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Hippocampal neurons respond to brain activity with functional hypoxia

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Hippocampal neurons respond to brain activity with functional hypoxia. / Butt, Umer Javed; Steixner-Kumar, Agnes A; Depp, Constanze; Sun, Ting; Hassouna, Imam; Wüstefeld, Liane; Arinrad, Sahab; Zillmann, Matthias R; Schopf, Nadine; Fernandez Garcia-Agudo, Laura; Mohrmann, Leonie; Bode, Ulli; Ronnenberg, Anja; Hindermann, Martin; Goebbels, Sandra; Bonn, Stefan; Katschinski, Dörthe M; Miskowiak, Kamilla W; Nave, Klaus-Armin; Ehrenreich, Hannelore.

In: MOL PSYCHIATR, Vol. 26, No. 6, 06.2021, p. 1790-1807.

Research output: SCORING: Contribution to journal › SCORING: Journal article › Research › peer-review

Harvard

Butt, UJ, Steixner-Kumar, AA, Depp, C, Sun, T, Hassouna, I, Wüstefeld, L, Arinrad, S, Zillmann, MR, Schopf, N, Fernandez Garcia-Agudo, L, Mohrmann, L, Bode, U, Ronnenberg, A, Hindermann, M, Goebbels, S, Bonn, S, Katschinski, DM, Miskowiak, KW, Nave, K-A & Ehrenreich, H 2021, 'Hippocampal neurons respond to brain activity with functional hypoxia', MOL PSYCHIATR, vol. 26, no. 6, pp. 1790-1807. https://doi.org/10.1038/s41380-020-00988-w

APA

Butt, U. J., Steixner-Kumar, A. A., Depp, C., Sun, T., Hassouna, I., Wüstefeld, L., Arinrad, S., Zillmann, M. R., Schopf, N., Fernandez Garcia-Agudo, L., Mohrmann, L., Bode, U., Ronnenberg, A., Hindermann, M., Goebbels, S., Bonn, S., Katschinski, D. M., Miskowiak, K. W., Nave, K-A., & Ehrenreich, H. (2021). Hippocampal neurons respond to brain activity with functional hypoxia. MOL PSYCHIATR, 26(6), 1790-1807. https://doi.org/10.1038/s41380-020-00988-w

Vancouver

Butt UJ, Steixner-Kumar AA, Depp C, Sun T, Hassouna I, Wüstefeld L et al. Hippocampal neurons respond to brain activity with functional hypoxia. MOL PSYCHIATR. 2021 Jun;26(6):1790-1807. https://doi.org/10.1038/s41380-020-00988-w

Bibtex

@article{c0a2628fbd5b4c94a447f14716f68e40,
title = "Hippocampal neurons respond to brain activity with functional hypoxia",
abstract = "Physical activity and cognitive challenge are established non-invasive methods to induce comprehensive brain activation and thereby improve global brain function including mood and emotional well-being in healthy subjects and in patients. However, the mechanisms underlying this experimental and clinical observation and broadly exploited therapeutic tool are still widely obscure. Here we show in the behaving brain that physiological (endogenous) hypoxia is likely a respective lead mechanism, regulating hippocampal plasticity via adaptive gene expression. A refined transgenic approach in mice, utilizing the oxygen-dependent degradation (ODD) domain of HIF-1α fused to CreERT2 recombinase, allows us to demonstrate hypoxic cells in the performing brain under normoxia and motor-cognitive challenge, and spatially map them by light-sheet microscopy, all in comparison to inspiratory hypoxia as strong positive control. We report that a complex motor-cognitive challenge causes hypoxia across essentially all brain areas, with hypoxic neurons particularly abundant in the hippocampus. These data suggest an intriguing model of neuroplasticity, in which a specific task-associated neuronal activity triggers mild hypoxia as a local neuron-specific as well as a brain-wide response, comprising indirectly activated neurons and non-neuronal cells.",
author = "Butt, {Umer Javed} and Steixner-Kumar, {Agnes A} and Constanze Depp and Ting Sun and Imam Hassouna and Liane W{\"u}stefeld and Sahab Arinrad and Zillmann, {Matthias R} and Nadine Schopf and {Fernandez Garcia-Agudo}, Laura and Leonie Mohrmann and Ulli Bode and Anja Ronnenberg and Martin Hindermann and Sandra Goebbels and Stefan Bonn and Katschinski, {D{\"o}rthe M} and Miskowiak, {Kamilla W} and Klaus-Armin Nave and Hannelore Ehrenreich",
year = "2021",
month = jun,
doi = "10.1038/s41380-020-00988-w",
language = "English",
volume = "26",
pages = "1790--1807",
journal = "MOL PSYCHIATR",
issn = "1359-4184",
publisher = "NATURE PUBLISHING GROUP",
number = "6",

