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Published in: Journal of NeuroEngineering and Rehabilitation 1/2019

Open Access 01-12-2019 | Research

Control of cortical oscillatory frequency by a closed-loop system

Authors: Mattia D’Andola, Massimiliano Giulioni, Vittorio Dante, Paolo Del Giudice, Maria V. Sanchez-Vives

Published in: Journal of NeuroEngineering and Rehabilitation | Issue 1/2019

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Abstract

Background

We present a closed-loop system able to control the frequency of slow oscillations (SO) spontaneously generated by the cortical network in vitro. The frequency of SO can be controlled by direct current (DC) electric fields within a certain range. Here we set out to design a system that would be able to autonomously bring the emergent oscillatory activity to a target frequency determined by the experimenter.

Methods

The cortical activity was recorded through an electrode and was analyzed online. Once a target frequency was set, the frequency of the slow oscillation was steered through the injection of DC of variable intensity that generated electric fields of proportional amplitudes in the brain slice. To achieve such closed-loop control, we designed a custom programmable stimulator ensuring low noise and accurate tuning over low current levels. For data recording and analysis, we relied on commercial acquisition and software tools.

Results

The result is a flexible and reliable system that ensures control over SO frequency in vitro. The system guarantees artifact removal, minimal gaps in data acquisition and robustness in spite of slice heterogeneity.

