Axons, but not cell bodies, are activated by electrical stimulation in cortical gray matter

Nowak, L. G.; Bullier, J.

doi:10.1007/s002210050304

Cited by 492Neuroscience and Neuropharmacology ResearchNeural dynamics and brain functionNeuroscience and Neural Engineering

Axons, but not cell bodies, are activated by electrical stimulation in cortical gray matter

Nowak, L. G., Bullier, J.·1998·Experimental Brain Research

DOI 10.1007/s002210050304

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Abstract

Extracellular electrical stimulation of the gray matter is often used to determine the function of a given cortical area or pathway. However, when it is used to elicit postsynaptic effects, the presynaptic neuronal elements activated by electrical stimulation have never been clearly identified: it could be the excitable dendrites, the cell body, the axon initial segment, or the axonal branches. To identify these elements, we performed two series of experiments on slices of rat visual cortex maintained in vitro. The first series of experiments, reported in this paper, was aimed at determining the chronaxie, a temporal parameter related to the membrane properties of the neuronal elements. In order to identify the presynaptic elements that were activated by extracellular electrical stimulation, chronaxies corresponding to postsynaptic responses were measured and compared with those corresponding to the activation of axons (antidromic activation) and those corresponding to the activation of cell bodies (intracellular current injection in intracellularly recorded neurons). The chronaxie for orthodromic activation was similar to that for axonal activation, but was 40 times smaller than the chronaxie for direct cell body activation. This suggests that, whenever a postsynaptic response is elicited after electrical stimulation of the cortical gray matter, axons (either axonal branches or axon initial segments), but not cell bodies, are the neuronal elements activated.

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It remains probable that electrical and neuronal interactions play an additional complicating role.
“Nonetheless, it remains probable that electrical and neuronal interactions play an additional complicating role54.”
From A virtual patient simulation modeling the neural and perceptual effects of human visual cortical stimulation, from pulse trains to percepts (2024) · cites this paper as [54]

