High frequency stimulations change the phase-locking relationship between neuronal firing and the rhythms of field potentials_Journal of Biomedical Engineering

Authors：

MA Weijian ,  FENG Zhouyan , ZHOU Wenjie , WANG Zhaoxiang , CAI Ziyan

Key Laboratory of Biomedical Engineering of Ministry of Education, College of Biomedical Engineering and Instrument Science, Zhejiang University, Hangzhou 310027, P.R.China;

Corresponding author：

FENG Zhouyan, Email: fengzhouyan@139.com

Keywords：

high frequency stimulation; spike; rhythmic firing; θ rhythm; phase-locking

DOI：

10.7507/1001-5515.201706073

Video：

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Deep brain stimulation (DBS) has been successfully used to treat a variety of brain diseases in clinic. Recent investigations have suggested that high frequency stimulation (HFS) of electrical pulses used by DBS might change pathological rhythms in action potential firing of neurons, which may be one of the important mechanisms of DBS therapy. However, experimental data are required to confirm the hypothesis. In the present study, 1 min of 100 Hz HFS was applied to the Schaffer collaterals of hippocampal CA1 region in anaesthetized rats. The changes of the rhythmic firing of action potentials from pyramidal cells and interneurons were investigated in the downstream CA1 region. The results showed that obvious θ rhythms were present in the field potential of CA1 region of the anesthetized rats. The θ rhythms were especially pronounced in the stratum radiatum. In addition, there was a phase-locking relationship between neuronal spikes and the θ rhythms. However, HFS trains significantly decreased the phase-locking values between the spikes of pyramidal cells and the θ rhythms in stratum radiatum from 0.36 ± 0.12 to 0.06 ± 0.04 (P < 0.001, paired t-test, N = 8). The phase-locking values of interneuron spikes were also decreased significantly from 0.27 ± 0.08 to 0.09 ± 0.05 (P < 0.01, paired t-test, N = 8). Similar changes were obtained in the phase-locking values between neuronal spikes and the θ rhythms in the pyramidal layer. These results suggested that axonal HFS could eliminate the phase-locking relationship between action potentials of neurons and θ rhythms thereby changing the rhythmic firing of downstream neurons. HFS induced conduction block in the axons might be one of the underlying mechanisms. The finding is important for further understanding the mechanisms of DBS.

Citation： MA Weijian, FENG Zhouyan, ZHOU Wenjie, WANG Zhaoxiang, CAI Ziyan. High frequency stimulations change the phase-locking relationship between neuronal firing and the rhythms of field potentials. Journal of Biomedical Engineering, 2018, 35(1): 1-7. doi: 10.7507/1001-5515.201706073 Copy

