Trends Cogn. Sci."},{"key":"ref36","doi-asserted-by":"publisher","first-page":"242","DOI":"10.1111\/ner.12100","article-title":"Reversible nerve conduction block using kilohertz frequency alternating current","volume":"17","author":"Kilgore","year":"2014","journal-title":"Neuromodulation"},{"key":"ref37","doi-asserted-by":"publisher","first-page":"1965","DOI":"10.1152\/jn.00276.2011","article-title":"Decreased afferent excitability contributes to synaptic depression during high-frequency stimulation in hippocampal area CA1","volume":"108","author":"Kim","year":"2012","journal-title":"J. Neurophysiol."},{"key":"ref38","doi-asserted-by":"publisher","first-page":"2435","DOI":"10.1152\/jn.2001.86.5.2435","article-title":"Apical and basal orthodromic population spikes in hippocampal CA1 in vivo show different origins and patterns of propagation","volume":"86","author":"Kloosterman","year":"2001","journal-title":"J. Neurophysiol."},{"key":"ref39","doi-asserted-by":"publisher","first-page":"75","DOI":"10.1038\/s41582-020-00426-z","article-title":"Technology of deep brain stimulation: current status and future directions","volume":"17","author":"Krauss","year":"2021","journal-title":"Nat. Rev. Neurol."},{"key":"ref40","doi-asserted-by":"publisher","first-page":"44","DOI":"10.3389\/fncel.2015.00044","article-title":"A pre-docking source for the power-law behavior of spontaneous quantal release: application to the analysis of LTP","volume":"9","author":"Lamanna","year":"2015","journal-title":"Front. Cell. Neurosci."},{"key":"ref41","doi-asserted-by":"publisher","first-page":"427","DOI":"10.1113\/jphysiol.2002.033209","article-title":"Local suppression of epileptiform activity by electrical stimulation in rat hippocampus in vitro","volume":"547","author":"Lian","year":"2003","journal-title":"J. Physiol."},{"key":"ref42","doi-asserted-by":"publisher","first-page":"1511","DOI":"10.3389\/fphys.2018.01511","article-title":"Long-range temporal correlations of patients in minimally conscious state modulated by spinal cord stimulation","volume":"9","author":"Liang","year":"2018","journal-title":"Front. Physiol."},{"key":"ref43","doi-asserted-by":"publisher","first-page":"517","DOI":"10.1007\/BF02368171","article-title":"A model of ion channel kinetics based on deterministic, chaotic motion in a potential with 2 local minima","volume":"20","author":"Liebovitch","year":"1992","journal-title":"Ann. Biomed. Eng."},{"key":"ref44","doi-asserted-by":"publisher","first-page":"3590","DOI":"10.1109\/EMBC.2013.6610319","article-title":"Effects of low amplitude pulsed radiofrequency stimulation with different waveform in rats for neuropathic pain","volume":"2013","author":"Lin","year":"2013","journal-title":"Annu. Int. Conf. IEEE Eng. Med. Biol. Soc."},{"key":"ref45","doi-asserted-by":"publisher","first-page":"203","DOI":"10.1111\/j.1460-9568.2004.03116.x","article-title":"Stimulus-induced change in long-range temporal correlations and scaling behaviour of sensorimotor oscillations","volume":"19","author":"Linkenkaer-Hansen","year":"2004","journal-title":"Eur. J. Neurosci."},{"key":"ref46","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1155\/2021\/6632394","article-title":"Galvanic vestibular stimulation improves subnetwork interactions in Parkinson\u2019s disease","volume":"2021","author":"Liu","year":"2021","journal-title":"J. Healthcare Eng."},{"key":"ref47","doi-asserted-by":"publisher","first-page":"1649","DOI":"10.1109\/TNSRE.2018.2853118","article-title":"Mathematical modeling for description of oscillation suppression induced by deep brain stimulation","volume":"26","author":"Liu","year":"2018","journal-title":"IEEE Trans. Neural Syst. Rehabil. Eng."},{"key":"ref48","doi-asserted-by":"publisher","first-page":"5970","DOI":"10.1103\/PhysRevE.59.5970","article-title":"Fractal ion-channel behavior generates fractal firing patterns in neuronal models","volume":"59","author":"Lowen","year":"1999","journal-title":"Phys. Rev. E"},{"key":"ref49","doi-asserted-by":"publisher","first-page":"377","DOI":"10.1006\/meth.2001.1207","article-title":"Fractal features of dark, maintained, and driven neural discharges in the cat visual system","volume":"24","author":"Lowen","year":"2001","journal-title":"Methods"},{"key":"ref50","doi-asserted-by":"publisher","first-page":"148","DOI":"10.1038\/s41582-018-0128-2","article-title":"Deep brain stimulation: current challenges and future directions","volume":"15","author":"Lozano","year":"2019","journal-title":"Nat. Rev. Neurol."