}

RIS

TY - JOUR

T1 - Hippocampal neurons respond to brain activity with functional hypoxia

AU - Butt, Umer Javed

AU - Steixner-Kumar, Agnes A

AU - Depp, Constanze

AU - Sun, Ting

AU - Hassouna, Imam

AU - Wüstefeld, Liane

AU - Arinrad, Sahab

AU - Zillmann, Matthias R

AU - Schopf, Nadine

AU - Fernandez Garcia-Agudo, Laura

AU - Mohrmann, Leonie

AU - Bode, Ulli

AU - Ronnenberg, Anja

AU - Hindermann, Martin

AU - Goebbels, Sandra

AU - Bonn, Stefan

AU - Katschinski, Dörthe M

AU - Miskowiak, Kamilla W

AU - Nave, Klaus-Armin

AU - Ehrenreich, Hannelore

PY - 2021/6

Y1 - 2021/6

N2 - Physical activity and cognitive challenge are established non-invasive methods to induce comprehensive brain activation and thereby improve global brain function including mood and emotional well-being in healthy subjects and in patients. However, the mechanisms underlying this experimental and clinical observation and broadly exploited therapeutic tool are still widely obscure. Here we show in the behaving brain that physiological (endogenous) hypoxia is likely a respective lead mechanism, regulating hippocampal plasticity via adaptive gene expression. A refined transgenic approach in mice, utilizing the oxygen-dependent degradation (ODD) domain of HIF-1α fused to CreERT2 recombinase, allows us to demonstrate hypoxic cells in the performing brain under normoxia and motor-cognitive challenge, and spatially map them by light-sheet microscopy, all in comparison to inspiratory hypoxia as strong positive control. We report that a complex motor-cognitive challenge causes hypoxia across essentially all brain areas, with hypoxic neurons particularly abundant in the hippocampus. These data suggest an intriguing model of neuroplasticity, in which a specific task-associated neuronal activity triggers mild hypoxia as a local neuron-specific as well as a brain-wide response, comprising indirectly activated neurons and non-neuronal cells.

AB - Physical activity and cognitive challenge are established non-invasive methods to induce comprehensive brain activation and thereby improve global brain function including mood and emotional well-being in healthy subjects and in patients. However, the mechanisms underlying this experimental and clinical observation and broadly exploited therapeutic tool are still widely obscure. Here we show in the behaving brain that physiological (endogenous) hypoxia is likely a respective lead mechanism, regulating hippocampal plasticity via adaptive gene expression. A refined transgenic approach in mice, utilizing the oxygen-dependent degradation (ODD) domain of HIF-1α fused to CreERT2 recombinase, allows us to demonstrate hypoxic cells in the performing brain under normoxia and motor-cognitive challenge, and spatially map them by light-sheet microscopy, all in comparison to inspiratory hypoxia as strong positive control. We report that a complex motor-cognitive challenge causes hypoxia across essentially all brain areas, with hypoxic neurons particularly abundant in the hippocampus. These data suggest an intriguing model of neuroplasticity, in which a specific task-associated neuronal activity triggers mild hypoxia as a local neuron-specific as well as a brain-wide response, comprising indirectly activated neurons and non-neuronal cells.

U2 - 10.1038/s41380-020-00988-w

DO - 10.1038/s41380-020-00988-w

M3 - SCORING: Journal article

C2 - 33564132

VL - 26

SP - 1790

EP - 1807

JO - MOL PSYCHIATR

JF - MOL PSYCHIATR

SN - 1359-4184

IS - 6

ER -