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DEEP BRAIN STIMULATION
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Translational principles of deep brain stimulation
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Transcranial alternating current stimulation: a review of the underlying mechanisms and modulation of cognitive processes
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Detection, stimulation, and inhibition of neuronal signals with high-density nanowire transistor arrays.
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Uncovering the mechanism(s) of action of deep brain stimulation: activation, inhibition, or both
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Glial responses to implanted electrodes in the brain
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Direct activation of sparse, distributed populations of cortical neurons by electrical microstimulation
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High Frequency Stimulation of the Subthalamic Nucleus Eliminates Pathological Thalamic Rhythmicity in a Computational Model
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Constraints on Somatotopic Organization in the Primary Motor Cortex
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Short‐interval paired‐pulse inhibition and facilitation of human motor cortex: the dimension of stimulus intensity
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Nanomaterials for Neural Interfaces
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Implanted Neural Interfaces: Biochallenges and Engineered Solutions
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Electric field and stimulating influence generated by deep brain stimulation of the subthalamic nucleus
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Beyond the arcuate fasciculus: consensus and controversy in the connectional anatomy of language
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Mechanisms of deep brain stimulation
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Selection of stimulus parameters for deep brain stimulation
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Chronic subthalamic nucleus stimulation reduces medication requirements in Parkinson’s disease
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Deep brain stimulation creates an informational lesion of the stimulated nucleus
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Introduction to the programming of deep brain stimulators
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Direct and Indirect Activation of Cortical Neurons by Electrical Microstimulation
Tehovnik, E. J., Tolias, A. S., Sultan, F. R., Slocum, W. M., & Logothetis, N. K. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00126.2006 · Cited by 358 · see citing works
Electrical Stimulation of Mammalian Retinal Ganglion Cells With Multielectrode Arrays
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Axons, but not cell bodies, are activated by electrical stimulation in cortical gray matter
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Simulation of transcranial magnetic stimulation in head model with morphologically-realistic cortical neurons
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Excitation of Central Nervous System Neurons by Nonuniform Electric Fields
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Computational Analysis of Subthalamic Nucleus and Lenticular Fasciculus Activation During Therapeutic Deep Brain Stimulation
Miocinovic, S., Parent, M., Butson, C. R., Hahn, P. J., Russo, G. S., Vitek, J. L., & McIntyre, C. C. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00305.2006 · Cited by 304 · see citing works
Bilateral high-frequency stimulation in the subthalamic nucleus for the treatment of Parkinson disease: correlation of therapeutic effect with anatomical electrode position
Voges, J., Volkmann, J., Allert, N., Lehrke, R., Koulousakis, A., Freund, H., & Sturm, V. (2002) · Journal of neurosurgery · doi:10.3171/jns.2002.96.2.0269 · Cited by 301 · see citing works
Motor cortex stimulation in neuropathic pain. Correlations between analgesic effect and hemodynamic changes in the brain. A PET study
Peyron, R., Faillenot, I., Mertens, P., Laurent, B., & Garcı́a-Larrea, L. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.08.037 · Cited by 273 · see citing works
Tracking axonal action potential propagation on a high-density microelectrode array across hundreds of sites
Bakkum, D. J., Frey, U., Radivojević, M., Russell, T. L., Müller, J., Michele, F., Takahashi, H., & Hierlemann, A. R. (2013) · Nature Communications · doi:10.1038/ncomms3181 · Cited by 269 · see citing works
Good vibrations: Oscillatory phase shapes perception
Neuling, T., Rach, S., Wagner, S., Wolters, C. H., & Herrmann, C. S. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.07.024 · Cited by 270 · see citing works
Electrophysiological and metabolic evidence that high‐frequency stimulation of the subthalamic nucleus bridles neuronal activity in the subthalamic nucleus and the substantia nigra reticulata