Conclusions

Our tool opens new possibilities for the investigation of dynamics of cortical slow oscillations—an activity pattern that is associated with cognitive processes such as memory consolidation, and that is altered in several neurological conditions—and also for potential applications of this technology.
Literature
1.
go back to reference Hodgkin AL, Huxley AF. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol. 1952;117:500–44.CrossRef Hodgkin AL, Huxley AF. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol. 1952;117:500–44.CrossRef
2.
go back to reference Sharp AA, O’Neil MB, Abbott LF, Marder E. The dynamic clamp: artificial conductances in biological neurons. Trends Neurosci. 1993;16:389–94.CrossRef Sharp AA, O’Neil MB, Abbott LF, Marder E. The dynamic clamp: artificial conductances in biological neurons. Trends Neurosci. 1993;16:389–94.CrossRef
3.
go back to reference Wagenaar DA, Madhavan R, Pine J, Potter SM. Controlling bursting in cortical cultures with closed-loop multi-electrode stimulation. J Neurosci. 2005;25:680–8.CrossRef Wagenaar DA, Madhavan R, Pine J, Potter SM. Controlling bursting in cortical cultures with closed-loop multi-electrode stimulation. J Neurosci. 2005;25:680–8.CrossRef
4.
5.
go back to reference Jackson A, Mavoori J, Fetz EE. Long-term motor cortex plasticity induced by an electronic neural implant. Nature. 2006;444:56–60.CrossRef Jackson A, Mavoori J, Fetz EE. Long-term motor cortex plasticity induced by an electronic neural implant. Nature. 2006;444:56–60.CrossRef
6.
go back to reference Ezzyat Y, Wanda PA, Levy DF, Kadel A, Aka A, Pedisich I, et al. Closed-loop stimulation of temporal cortex rescues functional networks and improves memory. Nat Commun. 2018;9:365.CrossRef Ezzyat Y, Wanda PA, Levy DF, Kadel A, Aka A, Pedisich I, et al. Closed-loop stimulation of temporal cortex rescues functional networks and improves memory. Nat Commun. 2018;9:365.CrossRef
7.
go back to reference Arsiero M, Luscher HR, Giugliano M. Real-time closed-loop electrophysiology: towards new frontiers in in vitro investigations in the neurosciences. Arch Ital Biol. 2007;145:193–209.PubMed Arsiero M, Luscher HR, Giugliano M. Real-time closed-loop electrophysiology: towards new frontiers in in vitro investigations in the neurosciences. Arch Ital Biol. 2007;145:193–209.PubMed
8.
go back to reference Limousin P, Pollak P, Benazzouz A, Hoffmann D, Le Bas JF, Perret JE, et al. Effect on parkinsonian signs and symptoms of bilateral subthalamic nucleus stimulation. Lancet. 1995;345:91–5.CrossRef Limousin P, Pollak P, Benazzouz A, Hoffmann D, Le Bas JF, Perret JE, et al. Effect on parkinsonian signs and symptoms of bilateral subthalamic nucleus stimulation. Lancet. 1995;345:91–5.CrossRef
9.
go back to reference Little S, Pogosyan A, Neal S, Zavala B, Zrinzo L, Hariz M, et al. Adaptive deep brain stimulation in advanced Parkinson disease. Ann Neurol. 2013;74:449–57.CrossRef Little S, Pogosyan A, Neal S, Zavala B, Zrinzo L, Hariz M, et al. Adaptive deep brain stimulation in advanced Parkinson disease. Ann Neurol. 2013;74:449–57.CrossRef
10.
go back to reference Rosin B, Slovik M, Mitelman R, Rivlin-Etzion M, Haber SN, Israel Z, et al. Closed-loop deep brain stimulation is superior in ameliorating parkinsonism. Neuron. 2011;72:370–84.CrossRef Rosin B, Slovik M, Mitelman R, Rivlin-Etzion M, Haber SN, Israel Z, et al. Closed-loop deep brain stimulation is superior in ameliorating parkinsonism. Neuron. 2011;72:370–84.CrossRef
11.
go back to reference Sanchez-Vives MV, McCormick DA. Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci. 2000;3:1027–34.CrossRef Sanchez-Vives MV, McCormick DA. Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci. 2000;3:1027–34.CrossRef
12.
