Repetitive Magnetic Stimulation Induces Functional and Structural Plasticity of Excitatory Postsynapses in Mouse Organotypic Hippocampal Slice Cultures

Repetitive transcranial magnetic stimulation (rTMS) is a noninvasive brain stimulation technique that can alter cortical excitability in human subjects for hours beyond the stimulation period. It thus has potential as a therapeutic tool in neuropsychiatric disorders associated with alterations in co...

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Published inThe Journal of neuroscience Vol. 32; no. 48; pp. 17514 - 17523
Main Authors Vlachos, Andreas, Müller-Dahlhaus, Florian, Rosskopp, Johannes, Lenz, Maximilian, Ziemann, Ulf, Deller, Thomas
Format Journal Article
LanguageEnglish
Published United States Society for Neuroscience 28.11.2012
Subjects
Animals
Dendritic Spines - physiology
Excitatory Postsynaptic Potentials - physiology
Hippocampus - cytology
Hippocampus - physiology
Mice
Miniature Postsynaptic Potentials - physiology
Neuronal Plasticity - physiology
Neurons - cytology
Neurons - physiology
Patch-Clamp Techniques
Synapses - physiology
Synaptic Transmission - physiology
Transcranial Magnetic Stimulation
Online AccessGet full text
ISSN0270-6474
1529-2401
1529-2401
DOI10.1523/JNEUROSCI.0409-12.2012