Tai, C., Boraud, T., Bézard, E., Bioulac, B. H., Gross, C. E., & Benazzouz, A. (2003) · The FASEB Journal · doi:10.1096/fj.03-0163com · Cited by 261 · see citing works
Selective Microstimulation of Central Nervous System Neurons
McIntyre, C. C., & Grill, W. M. (2000) · Annals of Biomedical Engineering · doi:10.1114/1.262 · Cited by 259 · see citing works
Mapping Cortical Activity Elicited with Electrical Microstimulation Using fMRI in the Macaque
Tolias, A. S., Sultan, F. R., Augath, M. A., Oeltermann, A., Tehovnik, E. J., Schiller, P. H., & Logothetis, N. K. (2005) · Neuron · doi:10.1016/j.neuron.2005.11.034 · Cited by 251 · see citing works
Spatiotemporal Effects of Microstimulation in Rat Neocortex: A Parametric Study Using Multielectrode Recordings
Butovas, S., & Schwarz, C. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00245.2003 · Cited by 246 · see citing works
Deep brain stimulation of the subthalamic nucleus in Parkinson's disease: effects of variation in stimulation parameters
Rizzone, M. G. (2001) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.71.2.215 · Cited by 248 · see citing works
Which Neuronal Elements are Activated Directly by Spinal Cord Stimulation
Holsheimer, J. (2002) · Neuromodulation Technology at the Neural Interface · doi:10.1046/j.1525-1403.2002._2005.x · Cited by 248 · see citing works
Dual Effect of High-Frequency Stimulation on Subthalamic Neuron Activity
García, L., Audin, J., D’Alessandro, G., Bioulac, B. H., & Hammond, C. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-25-08743.2003 · Cited by 245 · see citing works
High-frequency stimulation in Parkinson's disease: more or less?
García, L., D’Alessandro, G., Bioulac, B. H., & Hammond, C. (2005) · Trends in Neurosciences · doi:10.1016/j.tins.2005.02.005 · Cited by 239 · see citing works
Two phases of short-interval intracortical inhibition
Roshan, L., Paradiso, G. O., & Chen, R. E. (2003) · Experimental Brain Research · doi:10.1007/s00221-003-1502-9 · Cited by 238 · see citing works
Synaptic Overflow of Dopamine in the Nucleus Accumbens Arises from Neuronal Activity in the Ventral Tegmental Area
Sombers, L. A., Beyene, M., Carelli, R. M., & Wightman, R. M. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.5562-08.2009 · Cited by 231 · see citing works
Cellular, molecular, and clinical mechanisms of action of deep brain stimulation—a systematic review on established indications and outlook on future developments
Jakobs, M., Fomenko, A., Lozano, A. M., & Kiening, K. L. (2019) · EMBO Molecular Medicine · doi:10.15252/emmm.201809575 · Cited by 229 · see citing works
Finite-Element Model Predicts Current Density Distribution for Clinical Applications of tDCS and tACS
Neuling, T., Wagner, S., Wolters, C. H., Zaehle, T., & Herrmann, C. S. (2012) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2012.00083 · Cited by 227 · see citing works
Basal ganglia circuit loops, dopamine and motivation: a review and enquiry
Ikemoto, S., Yang, C., & Tan, A. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.04.018 · Cited by 226 · see citing works
“[78–80]; therefore, it is difficult to interpret the data.”
Transcranial magnetic stimulation
Lefaucheur, J. (2019) · Handbook of clinical neurology · doi:10.1016/b978-0-444-64032-1.00037-0 · Cited by 225 · see citing works
Stimulation of the Human Lumbar Spinal Cord With Implanted and Surface Electrodes: A Computer Simulation Study
Ladenbauer, J., Minassian, K., Hofstoetter, U. S., Dimitrijevic, M. R., & Rattay, F. (2010) · IEEE Transactions on Neural Systems and Rehabilitation Engineering · doi:10.1109/tnsre.2010.2054112 · Cited by 223 · see citing works
Motor cortex stimulation for neuropathic pain: From phenomenology to mechanisms
Garcia-Larrea, L., & Peyron, R. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.05.062 · Cited by 259 · see citing works
Latest view on the mechanism of action of deep brain stimulation
Hammond, C., Ammari, R., Bioulac, B. H., & García, L. (2008) · Movement Disorders · doi:10.1002/mds.22120 · Cited by 216 · see citing works
Electric field strength and focality in electroconvulsive therapy and magnetic seizure therapy: a finite element simulation study
Deng, Z.-D., Lisanby, S. H., & Peterchev, A. V. (2011) · Journal of Neural Engineering · doi:10.1088/1741-2560/8/1/016007 · Cited by 216 · see citing works
Direct electrical stimulation as an input gate into brain functional networks: principles, advantages and limitations
Mandonnet, E., Winkler, P., & Duffau, H. (2009) · Acta Neurochirurgica · doi:10.1007/s00701-009-0469-0 · Cited by 217 · see citing works
Electroconvulsive Therapy Stimulus Parameters: Rethinking Dosage
Peterchev, A. V., Rosa, M. A., Deng, Z.-D., Prudic, J., & Lisanby, S. H. (2010) · The Journal of ECT · doi:10.1097/yct.0b013e3181e48165 · Cited by 213 · see citing works
The use of repetitive transcranial magnetic stimulation (rTMS) and transcranial direct current stimulation (tDCS) to relieve pain.