1.	Pouratian N, Thakkar S, Kim W, et al. Deep brain stimulation for the treatment of Parkinson's disease: efficacy and safety. Degener Neurol Neuromuscul Dis, 2012(2): 6-17.
2.	Lega B C, Halpern C H, Jaggi J L, et al. Deep brain stimulation in the treatment of refractory epilepsy: update on current data and future directions. Neurobiol Dis, 2010, 38(3): 354-360.
3.	Mayberg H S, Lozano A M, Voon V, et al. Deep brain stimulation for Treatment-Resistant depression. Neuron, 2005, 45(5): 651-660.
4.	Birdno M J, Kuncel A M, Dorval A D, et al. Stimulus features underlying reduced tremor suppression with temporally patterned deep brain stimulation. J Neurophysiol, 2012, 107(1): 364-383.
5.	Chiken S, Nambu A. Mechanism of deep brain stimulation: inhibition, excitation, or disruption? Neuroscientist, 2016, 22(3): 313-322.
6.	Udupa K, Chen R. The mechanisms of action of deep brain stimulation and ideas for the future development. Prog Neurobiol, 2015, 133: 27-49.
7.	Alhourani A, Mcdowell M M, Randazzo M J, et al. Network effects of deep brain stimulation. J Neurophysiol, 2015, 114(4): 2105-2117.
8.	Iremonger K J, Anderson T R, Hu Bin, et al. Cellular mechanisms preventing sustained activation of cortex during subcortical high-frequency stimulation. J Neurophysiol, 2006, 96(2): 613-621.
9.	Deniau J M, Degos B, Bosch C, et al. Deep brain stimulation mechanisms: beyond the concept of local functional inhibition. Eur J Neurosci, 2010, 32(7): 1080-1091.
10.	McConnell G C, So R Q, Hilliard J D, et al. Effective deep brain stimulation suppresses low-frequency network oscillations in the basal ganglia by regularizing neural firing patterns. J Neurosci, 2012, 32(45): 15657-15668.
11.	Rosenbaum R, Zimnik A, ZHENG Fang, et al. Axonal and synaptic failure suppress the transfer of firing rate oscillations, synchrony and information during high frequency deep brain stimulation. Neurobiol Dis, 2014, 62(2): 86-99.
12.	Feng Zhouyan, Zheng Xiaojing, Yu Ying, et al. Functional disconnection of axonal fibers generated by high frequency stimulation in the hippocampal CA1 region in-vivo. Brain Res, 2013, 1509(7): 32-42.
13.	Yu Ying, Feng Zhouyan, Cao Jiayue, et al. Modulation of local field potentials by high-frequency stimulation of afferent axons in the hippocampal CA1 region. J Integr Neurosci, 2016, 15(1): 1-17.
14.	Buzsáki G. Theta oscillations in the hippocampus. Neuron, 2002, 33(3): 325-340.
15.	Rutishauser U, Ross I B, Mamelak A N, et al. Human memory strength is predicted by theta-frequency phase-locking of single neurons. Nature, 2010, 464(7290): 903-907.
16.	Kitchigina V, Popova I, Sinelnikova V, et al. Disturbances of septohippocampal theta oscillations in the epileptic brain: reasons and consequences. Exp Neurol, 2013, 247(3): 314-327.