},{"key":"ref51","volume-title":"The Fractal Geometry of Nature","author":"Mandelbrot","year":"1982"},{"key":"ref52","doi-asserted-by":"publisher","first-page":"584","DOI":"10.1055\/s-0034-1396011","article-title":"Closed-loop rehabilitation of age-related cognitive disorders","volume":"34","author":"Mishra","year":"2014","journal-title":"Semin. Neurol."},{"key":"ref53","doi-asserted-by":"publisher","first-page":"1614","DOI":"10.1073\/pnas.0811699106","article-title":"Altered temporal correlations in parietal alpha and prefrontal theta oscillations in early-stage Alzheimer disease","volume":"106","author":"Montez","year":"2009","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref54","doi-asserted-by":"publisher","first-page":"1386","DOI":"10.1093\/cercor\/bhl049","article-title":"Epileptogenic neocortical networks are revealed by abnormal temporal dynamics in seizure-free subdural EEG","volume":"17","author":"Monto","year":"2007","journal-title":"Cereb. Cortex"},{"key":"ref55","doi-asserted-by":"publisher","first-page":"561008","DOI":"10.3389\/fnins.2020.561008","article-title":"Systematic evaluation of DBS parameters in the hemi-parkinsonian rat model","volume":"14","author":"Mottaghi","year":"2020","journal-title":"Front. Neurosci."},{"key":"ref56","doi-asserted-by":"publisher","first-page":"1551","DOI":"10.1113\/JP278935","article-title":"Fractal spike dynamics and neuronal coupling in the primate visual system","volume":"598","author":"Munn","year":"2020","journal-title":"J. Physiol."},{"key":"ref57","doi-asserted-by":"publisher","first-page":"7","DOI":"10.1186\/1475-925X-3-7","article-title":"Nonlinear analysis of EEG signals at different mental states","volume":"3","author":"Natarajan","year":"2004","journal-title":"Biomed. Eng. Online"},{"key":"ref58","doi-asserted-by":"publisher","first-page":"162","DOI":"10.1016\/j.neuroimage.2012.03.008","article-title":"Attenuation of long-range temporal correlations in the amplitude dynamics of alpha and beta neuronal oscillations in patients with schizophrenia","volume":"61","author":"Nikulin","year":"2012","journal-title":"NeuroImage"},{"key":"ref59","doi-asserted-by":"publisher","first-page":"6","DOI":"10.1186\/1753-4631-3-6","article-title":"Comparative study of nonlinear properties of EEG signals of normal persons and epileptic patients","volume":"3","author":"Nurujjaman","year":"2009","journal-title":"Nonlinear Biomed. Phys."},{"key":"ref60","doi-asserted-by":"publisher","first-page":"167","DOI":"10.1007\/s00221-003-1442-4","article-title":"Neuronal activity in the substantia nigra in the anaesthetized rat has fractal characteristics. Evidence for firing-code patterns in the basal ganglia","volume":"151","author":"Rodriguez","year":"2003","journal-title":"Exp. Brain Res."},{"key":"ref61","doi-asserted-by":"publisher","first-page":"86","DOI":"10.1016\/j.nbd.2013.09.006","article-title":"Axonal and synaptic failure suppress the transfer of firing rate oscillations, synchrony and information during high frequency deep brain stimulation","volume":"62","author":"Rosenbaum","year":"2014","journal-title":"Neurobiol. Dis."},{"key":"ref62","doi-asserted-by":"publisher","first-page":"666","DOI":"10.1093\/bja\/82.5.666","article-title":"Comparison of bispectral index, 95% spectral edge frequency and approximate entropy of the EEG, with changes in heart rate variability during induction of general anaesthesia","volume":"82","author":"Sleigh","year":"1999","journal-title":"Br. J. Anaesth."},{"key":"ref63","doi-asserted-by":"publisher","first-page":"810","DOI":"10.1007\/s10548-017-0588-5","article-title":"Long-range temporal correlations reflect treatment response in the electroencephalogram of patients with infantile spasms","volume":"30","author":"Smith","year":"2017","journal-title":"Brain Topogr."