Lefaucheur, J., Antal, A., Ahdab, R., de Andrade, D. C., Fregni, F., Khedr, E., Nitsche, M., & Paulus, W. (2008) · Brain Stimulation · doi:10.1016/j.brs.2008.07.003 · Cited by 209 · see citing works
Deep brain stimulation mechanisms: beyond the concept of local functional inhibition
Deniau, J., Degos, B., Bosch‐Bouju, C., & Maurice, N. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07413.x · Cited by 203 · see citing works
Serotonergic versus nonserotonergic dorsal raphe projection neurons: differential participation in reward circuitry
McDevitt, R. A., Tiran-Cappello, A., Shen, H., Balderas, I., Britt, J. P., Marino, R. A. M., Chung, S. L., Richie, C. T., Harvey, B. K., & Bonci, A. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.08.037 · Cited by 203 · see citing works
High-Frequency Deep Brain Stimulation of the Nucleus Accumbens Region Suppresses Neuronal Activity and Selectively Modulates Afferent Drive in Rat Orbitofrontal CortexIn Vivo
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Probabilistic analysis of activation volumes generated during deep brain stimulation
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Biophysically realistic neuron models for simulation of cortical stimulation
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Influence of the frequency parameter on extracellular glutamate and γ‐aminobutyric acid in substantia nigra and globus pallidus during electrical stimulation of subthalamic nucleus in rats
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Control of Neuronal Synchrony by Nonlinear Delayed Feedback
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Energy-efficient waveform shapes for neural stimulation revealed with a genetic algorithm
Wongsarnpigoon, A., & Grill, W. M. (2010) · Journal of Neural Engineering · doi:10.1088/1741-2560/7/4/046009 · Cited by 166 · see citing works
Consensus Paper: Experimental Neurostimulation of the Cerebellum
Miterko, L. N., Baker, K. B., Beckinghausen, J., Bradnam, L. V., Cheng, M., Cooperrider, J., DeLong, M. R., Gornati, S. V., Hallett, M., Heck, D. H., et al. (2019) · The Cerebellum · doi:10.1007/s12311-019-01041-5 · Cited by 162 · see citing works
Neurophysiological effects of stimulation through electrodes in the human subthalamic nucleus
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Thresholds for Activation of Rabbit Retinal Ganglion Cells with Relatively Large, Extracellular Microelectrodes
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Evaluation of novel stimulus waveforms for deep brain stimulation
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Deep brain stimulation in neurological diseases and experimental models: From molecule to complex behavior
Gubellini, P., Salin, P., Goff, L. K., & Baunez, C. (2009) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2009.06.003 · Cited by 160 · see citing works
Transcranial magnetic stimulation of the brain
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Horizontal synaptic connections in monkey prefrontal cortex: An in vitro electrophysiological study
Gonzalez-Burgos, G. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.1.82 · Cited by 169 · see citing works
Principles of electrical stimulation of neural tissue
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Selective Activation of Neuronal Targets With Sinusoidal Electric Stimulation
Freeman, D. K., Eddington, D. K., Rizzo, J. F., & Fried, S. I. (2010) · Journal of Neurophysiology · doi:10.1152/jn.00551.2010 · Cited by 149 · see citing works
Thresholds for Activation of Rabbit Retinal Ganglion Cells with an Ultrafine, Extracellular Microelectrode
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Authors: Nowak, L. G., & Bullier, J.
Affiliations: Inserm (FR)
ORCID: Nowak, L. G.
Venue: Experimental Brain Research
Publisher: Springer Science and Business Media LLC
Published: 1998-02-02
Volume: 118
Issue: 4
Pages: 477-488
ISSN: 0014-4819 (ISSN-L)
1432-1106
DOI: 10.1007/s002210050304
OpenAlex: W2183760535
Cited by: 492
References: 124
Citations by year: 2026: 6 · 2025: 16 · 2024: 14 · 2023: 17 · 2022: 16 · 2021: 20 · 2020: 21 · 2019: 14 · 2018: 15 · 2017: 19 · 2016: 15 · 2015: 30 · 2014: 17 · 2013: 22 · 2012: 24
FWCI: 2.24
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Experimental Brain Research (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neural Engineering
Keywords: extracellular electrical stimulation, cortical gray matter, axons, axon initial segment, chronaxie, antidromic activation, postsynaptic response, membrane properties
MeSH terms: Animals, Axons, Electric Stimulation, Electrophysiology, Extracellular Space, Female, Male, Neural Conduction, Neurons, Visual Cortex, Rats, Sprague-Dawley, Rats, Wistar, Excitatory Postsynaptic Potentials, Rats, In Vitro Techniques

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Axons, but not cell bodies, are activated by electrical stimulation in cortical gray matter

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