go back to reference Compte A, Reig R, Descalzo VF, Harvey MA, Puccini GD, Sanchez-Vives MV. Spontaneous high-frequency (10-80 Hz) oscillations during up states in the cerebral cortex in vitro. J Neurosci. 2008;28:13828–44.CrossRef Compte A, Reig R, Descalzo VF, Harvey MA, Puccini GD, Sanchez-Vives MV. Spontaneous high-frequency (10-80 Hz) oscillations during up states in the cerebral cortex in vitro. J Neurosci. 2008;28:13828–44.CrossRef
13.
go back to reference Sanchez-Vives MV, Mattia M. Slow wave activity as the default mode of the cerebral cortex. Arch Ital Biol. 2014;152:147–55.PubMed Sanchez-Vives MV, Mattia M. Slow wave activity as the default mode of the cerebral cortex. Arch Ital Biol. 2014;152:147–55.PubMed
14.
go back to reference Sanchez-Vives M V., Massimini M, Mattia M. Shaping the Default Activity Pattern of the Cortical Network. Neuron. 2017;94:993–1001. Sanchez-Vives M V., Massimini M, Mattia M. Shaping the Default Activity Pattern of the Cortical Network. Neuron. 2017;94:993–1001.
15.
go back to reference Marshall L, Molle M, Hallschmid M, Born J. Transcranial direct current stimulation during sleep improves declarative memory. J Neurosci. 2004;24:9985–92.CrossRef Marshall L, Molle M, Hallschmid M, Born J. Transcranial direct current stimulation during sleep improves declarative memory. J Neurosci. 2004;24:9985–92.CrossRef
16.
go back to reference Diekelmann S, Born J. The memory function of sleep. Nat Rev Neurosci. 2010;11:114–26. Diekelmann S, Born J. The memory function of sleep. Nat Rev Neurosci. 2010;11:114–26.
17.
go back to reference Wilckens KA, Ferrarelli F, Walker MP, Buysse DJ. Slow-wave activity enhancement to improve cognition. Trends Neurosci. 2018;41:470–82.CrossRef Wilckens KA, Ferrarelli F, Walker MP, Buysse DJ. Slow-wave activity enhancement to improve cognition. Trends Neurosci. 2018;41:470–82.CrossRef
18.
go back to reference Steriade M, Contreras D, Curró Dossi R, Nuñez A. The slow (< 1 Hz) oscillation in reticular thalamic and thalamocortical neurons: scenario of sleep rhythm generation in interacting thalamic and neocortical networks. J Neurosci. 1993;13:3284–99.CrossRef Steriade M, Contreras D, Curró Dossi R, Nuñez A. The slow (< 1 Hz) oscillation in reticular thalamic and thalamocortical neurons: scenario of sleep rhythm generation in interacting thalamic and neocortical networks. J Neurosci. 1993;13:3284–99.CrossRef
19.
go back to reference Steriade M, Amzica F, Contreras D. Synchronization of fast (30–40 Hz) spontaneous cortical rhythms during brain activation. J Neurosci. 1996;16:392 LP–417.CrossRef Steriade M, Amzica F, Contreras D. Synchronization of fast (30–40 Hz) spontaneous cortical rhythms during brain activation. J Neurosci. 1996;16:392 LP–417.CrossRef
20.
go back to reference Buzsaki G, Silva FL. High frequency oscillations in the intact brain. Prog Neurobiol. 2012;98:241–9.CrossRef Buzsaki G, Silva FL. High frequency oscillations in the intact brain. Prog Neurobiol. 2012;98:241–9.CrossRef
21.
go back to reference Siegel M, Donner TH, Engel AK. Spectral fingerprints of large-scale neuronal interactions. Nat Rev Neurosci. 2012;13:121–34.CrossRef Siegel M, Donner TH, Engel AK. Spectral fingerprints of large-scale neuronal interactions. Nat Rev Neurosci. 2012;13:121–34.CrossRef
22.
go back to reference Lopes da Silva FH, van Rotterdam A, Storm van Leeuwen W, Tielen AM. Dynamic characteristics of visual evoked potentials in the dog. I. Cortical and subcortical potentials evoked by sine wave modulated light. Electroencephalogr Clin Neurophysiol. 1970;29:246–59.CrossRef Lopes da Silva FH, van Rotterdam A, Storm van Leeuwen W, Tielen AM. Dynamic characteristics of visual evoked potentials in the dog. I. Cortical and subcortical potentials evoked by sine wave modulated light. Electroencephalogr Clin Neurophysiol. 1970;29:246–59.CrossRef
23.
go back to reference Lopes da Silva FH, van Rotterdam A, Storm van Leeuwen W, Tielen AM. Dynamic characteristics of visual evoked potentials in the dog. II. Beta frequency selectivity in evoked potentials and background activity. Electroencephalogr Clin Neurophysiol. 1970;29:260–8.CrossRef Lopes da Silva FH, van Rotterdam A, Storm van Leeuwen W, Tielen AM. Dynamic characteristics of visual evoked potentials in the dog. II. Beta frequency selectivity in evoked potentials and background activity. Electroencephalogr Clin Neurophysiol. 1970;29:260–8.CrossRef