},{"key":"ref64","doi-asserted-by":"publisher","first-page":"197","DOI":"10.1111\/ner.12266","article-title":"High-frequency electrical nerve block for postamputation pain: a pilot study","volume":"18","author":"Soin","year":"2015","journal-title":"Neuromodulation"},{"key":"ref65","doi-asserted-by":"publisher","first-page":"147875","DOI":"10.1016\/j.brainres.2022.147875","article-title":"The visual cortical responses to sinusoidal transcorneal electrical stimulation","volume":"1785","author":"Su","year":"2022","journal-title":"Brain Res."},{"key":"ref66","doi-asserted-by":"publisher","first-page":"150","DOI":"10.1109\/10.16460","article-title":"Fractal character of the auditory neural spike train","volume":"36","author":"Teich","year":"1989","journal-title":"IEEE Trans. Biomed. Eng."},{"key":"ref67","doi-asserted-by":"publisher","first-page":"529","DOI":"10.1364\/JOSAA.14.000529","article-title":"Fractal character of the neural spike train in the visual system of the cat","volume":"14","author":"Teich","year":"1997","journal-title":"J. Opt. Soc. Am. A Opt. Image Sci. Vis."},{"key":"ref68","doi-asserted-by":"publisher","first-page":"413","DOI":"10.1109\/TNSRE.2015.2415811","article-title":"The retinal response to sinusoidal electrical stimulation","volume":"24","author":"Twyford","year":"2016","journal-title":"IEEE Trans. Neural Syst. Rehabil. Eng."},{"key":"ref69","doi-asserted-by":"publisher","first-page":"3805","DOI":"10.1103\/PhysRevLett.68.3805","article-title":"Evolution of long-range fractal correlations and 1\/f noise in DNA base sequences","volume":"68","author":"Voss","year":"1992","journal-title":"Phys. Rev. Lett."},{"key":"ref70","doi-asserted-by":"publisher","first-page":"413","DOI":"10.31083\/j.jin.2020.03.207","article-title":"Sinusoidal stimulation on afferent fibers modulates the firing pattern of downstream neurons in rat hippocampus","volume":"19","author":"Wang","year":"2020","journal-title":"J. Integr. Neurosci."},{"key":"ref71","doi-asserted-by":"crossref","DOI":"10.1201\/9781003479970-11","article-title":"EEG signal processing-driven machine learning for cognitive task recognition","volume-title":"Artificial Intelligence Enabled Signal Processing Based Models for Neural Information Processing","author":"Wang","year":"2024"},{"key":"ref72","doi-asserted-by":"crossref","DOI":"10.1142\/8577","volume-title":"Fractal Physiology and Chaos in Medicine","author":"West","year":"2013"},{"key":"ref73","doi-asserted-by":"publisher","first-page":"312","DOI":"10.1111\/ner.12011","article-title":"Block of peripheral pain response by high-frequency sinusoidal stimulation","volume":"16","author":"Wodlinger","year":"2013","journal-title":"Neuromodulation"},{"key":"ref74","doi-asserted-by":"publisher","first-page":"e2105795118","DOI":"10.1073\/pnas.2105795118","article-title":"Interactions among diameter, myelination, and the Na\/K pump affect axonal resilience to high-frequency spiking","volume":"118","author":"Zang","year":"2021","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref75","doi-asserted-by":"publisher","first-page":"1818","DOI":"10.1016\/j.cub.2023.03.043","article-title":"Sodium channel slow inactivation normalizes firing in axons with uneven conductance distributions","volume":"33","author":"Zang","year":"2023","journal-title":"Curr. Biol."},{"key":"ref76","doi-asserted-by":"publisher","first-page":"2882","DOI":"10.1016\/j.clinph.2016.04.028","article-title":"Modulation of critical brain dynamics using closed-loop neurofeedback stimulation","volume":"127","author":"Zhigalov","year":"2016","journal-title":"Clin. Neurophysiol."}],"container-title":["Frontiers in Computational Neuroscience"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fncom.2024.1388224\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,8,30]],"date-time":"2024-08-30T04:42:25Z","timestamp":1724992945000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fncom.2024.1388224\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,8,30]]},"references-count":76,"alternative-id":["10.3389\/fncom.2024.1388224"],"URL":"https:\/\/doi.org\/10.3389\/fncom.2024.1388224","relation":{},"ISSN":["1662-5188"],"issn-type":[{"value":"1662-5188","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,8,30]]},"article-number":"1388224"}}