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1. A consensus protocol for functional connectivity analysis in the rat brain

Author

Grandjean, J., Desrosiers-Gregoire, G., Anckaerts, C., Angeles-Valdez, D., Ayad, F., Barrière, D., Blockx, I., Bortel, A., Broadwater, M., Cardoso, B., Célestine, M., Chavez-Negrete, J., Choi, S., Christiaen, E., Clavijo, P., Colon-Perez, L., Cramer, S., Daniele, T., Dempsey, E., Diao, Y., Doelemeyer, A., Dopfel, D., Dvořáková, L., Falfán-Melgoza, C., Fernandes, F., Fowler, C., Fuentes-Ibañez, A., Garin, C., Gelderman, E., Golden, C., Guo, C., Henckens, M., Hennessy, L., Herman , P., Hofwijks, N., Horien, C., Ionescu, T., Jones, J., Kaesser, J., Kim, E., Lambers, H., Lazari, A., Lee, S., Lillywhite, A., Liu, Y., López-Castro, A., López-Gil , X., Ma, Z., MacNicol, E., Madularu, D., Mandino, F., Marciano, S., McAuslan, M., McCunn, P., McIntosh, A., Meng, X., Meyer-Baese, L., Missault, S., Moro, F., Naessens, D., Nava-Gomez, L., Nonaka, H., Ortiz, J., Paasonen, J., Pais-Roldán, P., Peeters, L., Pereira, M., Perez, P., Pompilus, M., Prior, M., Rakhmatullin, R., Reimann, H., Reinwald, J., Triana Del Rio, R., Rivera-Olvera, A., Ruiz-Pérez, D., Russo, G., Rutten, T., Ryoke, R., Sack, M., Salvan, P., Sanganahalli, B., Schroeter, A., Seewoo , B., Selingue, E., Seuwen, A., Shi, B., Sirmpilatze, N., Smith, J., Smith, C., Sobczak, F., Stenroos, P., Straathof, M., Strobelt, S., Sumiyoshi, A., Takahashi, K., Torres-García, M., Tudela, R., van den Berg, M., van der Marel, K., van Hout, A., Vertullo, R., Vidal, B., Vrooman, R., Wang, X., Wank, I., Watson, D., Yin, T., Zhang, Y., Zurbruegg, S., Achard, S., Alcauter, S., Auer, D., Barbier, E., Baudewig, J., Beckmann, C., Beckmann, N., Becq, G., Blezer, E., Bolbos, R., Boretius, S., Bouvard, S., Budinger, E., Buxbaum, J., Cash, D., Chapman, V., Chuang, K., Ciobanu, L., Coolen, B., Dalley, J., Dhenain, M., Dijkhuizen, R., Esteban, O., Faber, C., Febo, M., Feindel, K., Forloni, G., Fouquet, J., Garza-Villarreal, E., Gass, N., Glennon, J., Gozzi, A., Gröhn, O., Harkin, A., Heerschap, A., Helluy, X., Herfert , K., Heuser, A., Homberg, J., Houwing, D., Hyder, F., Ielacqua, G., Jelescu, I., Johansen-Berg, H., Kaneko, G., Kawashima, R., Keilholz, S., Keliris, G., Kelly, C., Kerskens, C., Khokhar, J., Kind, P., Langlois, J., Lerch, J., López-Hidalgo, M., Manahan-Vaughan, D., Marchand, F., Mars, R., Marsella, G., Micotti , E., Muñoz-Moreno , E., Near, J., Niendorf, T., Otte, W., Pan , W., Prado-Alcalá, R., Quirarte, G., Rodger , J., Rosenow, T., Sampaio-Baptista, C., Sartorius, A., Sawiak, S., Scheenen, T., Shemesh, Shih, Y., Shmuel, A., Soria, G., Stoop, R., Thompson, G., Till, S., Todd, N., Van Der Linden, A., van der Toorn, A., van Tilborg, G., Vanhove, C., Veltien, A., Verhoye, M., Wachsmuth, L., Weber-Fahr, W., Wenk , P., Yu, X., Zerbi , V., Zhang , N., Zhang, B., Zimmer, L., Devenyi, G., Chakravarty, M., and Hess, A.