24.
go back to reference Bouyer JJ, Montaron MF, Rougeul A, Buser P. Parietal electrocortical rhythms in the cat: their relation to a behavior of focused attention and possible mesencephalic control through a dopaminergic pathway. C R Seances Acad Sci D. 1980;291:779–83.PubMed Bouyer JJ, Montaron MF, Rougeul A, Buser P. Parietal electrocortical rhythms in the cat: their relation to a behavior of focused attention and possible mesencephalic control through a dopaminergic pathway. C R Seances Acad Sci D. 1980;291:779–83.PubMed
25.
go back to reference Desmedt JE, Tomberg C. Transient phase-locking of 40 Hz electrical oscillations in prefrontal and parietal human cortex reflects the process of conscious somatic perception. Neurosci Lett. 1994;168:126–9.CrossRef Desmedt JE, Tomberg C. Transient phase-locking of 40 Hz electrical oscillations in prefrontal and parietal human cortex reflects the process of conscious somatic perception. Neurosci Lett. 1994;168:126–9.CrossRef
26.
go back to reference Frohlich F, McCormick DA. Endogenous electric fields may guide neocortical network activity. Neuron. 2010;67:129–43.CrossRef Frohlich F, McCormick DA. Endogenous electric fields may guide neocortical network activity. Neuron. 2010;67:129–43.CrossRef
27.
go back to reference Reato D, Rahman A, Bikson M, Parra LC. Low-intensity electrical stimulation affects network dynamics by modulating population rate and spike timing. J Neurosci. 2010;30:15067–79.CrossRef Reato D, Rahman A, Bikson M, Parra LC. Low-intensity electrical stimulation affects network dynamics by modulating population rate and spike timing. J Neurosci. 2010;30:15067–79.CrossRef
28.
go back to reference D’Andola M, Weinert JF, Mattia M, Sanchez-Vives M V. Modulation of slow and fast oscillations by direct current stimulation in the cerebral cortex in vitro. bioRxiv. Cold Spring Harbor Laboratory; 2018;246819. D’Andola M, Weinert JF, Mattia M, Sanchez-Vives M V. Modulation of slow and fast oscillations by direct current stimulation in the cerebral cortex in vitro. bioRxiv. Cold Spring Harbor Laboratory; 2018;246819.
29.
go back to reference D’Andola M, Giulioni M, Dante V, Del Giudice P, Sanchez-Vives M V. A closed-loop stimulation system to modulate slow oscillations frequency of in vitro acute cortical slices. B-DEBATE A Dialogue with Cereb Cortex Cortical Funct Interfacing. Frontiers in Systems Neuroscience; 2015. D’Andola M, Giulioni M, Dante V, Del Giudice P, Sanchez-Vives M V. A closed-loop stimulation system to modulate slow oscillations frequency of in vitro acute cortical slices. B-DEBATE A Dialogue with Cereb Cortex Cortical Funct Interfacing. Frontiers in Systems Neuroscience; 2015.
30.
go back to reference Sorensen M, DeWeerth S, Cymbalyuk G, Calabrese RL. Using a hybrid neural system to reveal regulation of neuronal network activity by an intrinsic current. J Neurosci. 2004;24:5427–38.CrossRef Sorensen M, DeWeerth S, Cymbalyuk G, Calabrese RL. Using a hybrid neural system to reveal regulation of neuronal network activity by an intrinsic current. J Neurosci. 2004;24:5427–38.CrossRef
31.
go back to reference Mavoori J, Jackson A, Diorio C, Fetz E. An autonomous implantable computer for neural recording and stimulation in unrestrained primates. J Neurosci Methods. 2005;148:71–7.CrossRef Mavoori J, Jackson A, Diorio C, Fetz E. An autonomous implantable computer for neural recording and stimulation in unrestrained primates. J Neurosci Methods. 2005;148:71–7.CrossRef
32.