17.	Singh A, Mewes K, Gross R E, et al. Human striatal recordings reveal abnormal discharge of projection neurons in Parkinson's disease. Proc Natl Acad Sci U S A, 2016, 113(34): 9629-9634.
18.	Dorval A D, Russo G S, Hashimoto T, et al. Deep brain stimulation reduces neuronal entropy in the MPTP-primate model of Parkinson's disease. J Neurophysiol, 2008, 100(5): 2807-2818.
19.	McConnell G C, So R Q, Grill W M. Failure to suppress low-frequency neuronal oscillatory activity underlies the reduced effectiveness of random patterns of deep brain stimulation. J Neurophysiol, 2016, 115(6): 2791-2802.
20.	Feng Zhouyan, Wang Zhaoxiang, Guo Zheshan, et al. High frequency stimulation of afferent fibers generates asynchronous firing in the downstream neurons in hippocampus through partial block of axonal conduction. Brain Res, 2017, 1661: 67-78.
21.	Vargas-Irwin C E, Donoghue J P. Automated spike sorting using density grid contour clustering and subtractive waveform decomposition. J Neurosci Methods, 2007, 164(1): 1-18.
22.	Barthó P, Hirase H, Monconduit L, et al. Characterization of neocortical principal cells and interneurons by network interactions and extracellular features. J Neurophysiol, 2004, 92(1): 600-608.
23.	Klausberger T, Márton L F, Baude A, et al. Spike timing of dendrite-targeting bistratified cells during hippocampal network oscillations in vivo. Nat Neurosci, 2004, 7(1): 41-47.
24.	Berens P. CircStat: a MATLAB toolbox for circular statistics. J Stat Softw, 2009, 31(1): 1-21.
25.	Lowet E, Roberts M J, Bonizzi P, et al. Quantifying neural oscillatory synchronization: a comparison between spectral coherence and Phase-Locking value approaches. PLoS One, 2016, 11(1): e0146443.
26.	Lee M G, Chrobak J J, Sik A, et al. Hippocampal theta activity following selective lesion of the septal cholinergic system. Neuroscience, 1994, 62(4): 1033-1047.
27.	Kamondi A, Acsády L, Wang X J, et al. Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: activity-dependent phase-precession of action potentials. Hippocampus, 1998, 8(3): 244-261.
28.	Buzsáki G, Moser E I. Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat Neurosci, 2013, 16(2): 130-138.
29.	Meeks J P, Mennerick S. Selective effects of Potassium elevations on glutamate signaling and action potential conduction in hippocampus. J Neurosci, 2004, 24(1): 197-206.
30.	Bellinger S C, Miyazawa G, Steinmetz P N. Submyelin Potassium accumulation May functionally block subsets of local axons during deep brain stimulation: a modeling study. J Neural Eng, 2008, 5(3): 263-274.
31.	Ranck J B. Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res, 1975, 98(3): 417-440.
32.	Lehnertz K, Bialonski S, Horstmann M T, et al. Synchronization phenomena in human epileptic brain networks. J Neurosci Methods, 2009, 183(1): 42-48.
33.	Rubchinsky L L, Park C, Worth R M. Intermittent neural synchronization in Parkinson’s disease. Nonlinear Dyn, 2012, 68(3): 329-346.

