Selective modulation of neuronal firing by pulse stimulations with different frequencies in rat hippocampus

Abstract Background Deep brain stimulation (DBS) has a good prospect for treating many brain diseases. Recent studies have shown that axonal activation induced by pulse stimulations may play an important role in DBS therapies through wide projections of axonal fibers. However, it is undetermined whe...

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Main Authors: Chen Qiu, Zhouyan Feng, Lvpiao Zheng, Weijian Ma
Format: Article
Language:English
Published: BMC 2019-07-01
Series:BioMedical Engineering OnLine
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12938-019-0700-z
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author Chen Qiu
Zhouyan Feng
Lvpiao Zheng
Weijian Ma
author_facet Chen Qiu
Zhouyan Feng
Lvpiao Zheng
Weijian Ma
author_sort Chen Qiu
collection DOAJ
description Abstract Background Deep brain stimulation (DBS) has a good prospect for treating many brain diseases. Recent studies have shown that axonal activation induced by pulse stimulations may play an important role in DBS therapies through wide projections of axonal fibers. However, it is undetermined whether the downstream neurons are inhibited or excited by axonal stimulation. The present study addressed the question in rat hippocampus by in vivo experiments. Methods Pulse stimulations with different frequencies (10–400 Hz) were applied to the Schaffer collateral, the afferent fiber of hippocampal CA1 region in anaesthetized rats. Single-unit spikes of interneurons and pyramidal cells in the downstream region of stimulation were recorded and evaluated. Results Stimulations with a lower frequency (10 or 20 Hz) did not change the firing rates of interneurons but decreased the firing rates of pyramidal cells (the principal neurons) significantly. The phase-locked firing of interneurons during these stimulations might increase the efficacy of GABAergic inhibitions on the principal neurons. However, stimulations with a higher frequency (100–400 Hz) increased the firing rates of both types of the neurons significantly. In addition, the increases of interneurons’ firing were greater than the increases of pyramidal cells. Presumably, increase of direct excitation from afferent impulses together with failure of GABAergic inhibition might result in the increase of pyramidal cells’ firing by a higher stimulation frequency. Furthermore, silent periods appeared immediately following the cessation of stimulations, indicating a full control of the neuronal firing by the stimulation pulses during axonal stimulation. Furthermore longer silent periods were associated with higher stimulation frequencies. Conclusions Low-frequency (10–20 Hz) and high-frequency (100–400 Hz) stimulations of afferent axonal fibers exerted opposite effects on principal neurons in rat hippocampus CA1. These results provide new information for advancing deep brain stimulation to treat different brain disorders.
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spelling doaj.art-8d6bcd9e4a1b45d48f02f9fa32d33ac62022-12-21T18:53:48ZengBMCBioMedical Engineering OnLine1475-925X2019-07-0118111310.1186/s12938-019-0700-zSelective modulation of neuronal firing by pulse stimulations with different frequencies in rat hippocampusChen Qiu0Zhouyan Feng1Lvpiao Zheng2Weijian Ma3Key Laboratory of Biomedical Engineering of Education Ministry, College of Biomedical Engineering and Instrumentation Science, Zhejiang UniversityKey Laboratory of Biomedical Engineering of Education Ministry, College of Biomedical Engineering and Instrumentation Science, Zhejiang UniversityKey Laboratory of Biomedical Engineering of Education Ministry, College of Biomedical Engineering and Instrumentation Science, Zhejiang UniversityKey Laboratory of Biomedical Engineering of Education Ministry, College of Biomedical Engineering and Instrumentation Science, Zhejiang UniversityAbstract Background Deep brain stimulation (DBS) has a good prospect for treating many brain diseases. Recent studies have shown that axonal activation induced by pulse stimulations may play an important role in DBS therapies through wide projections of axonal fibers. However, it is undetermined whether the downstream neurons are inhibited or excited by axonal stimulation. The present study addressed the question in rat hippocampus by in vivo experiments. Methods Pulse stimulations with different frequencies (10–400 Hz) were applied to the Schaffer collateral, the afferent fiber of hippocampal CA1 region in anaesthetized rats. Single-unit spikes of interneurons and pyramidal cells in the downstream region of stimulation were recorded and evaluated. Results Stimulations with a lower frequency (10 or 20 Hz) did not change the firing rates of interneurons but decreased the firing rates of pyramidal cells (the principal neurons) significantly. The phase-locked firing of interneurons during these stimulations might increase the efficacy of GABAergic inhibitions on the principal neurons. However, stimulations with a higher frequency (100–400 Hz) increased the firing rates of both types of the neurons significantly. In addition, the increases of interneurons’ firing were greater than the increases of pyramidal cells. Presumably, increase of direct excitation from afferent impulses together with failure of GABAergic inhibition might result in the increase of pyramidal cells’ firing by a higher stimulation frequency. Furthermore, silent periods appeared immediately following the cessation of stimulations, indicating a full control of the neuronal firing by the stimulation pulses during axonal stimulation. Furthermore longer silent periods were associated with higher stimulation frequencies. Conclusions Low-frequency (10–20 Hz) and high-frequency (100–400 Hz) stimulations of afferent axonal fibers exerted opposite effects on principal neurons in rat hippocampus CA1. These results provide new information for advancing deep brain stimulation to treat different brain disorders.http://link.springer.com/article/10.1186/s12938-019-0700-zElectrical pulse stimulationHippocampal CA1 regionInterneuronsPyramidal cellsUnit spikeStimulation frequency
spellingShingle Chen Qiu
Zhouyan Feng
Lvpiao Zheng
Weijian Ma
Selective modulation of neuronal firing by pulse stimulations with different frequencies in rat hippocampus
BioMedical Engineering OnLine
Electrical pulse stimulation
Hippocampal CA1 region
Interneurons
Pyramidal cells
Unit spike
Stimulation frequency
title Selective modulation of neuronal firing by pulse stimulations with different frequencies in rat hippocampus
title_full Selective modulation of neuronal firing by pulse stimulations with different frequencies in rat hippocampus
title_fullStr Selective modulation of neuronal firing by pulse stimulations with different frequencies in rat hippocampus
title_full_unstemmed Selective modulation of neuronal firing by pulse stimulations with different frequencies in rat hippocampus
title_short Selective modulation of neuronal firing by pulse stimulations with different frequencies in rat hippocampus
title_sort selective modulation of neuronal firing by pulse stimulations with different frequencies in rat hippocampus
topic Electrical pulse stimulation
Hippocampal CA1 region
Interneurons
Pyramidal cells
Unit spike
Stimulation frequency
url http://link.springer.com/article/10.1186/s12938-019-0700-z
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AT zhouyanfeng selectivemodulationofneuronalfiringbypulsestimulationswithdifferentfrequenciesinrathippocampus
AT lvpiaozheng selectivemodulationofneuronalfiringbypulsestimulationswithdifferentfrequenciesinrathippocampus
AT weijianma selectivemodulationofneuronalfiringbypulsestimulationswithdifferentfrequenciesinrathippocampus