go back to reference Schiff SJ. Neural control engineering: the emerging intersection between control theory and neuroscience. Press MIT, editor. Comput. Neurosci. Cambridge, Massachusetts: 2012 Massachusetts Institute of Technology; 2012. Schiff SJ. Neural control engineering: the emerging intersection between control theory and neuroscience. Press MIT, editor. Comput. Neurosci. Cambridge, Massachusetts: 2012 Massachusetts Institute of Technology; 2012.
33.
go back to reference Dorval AD, Christini DJ, White JA. Real-time linux dynamic clamp: a fast and flexible way to construct virtual ion channels in living cells. Ann Biomed Eng. 2001;29:897–907.CrossRef Dorval AD, Christini DJ, White JA. Real-time linux dynamic clamp: a fast and flexible way to construct virtual ion channels in living cells. Ann Biomed Eng. 2001;29:897–907.CrossRef
34.
go back to reference Rolston JD, Gross RE, Potter SM. Closed-loop, open-source electrophysiology. Front Neurosci. 2010;4. Rolston JD, Gross RE, Potter SM. Closed-loop, open-source electrophysiology. Front Neurosci. 2010;4.
35.
go back to reference Zrenner C, Eytan D, Wallach A, Thier P, Marom S. A generic framework for real-time multi-channel neuronal signal analysis, telemetry control, and sub-millisecond latency feedback generation. Front Neurosci. 2010;4:173.CrossRef Zrenner C, Eytan D, Wallach A, Thier P, Marom S. A generic framework for real-time multi-channel neuronal signal analysis, telemetry control, and sub-millisecond latency feedback generation. Front Neurosci. 2010;4:173.CrossRef
36.
go back to reference Sanchez-Vives MV. Spontaneous Rhythmic Activity in the Adult Cerebral Cortex In Vitro. In: Ballanyi K, editor. Isol Cent Nerv Syst Circuits. 2012. p. 263–84. Sanchez-Vives MV. Spontaneous Rhythmic Activity in the Adult Cerebral Cortex In Vitro. In: Ballanyi K, editor. Isol Cent Nerv Syst Circuits. 2012. p. 263–84.
37.
go back to reference Aghajanian GK, Rasmussen K. Intracellular studies in the facial nucleus illustrating a simple new method for obtaining viable motoneurons in adult rat brain slices. Synapse. 1989;3:331–8.CrossRef Aghajanian GK, Rasmussen K. Intracellular studies in the facial nucleus illustrating a simple new method for obtaining viable motoneurons in adult rat brain slices. Synapse. 1989;3:331–8.CrossRef
38.
go back to reference Reig R, Mattia M, Compte A, Belmonte C, Sanchez-Vives MV. Temperature modulation of slow and fast cortical rhythms. J Neurophysiol. 2010;103:1253–61.CrossRef Reig R, Mattia M, Compte A, Belmonte C, Sanchez-Vives MV. Temperature modulation of slow and fast cortical rhythms. J Neurophysiol. 2010;103:1253–61.CrossRef
39.
go back to reference Mattia M, Del Giudice P. Population dynamics of interacting spiking neurons. Phys Rev E Stat Nonlin Soft Matter Phys. United States. 2002;66:51917.CrossRef Mattia M, Del Giudice P. Population dynamics of interacting spiking neurons. Phys Rev E Stat Nonlin Soft Matter Phys. United States. 2002;66:51917.CrossRef
40.
go back to reference Ruiz-Mejias M, Ciria-Suarez L, Mattia M, Sanchez-Vives MV. Slow and fast rhythms generated in the cerebral cortex of the anesthetized mouse. J Neurophysiol. 2011;106(6):2910–21. Ruiz-Mejias M, Ciria-Suarez L, Mattia M, Sanchez-Vives MV. Slow and fast rhythms generated in the cerebral cortex of the anesthetized mouse. J Neurophysiol. 2011;106(6):2910–21.
41.
go back to reference Bikson M, Inoue M, Akiyama H, Deans JK, Fox JE, Miyakawa H, et al. Effects of uniform extracellular DC electric fields on excitability in rat hippocampal slices in vitro. J Physiol. 2004;557:175–90.CrossRef Bikson M, Inoue M, Akiyama H, Deans JK, Fox JE, Miyakawa H, et al. Effects of uniform extracellular DC electric fields on excitability in rat hippocampal slices in vitro. J Physiol. 2004;557:175–90.CrossRef
42.
go back to reference Sun FT, Morrell MJ. Closed-loop neurostimulation: the clinical experience. Neurotherapeutics. NeuroPace Inc., 445 N. Bernardo Avenue, Mountain View, CA, 94043, USA, fsun@neuropace.com; 2014;11:553–63. Sun FT, Morrell MJ. Closed-loop neurostimulation: the clinical experience. Neurotherapeutics. NeuroPace Inc., 445 N. Bernardo Avenue, Mountain View, CA, 94043, USA, fsun@neuropace.com; 2014;11:553–63.