1. Pouratian N, Thakkar S, Kim W, et al. Deep brain stimulation for the treatment of Parkinson's disease: efficacy and safety. Degener Neurol Neuromuscul Dis, 2012(2): 6-17.
2. Lega B C, Halpern C H, Jaggi J L, et al. Deep brain stimulation in the treatment of refractory epilepsy: update on current data and future directions. Neurobiol Dis, 2010, 38(3): 354-360.
3. Mayberg H S, Lozano A M, Voon V, et al. Deep brain stimulation for Treatment-Resistant depression. Neuron, 2005, 45(5): 651-660.
4. Birdno M J, Kuncel A M, Dorval A D, et al. Stimulus features underlying reduced tremor suppression with temporally patterned deep brain stimulation. J Neurophysiol, 2012, 107(1): 364-383.
5. Chiken S, Nambu A. Mechanism of deep brain stimulation: inhibition, excitation, or disruption? Neuroscientist, 2016, 22(3): 313-322.
6. Udupa K, Chen R. The mechanisms of action of deep brain stimulation and ideas for the future development. Prog Neurobiol, 2015, 133: 27-49.
7. Alhourani A, Mcdowell M M, Randazzo M J, et al. Network effects of deep brain stimulation. J Neurophysiol, 2015, 114(4): 2105-2117.
8. Iremonger K J, Anderson T R, Hu Bin, et al. Cellular mechanisms preventing sustained activation of cortex during subcortical high-frequency stimulation. J Neurophysiol, 2006, 96(2): 613-621.
9. Deniau J M, Degos B, Bosch C, et al. Deep brain stimulation mechanisms: beyond the concept of local functional inhibition. Eur J Neurosci, 2010, 32(7): 1080-1091.
10. McConnell G C, So R Q, Hilliard J D, et al. Effective deep brain stimulation suppresses low-frequency network oscillations in the basal ganglia by regularizing neural firing patterns. J Neurosci, 2012, 32(45): 15657-15668.
11. Rosenbaum R, Zimnik A, ZHENG Fang, et al. Axonal and synaptic failure suppress the transfer of firing rate oscillations, synchrony and information during high frequency deep brain stimulation. Neurobiol Dis, 2014, 62(2): 86-99.
12. Feng Zhouyan, Zheng Xiaojing, Yu Ying, et al. Functional disconnection of axonal fibers generated by high frequency stimulation in the hippocampal CA1 region in-vivo. Brain Res, 2013, 1509(7): 32-42.
13. Yu Ying, Feng Zhouyan, Cao Jiayue, et al. Modulation of local field potentials by high-frequency stimulation of afferent axons in the hippocampal CA1 region. J Integr Neurosci, 2016, 15(1): 1-17.
14. Buzsáki G. Theta oscillations in the hippocampus. Neuron, 2002, 33(3): 325-340.
15. Rutishauser U, Ross I B, Mamelak A N, et al. Human memory strength is predicted by theta-frequency phase-locking of single neurons. Nature, 2010, 464(7290): 903-907.
16. Kitchigina V, Popova I, Sinelnikova V, et al. Disturbances of septohippocampal theta oscillations in the epileptic brain: reasons and consequences. Exp Neurol, 2013, 247(3): 314-327.
17. Singh A, Mewes K, Gross R E, et al. Human striatal recordings reveal abnormal discharge of projection neurons in Parkinson's disease. Proc Natl Acad Sci U S A, 2016, 113(34): 9629-9634.
18. Dorval A D, Russo G S, Hashimoto T, et al. Deep brain stimulation reduces neuronal entropy in the MPTP-primate model of Parkinson's disease. J Neurophysiol, 2008, 100(5): 2807-2818.
19. McConnell G C, So R Q, Grill W M. Failure to suppress low-frequency neuronal oscillatory activity underlies the reduced effectiveness of random patterns of deep brain stimulation. J Neurophysiol, 2016, 115(6): 2791-2802.
20. Feng Zhouyan, Wang Zhaoxiang, Guo Zheshan, et al. High frequency stimulation of afferent fibers generates asynchronous firing in the downstream neurons in hippocampus through partial block of axonal conduction. Brain Res, 2017, 1661: 67-78.
21. Vargas-Irwin C E, Donoghue J P. Automated spike sorting using density grid contour clustering and subtractive waveform decomposition. J Neurosci Methods, 2007, 164(1): 1-18.
22. Barthó P, Hirase H, Monconduit L, et al. Characterization of neocortical principal cells and interneurons by network interactions and extracellular features. J Neurophysiol, 2004, 92(1): 600-608.
23. Klausberger T, Márton L F, Baude A, et al. Spike timing of dendrite-targeting bistratified cells during hippocampal network oscillations in vivo. Nat Neurosci, 2004, 7(1): 41-47.
24. Berens P. CircStat: a MATLAB toolbox for circular statistics. J Stat Softw, 2009, 31(1): 1-21.
25. Lowet E, Roberts M J, Bonizzi P, et al. Quantifying neural oscillatory synchronization: a comparison between spectral coherence and Phase-Locking value approaches. PLoS One, 2016, 11(1): e0146443.
26. Lee M G, Chrobak J J, Sik A, et al. Hippocampal theta activity following selective lesion of the septal cholinergic system. Neuroscience, 1994, 62(4): 1033-1047.
27. Kamondi A, Acsády L, Wang X J, et al. Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: activity-dependent phase-precession of action potentials. Hippocampus, 1998, 8(3): 244-261.
28. Buzsáki G, Moser E I. Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat Neurosci, 2013, 16(2): 130-138.
29. Meeks J P, Mennerick S. Selective effects of Potassium elevations on glutamate signaling and action potential conduction in hippocampus. J Neurosci, 2004, 24(1): 197-206.
30. Bellinger S C, Miyazawa G, Steinmetz P N. Submyelin Potassium accumulation May functionally block subsets of local axons during deep brain stimulation: a modeling study. J Neural Eng, 2008, 5(3): 263-274.
31. Ranck J B. Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res, 1975, 98(3): 417-440.
32. Lehnertz K, Bialonski S, Horstmann M T, et al. Synchronization phenomena in human epileptic brain networks. J Neurosci Methods, 2009, 183(1): 42-48.
33. Rubchinsky L L, Park C, Worth R M. Intermittent neural synchronization in Parkinson’s disease. Nonlinear Dyn, 2012, 68(3): 329-346.

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