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Abstract Repetitive transcranial magnetic stimulation (rTMS) is a noninvasive brain stimulation technique that can alter cortical excitability in human subjects for hours beyond the stimulation period. It thus has potential as a therapeutic tool in neuropsychiatric disorders associated with alterations in cortical excitability. However, rTMS-induced neural plasticity remains insufficiently understood at the cellular level. To learn more about the effects of repetitive magnetic stimulation (rMS), we established an in vitro model of rMS using mouse organotypic entorhino-hippocampal slice cultures. We assessed the outcome of a high-frequency (10 Hz) rMS protocol on functional and structural properties of excitatory synapses in mature hippocampal CA1 pyramidal neurons. Whole-cell patch-clamp recordings, immunohistochemistry, and time-lapse imaging techniques revealed that rMS induces a long-lasting increase in glutamatergic synaptic strength, which is accompanied by structural remodeling of dendritic spines. The effects of rMS on spine size were predominantly seen in small spines, suggesting differential effects of rMS on subpopulations of spines. Furthermore, our data indicate that rMS-induced postsynaptic changes depend on the NMDA receptor-mediated accumulation of GluA1-containing AMPA receptors. These results provide first experimental evidence that rMS induces coordinated functional and structural plasticity of excitatory postsynapses, which is consistent with a long-term potentiation of synaptic transmission.
AbstractList Repetitive transcranial magnetic stimulation (rTMS) is a noninvasive brain stimulation technique that can alter cortical excitability in human subjects for hours beyond the stimulation period. It thus has potential as a therapeutic tool in neuropsychiatric disorders associated with alterations in cortical excitability. However, rTMS-induced neural plasticity remains insufficiently understood at the cellular level. To learn more about the effects of repetitive magnetic stimulation (rMS), we established an in vitro model of rMS using mouse organotypic entorhino-hippocampal slice cultures. We assessed the outcome of a high-frequency (10 Hz) rMS protocol on functional and structural properties of excitatory synapses in mature hippocampal CA1 pyramidal neurons. Whole-cell patch-clamp recordings, immunohistochemistry, and time-lapse imaging techniques revealed that rMS induces a long-lasting increase in glutamatergic synaptic strength, which is accompanied by structural remodeling of dendritic spines. The effects of rMS on spine size were predominantly seen in small spines, suggesting differential effects of rMS on subpopulations of spines. Furthermore, our data indicate that rMS-induced postsynaptic changes depend on the NMDA receptor-mediated accumulation of GluA1-containing AMPA receptors. These results provide first experimental evidence that rMS induces coordinated functional and structural plasticity of excitatory postsynapses, which is consistent with a long-term potentiation of synaptic transmission.
Repetitive transcranial magnetic stimulation (rTMS) is a noninvasive brain stimulation technique that can alter cortical excitability in human subjects for hours beyond the stimulation period. It thus has potential as a therapeutic tool in neuropsychiatric disorders associated with alterations in cortical excitability. However, rTMS-induced neural plasticity remains insufficiently understood at the cellular level. To learn more about the effects of repetitive magnetic stimulation (rMS), we established an in vitro model of rMS using mouse organotypic entorhino-hippocampal slice cultures. We assessed the outcome of a high-frequency (10 Hz) rMS protocol on functional and structural properties of excitatory synapses in mature hippocampal CA1 pyramidal neurons. Whole-cell patch-clamp recordings, immunohistochemistry, and time-lapse imaging techniques revealed that rMS induces a long-lasting increase in glutamatergic synaptic strength, which is accompanied by structural remodeling of dendritic spines. The effects of rMS on spine size were predominantly seen in small spines, suggesting differential effects of rMS on subpopulations of spines. Furthermore, our data indicate that rMS-induced postsynaptic changes depend on the NMDA receptor-mediated accumulation of GluA1-containing AMPA receptors. These results provide first experimental evidence that rMS induces coordinated functional and structural plasticity of excitatory postsynapses, which is consistent with a long-term potentiation of synaptic transmission.
Repetitive transcranial magnetic stimulation (rTMS) is a noninvasive brain stimulation technique that can alter cortical excitability in human subjects for hours beyond the stimulation period. It thus has potential as a therapeutic tool in neuropsychiatric disorders associated with alterations in cortical excitability. However, rTMS-induced neural plasticity remains insufficiently understood at the cellular level. To learn more about the effects of repetitive magnetic stimulation (rMS), we established an in vitro model of rMS using mouse organotypic entorhino-hippocampal slice cultures. We assessed the outcome of a high-frequency (10 Hz) rMS protocol on functional and structural properties of excitatory synapses in mature hippocampal CA1 pyramidal neurons. Whole-cell patch-clamp recordings, immunohistochemistry, and time-lapse imaging techniques revealed that rMS induces a long-lasting increase in glutamatergic synaptic strength, which is accompanied by structural remodeling of dendritic spines. The effects of rMS on spine size were predominantly seen in small spines, suggesting differential effects of rMS on subpopulations of spines. Furthermore, our data indicate that rMS-induced postsynaptic changes depend on the NMDA receptor-mediated accumulation of GluA1-containing AMPA receptors. These results provide first experimental evidence that rMS induces coordinated functional and structural plasticity of excitatory postsynapses, which is consistent with a long-term potentiation of synaptic transmission.Repetitive transcranial magnetic stimulation (rTMS) is a noninvasive brain stimulation technique that can alter cortical excitability in human subjects for hours beyond the stimulation period. It thus has potential as a therapeutic tool in neuropsychiatric disorders associated with alterations in cortical excitability. However, rTMS-induced neural plasticity remains insufficiently understood at the cellular level. To learn more about the effects of repetitive magnetic stimulation (rMS), we established an in vitro model of rMS using mouse organotypic entorhino-hippocampal slice cultures. We assessed the outcome of a high-frequency (10 Hz) rMS protocol on functional and structural properties of excitatory synapses in mature hippocampal CA1 pyramidal neurons. Whole-cell patch-clamp recordings, immunohistochemistry, and time-lapse imaging techniques revealed that rMS induces a long-lasting increase in glutamatergic synaptic strength, which is accompanied by structural remodeling of dendritic spines. The effects of rMS on spine size were predominantly seen in small spines, suggesting differential effects of rMS on subpopulations of spines. Furthermore, our data indicate that rMS-induced postsynaptic changes depend on the NMDA receptor-mediated accumulation of GluA1-containing AMPA receptors. These results provide first experimental evidence that rMS induces coordinated functional and structural plasticity of excitatory postsynapses, which is consistent with a long-term potentiation of synaptic transmission.
Author Lenz, Maximilian
Müller-Dahlhaus, Florian
Rosskopp, Johannes
Deller, Thomas
Vlachos, Andreas
Ziemann, Ulf
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  surname: Ziemann
  fullname: Ziemann, Ulf
– sequence: 6
  givenname: Thomas
  surname: Deller
  fullname: Deller, Thomas
BackLink https://www.ncbi.nlm.nih.gov/pubmed/23197741$$D View this record in MEDLINE/PubMed
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A.V. and F.M.-D. contributed equally to this work.
Author contributions: A.V., F.M.-D., U.Z., and T.D. designed research; A.V., F.M.-D., J.R., and M.L. performed research; A.V., F.M.-D., J.R., and M.L. analyzed data; A.V., F.M.-D., U.Z., and T.D. wrote the paper.
U.Z. and T.D. contributed equally to this work.
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Snippet Repetitive transcranial magnetic stimulation (rTMS) is a noninvasive brain stimulation technique that can alter cortical excitability in human subjects for...
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SubjectTerms Animals
Dendritic Spines - physiology
Excitatory Postsynaptic Potentials - physiology
Hippocampus - cytology
Hippocampus - physiology
Mice
Miniature Postsynaptic Potentials - physiology
Neuronal Plasticity - physiology
Neurons - cytology
Neurons - physiology
Patch-Clamp Techniques
Synapses - physiology
Synaptic Transmission - physiology
Transcranial Magnetic Stimulation
Title Repetitive Magnetic Stimulation Induces Functional and Structural Plasticity of Excitatory Postsynapses in Mouse Organotypic Hippocampal Slice Cultures
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