43.
go back to reference Stam CJ, van der Made Y, Pijnenburg YA, Scheltens P. EEG synchronization in mild cognitive impairment and Alzheimer’s disease. Acta Neurol Scand. 2003;108:90–6.CrossRef Stam CJ, van der Made Y, Pijnenburg YA, Scheltens P. EEG synchronization in mild cognitive impairment and Alzheimer’s disease. Acta Neurol Scand. 2003;108:90–6.CrossRef
44.
go back to reference Babiloni C, Ferri R, Moretti DV, Strambi A, Binetti G, Dal Forno G, et al. Abnormal fronto-parietal coupling of brain rhythms in mild Alzheimer’s disease: a multicentric EEG study. Eur J Neurosci. 2004;19:2583–90.CrossRef Babiloni C, Ferri R, Moretti DV, Strambi A, Binetti G, Dal Forno G, et al. Abnormal fronto-parietal coupling of brain rhythms in mild Alzheimer’s disease: a multicentric EEG study. Eur J Neurosci. 2004;19:2583–90.CrossRef
45.
go back to reference Priori A, Berardelli A, Rona S, Accornero N, Manfredi M. Polarization of the human motor cortex through the scalp. Neuroreport. 1998;9:2257–60.CrossRef Priori A, Berardelli A, Rona S, Accornero N, Manfredi M. Polarization of the human motor cortex through the scalp. Neuroreport. 1998;9:2257–60.CrossRef
46.
go back to reference Nitsche MA, Cohen LG, Wassermann EM, Priori A, Lang N, Antal A, et al. Transcranial direct current stimulation: state of the art 2008. Brain Stimul. 2008;1:206–23.CrossRef Nitsche MA, Cohen LG, Wassermann EM, Priori A, Lang N, Antal A, et al. Transcranial direct current stimulation: state of the art 2008. Brain Stimul. 2008;1:206–23.CrossRef
47.
go back to reference Nitsche MA, Paulus W. Noninvasive brain stimulation protocols in the treatment of epilepsy: current state and perspectives. Neurotherapeutics. 2009;6:244–50.CrossRef Nitsche MA, Paulus W. Noninvasive brain stimulation protocols in the treatment of epilepsy: current state and perspectives. Neurotherapeutics. 2009;6:244–50.CrossRef
48.
go back to reference Lefaucheur J-P, Antal A, Ayache SS, Benninger DH, Brunelin J, Cogiamanian F, et al. Evidence-based guidelines on the therapeutic use of transcranial direct current stimulation (tDCS). Clin Neurophysiol. 2017;128:56–92.CrossRef Lefaucheur J-P, Antal A, Ayache SS, Benninger DH, Brunelin J, Cogiamanian F, et al. Evidence-based guidelines on the therapeutic use of transcranial direct current stimulation (tDCS). Clin Neurophysiol. 2017;128:56–92.CrossRef
49.
go back to reference Marshall L, Helgadóttir H, Mölle M, Born J. Boosting slow oscillations during sleep potentiates memory. Nature. 2006;444:610–3.CrossRef Marshall L, Helgadóttir H, Mölle M, Born J. Boosting slow oscillations during sleep potentiates memory. Nature. 2006;444:610–3.CrossRef
50.
go back to reference Kirov R, Weiss C, Siebner HR, Born J, Marshall L. Slow oscillation electrical brain stimulation during waking promotes EEG theta activity and memory encoding. Proc Natl Acad Sci. 2009;106:15460–5.CrossRef Kirov R, Weiss C, Siebner HR, Born J, Marshall L. Slow oscillation electrical brain stimulation during waking promotes EEG theta activity and memory encoding. Proc Natl Acad Sci. 2009;106:15460–5.CrossRef
51.
go back to reference Ngo HVV, Martinetz T, Born J, Mölle M. Auditory closed-loop stimulation of the sleep slow oscillation enhances memory. Neuron. 2013;78:545–53.CrossRef Ngo HVV, Martinetz T, Born J, Mölle M. Auditory closed-loop stimulation of the sleep slow oscillation enhances memory. Neuron. 2013;78:545–53.CrossRef
Metadata
Title
Control of cortical oscillatory frequency by a closed-loop system
Authors
Mattia D’Andola
Massimiliano Giulioni
Vittorio Dante
Paolo Del Giudice
Maria V. Sanchez-Vives
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Journal of NeuroEngineering and Rehabilitation / Issue 1/2019
Electronic ISSN: 1743-0003
DOI
https://doi.org/10.1186/s12984-018-0470-z

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