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Prolonged stimulation with low-intensity ultrasound induces delayed increases in spontaneous hippocampal culture spiking activity

Kim, Hyun-Bum ; Swanberg, Kelley M LU orcid ; Han, Hee-Sok ; Kim, Jung-Chae ; Kim, Jun-Woo ; Lee, Sungon ; Lee, C Justin ; Maeng, Sungho ; Kim, Tae-Seong and Park, Ji-Ho (2017) In Journal of Neuroscience Research 95(3). p.885-896
Abstract

Ultrasound is a promising neural stimulation modality, but an incomplete understanding of its range and mechanism of effect limits its therapeutic application. We investigated the modulation of spontaneous hippocampal spike activity by ultrasound at a lower acoustic intensity and longer time scale than has been previously attempted, hypothesizing that spiking would change conditionally upon the availability of glutamate receptors. Using a 60-channel multielectrode array (MEA), we measured spontaneous spiking across organotypic rat hippocampal slice cultures (N = 28) for 3 min each before, during, and after stimulation with low-intensity unfocused pulsed or sham ultrasound (spatial-peak pulse average intensity 780 μW/cm2 ) preperfused... (More)

Ultrasound is a promising neural stimulation modality, but an incomplete understanding of its range and mechanism of effect limits its therapeutic application. We investigated the modulation of spontaneous hippocampal spike activity by ultrasound at a lower acoustic intensity and longer time scale than has been previously attempted, hypothesizing that spiking would change conditionally upon the availability of glutamate receptors. Using a 60-channel multielectrode array (MEA), we measured spontaneous spiking across organotypic rat hippocampal slice cultures (N = 28) for 3 min each before, during, and after stimulation with low-intensity unfocused pulsed or sham ultrasound (spatial-peak pulse average intensity 780 μW/cm2 ) preperfused with artificial cerebrospinal fluid, 300 μM kynurenic acid (KA), or 0.5 μM tetrodotoxin (TTX) at 3 ml/min. Spike rates were normalized and compared across stimulation type and period, subregion, threshold level, and/or perfusion condition using repeated-measures ANOVA and generalized linear mixed models. Normalized 3-min spike counts for large but not midsized, small, or total spikes increased after but not during ultrasound relative to sham stimulation. This result was recapitulated in subregions CA1 and dentate gyrus and replicated in a separate experiment for all spike size groups in slices pretreated with aCSF but not KA or TTX. Increases in normalized 18-sec total, midsized, and large spike counts peaked predominantly 1.5 min following ultrasound stimulation. Our low-intensity ultrasound setup exerted delayed glutamate receptor-dependent, amplitude- and possibly region-specific influences on spontaneous spike rates across the hippocampus, expanding the range of known parameters at which ultrasound may be used for neural activity modulation. © 2016 Wiley Periodicals, Inc.

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author
; ; ; ; ; ; ; ; and
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Action Potentials/drug effects, Animals, Animals, Newborn, Dose-Response Relationship, Radiation, Excitatory Amino Acid Agents/pharmacology, Hippocampus/cytology, In Vitro Techniques, Microelectrodes, Neurons/drug effects, Organ Culture Techniques, Rats, Receptors, Glutamate/metabolism, Sodium Channel Blockers/pharmacology, Temperature, Tetrodotoxin/pharmacology, Time Factors, Ultrasonics/methods
in
Journal of Neuroscience Research
volume
95
issue
3
pages
885 - 896
publisher
John Wiley & Sons Inc.
external identifiers
  • scopus:84979787267
  • pmid:27465511
ISSN
1097-4547
DOI
10.1002/jnr.23845
language
English
LU publication?
no
additional info
© 2016 Wiley Periodicals, Inc.
id
6c72143f-2476-40af-9395-207161e4b62a
date added to LUP
2023-09-18 15:03:17
date last changed
2024-03-22 00:16:33
@article{6c72143f-2476-40af-9395-207161e4b62a,
  abstract     = {{<p>Ultrasound is a promising neural stimulation modality, but an incomplete understanding of its range and mechanism of effect limits its therapeutic application. We investigated the modulation of spontaneous hippocampal spike activity by ultrasound at a lower acoustic intensity and longer time scale than has been previously attempted, hypothesizing that spiking would change conditionally upon the availability of glutamate receptors. Using a 60-channel multielectrode array (MEA), we measured spontaneous spiking across organotypic rat hippocampal slice cultures (N = 28) for 3 min each before, during, and after stimulation with low-intensity unfocused pulsed or sham ultrasound (spatial-peak pulse average intensity 780 μW/cm2 ) preperfused with artificial cerebrospinal fluid, 300 μM kynurenic acid (KA), or 0.5 μM tetrodotoxin (TTX) at 3 ml/min. Spike rates were normalized and compared across stimulation type and period, subregion, threshold level, and/or perfusion condition using repeated-measures ANOVA and generalized linear mixed models. Normalized 3-min spike counts for large but not midsized, small, or total spikes increased after but not during ultrasound relative to sham stimulation. This result was recapitulated in subregions CA1 and dentate gyrus and replicated in a separate experiment for all spike size groups in slices pretreated with aCSF but not KA or TTX. Increases in normalized 18-sec total, midsized, and large spike counts peaked predominantly 1.5 min following ultrasound stimulation. Our low-intensity ultrasound setup exerted delayed glutamate receptor-dependent, amplitude- and possibly region-specific influences on spontaneous spike rates across the hippocampus, expanding the range of known parameters at which ultrasound may be used for neural activity modulation. © 2016 Wiley Periodicals, Inc.</p>}},
  author       = {{Kim, Hyun-Bum and Swanberg, Kelley M and Han, Hee-Sok and Kim, Jung-Chae and Kim, Jun-Woo and Lee, Sungon and Lee, C Justin and Maeng, Sungho and Kim, Tae-Seong and Park, Ji-Ho}},
  issn         = {{1097-4547}},
  keywords     = {{Action Potentials/drug effects; Animals; Animals, Newborn; Dose-Response Relationship, Radiation; Excitatory Amino Acid Agents/pharmacology; Hippocampus/cytology; In Vitro Techniques; Microelectrodes; Neurons/drug effects; Organ Culture Techniques; Rats; Receptors, Glutamate/metabolism; Sodium Channel Blockers/pharmacology; Temperature; Tetrodotoxin/pharmacology; Time Factors; Ultrasonics/methods}},
  language     = {{eng}},
  number       = {{3}},
  pages        = {{885--896}},
  publisher    = {{John Wiley & Sons Inc.}},
  series       = {{Journal of Neuroscience Research}},
  title        = {{Prolonged stimulation with low-intensity ultrasound induces delayed increases in spontaneous hippocampal culture spiking activity}},
  url          = {{http://dx.doi.org/10.1002/jnr.23845}},
  doi          = {{10.1002/jnr.23845}},
  volume       = {{95}},
  year         = {{2017}},
}