In vivo imaging of calcium and glutamate responses to intracortical microstimulation reveals distinct temporal responses of the neuropil and somatic compartments in layer II/III neurons.
Brain stimulation
Brain-computer interface
Calcium imaging
GCaMP6
Neuromodulation
iGluSnFr
Journal
Biomaterials
ISSN: 1878-5905
Titre abrégé: Biomaterials
Pays: Netherlands
ID NLM: 8100316
Informations de publication
Date de publication:
03 2020
03 2020
Historique:
received:
03
09
2019
revised:
22
12
2019
accepted:
05
01
2020
pubmed:
19
1
2020
medline:
15
5
2021
entrez:
19
1
2020
Statut:
ppublish
Résumé
Intracortical microelectrode implants can generate a tissue response hallmarked by glial scarring and neuron cell death within 100-150 μm of the biomaterial device. Many have proposed that any performance decline in intracortical microstimulation (ICMS) due to this foreign body tissue response could be offset by increasing the stimulation amplitude. The mechanisms of this approach are unclear, however, as there has not been consensus on how increasing amplitude affects the spatial and temporal recruitment patterns of ICMS. We clarify these unknowns using in vivo two-photon imaging of mice transgenically expressing the calcium sensor GCaMP6s in Thy1 neurons or virally expressing the glutamate sensor iGluSnFr in neurons. Calcium and neurotransmitter activity are tracked in the neuronal somas and neuropil during long-train stimulation in Layer II/III of somatosensory cortex. Neural calcium activity and glutamate release are dense and strongest within 20-40 μm around the electrode, falling off with distance from the electrode. Neuronal calcium increases with higher amplitude stimulations. During prolonged stimulation trains, a sub-population of somas fail to maintain calcium activity. Interestingly, neuropil calcium activity is 3-fold less correlated to somatic calcium activity for cells that drop-out during the long stimulation train compared to cells that sustain activity throughout the train. Glutamate release is apparent only within 20 μm of the electrode and is sustained for at least 10s after cessation of the 15 and 20 μA stimulation train, but not lower amplitudes. These results demonstrate that increasing amplitude can increase the radius and intensity of neural recruitment, but it also alters the temporal response of some neurons. Further, dense glutamate release is highest within the first 20 μm of the electrode site even at high amplitudes, suggesting that there may be spatial limitations to the amplitude parameter space. The glutamate elevation outlasts stimulation, suggesting that high-amplitude stimulation may affect neurotransmitter re-uptake. This ultimately suggests that increasing the amplitude of ICMS device stimulation may fundamentally alter the temporal neural response, which could have implications for using amplitude to improve the ICMS effect or "offset" the effects of glial scarring.
Identifiants
pubmed: 31954232
pii: S0142-9612(20)30013-2
doi: 10.1016/j.biomaterials.2020.119767
pmc: PMC7487166
mid: NIHMS1625791
pii:
doi:
Substances chimiques
Glutamic Acid
3KX376GY7L
Calcium
SY7Q814VUP
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
119767Subventions
Organisme : NINDS NIH HHS
ID : R01 NS094396
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS105691
Pays : United States
Organisme : NINDS NIH HHS
ID : R21 NS108098
Pays : United States
Informations de copyright
Copyright © 2020 Elsevier Ltd. All rights reserved.
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