Subjects
Action, intention, and motor control, General Neuroscience, fmri, Medizin, Stress-related disorders Donders Center for Medical Neuroscience [Radboudumc 13], Human medicine
Abstract

Task-free functional connectivity in animal models provides an experimental framework to examine connectivity phenomena under controlled conditions and allows for comparisons with data modalities collected under invasive or terminal procedures. Currently, animal acquisitions are performed with varying protocols and analyses that hamper result comparison and integration. Here we introduce StandardRat, a consensus rat functional magnetic resonance imaging acquisition protocol tested across 20 centers. To develop this protocol with optimized acquisition and processing parameters, we initially aggregated 65 functional imaging datasets acquired from rats across 46 centers. We developed a reproducible pipeline for analyzing rat data acquired with diverse protocols and determined experimental and processing parameters associated with the robust detection of functional connectivity across centers. We show that the standardized protocol enhances biologically plausible functional connectivity patterns relative to previous acquisitions. The protocol and processing pipeline described here is openly shared with the neuroimaging community to promote interoperability and cooperation toward tackling the most important challenges in neuroscience. The authors pooled resources to identify best practices and develop a new standardized protocol for estimating functional connectivity in rats with magnetic resonance imaging.

Published
2023

2. Author Correction: A consensus protocol for functional connectivity analysis in the rat brain

Author

Grandjean, J., Desrosiers-Gregoire, G., Anckaerts, C., Angeles-Valdez, D., Ayad, F., Barrière, D., Blockx, I., Bortel, A., Broadwater, M., Cardoso, B., Célestine, M., Chavez-Negrete, J., Choi, S., https://orcid.org/0000-0001-7327-1344, Christiaen, E., Clavijo, P., Colon-Perez, L., Cramer, S., Daniele, T., Dempsey, E., Diao, Y., Doelemeyer, A., Dopfel, D., Dvořáková, L., Falfán-Melgoza, C., Fernandes, F., Fowler, C., Fuentes-Ibañez, A., Garin, C., Gelderman, E., Golden, C., Guo, C., Henckens, M., Hennessy, L., Herman , P., Hofwijks, N., Horien, C., Ionescu, T., Jones, J., Kaesser, J., Kim, E., Lambers, H., Lazari, A., Lee, S., Lillywhite, A., Liu, Y., López-Castro, A., López-Gil , X., Ma, Z., MacNicol, E., Madularu, D., Mandino, F., Marciano, S., McAuslan, M., McCunn, P., McIntosh, A., Meng, X., Meyer-Baese, L., Missault, S., Moro, F., Naessens, D., Nava-Gomez, L., Nonaka, H., Ortiz, J., Paasonen, J., Pais-Roldán, P., https://orcid.org/0000-0002-9381-3048, Peeters, L., Pereira, M., Perez, P., Pompilus, M., Prior, M., Rakhmatullin, R., Reimann, H., Reinwald, J., Triana Del Rio, R., Rivera-Olvera, A., Ruiz-Pérez, D., Russo, G., Rutten, T., Ryoke, R., Sack, M., Salvan, P., Sanganahalli, B., Schroeter, A., Seewoo , B., Selingue, E., Seuwen, A., Shi, B., Sirmpilatze, N., Smith, J., Smith, C., Sobczak, F., Stenroos, P., Straathof, M., Strobelt, S., Sumiyoshi, A., Takahashi, K., Torres-García, M., Tudela, R., van den Berg, M., van der Marel, K., van Hout, A., Vertullo, R., Vidal, B., Vrooman, R., Wang, X., Wank, I., Watson, D., Yin, T., Zhang, Y., Zurbruegg, S., Achard, S., Alcauter, S., Auer, D., Barbier, E., Baudewig, J., Beckmann, C., Beckmann, N., Becq, G., Blezer, E., Bolbos, R., Boretius, S., Bouvard, S., Budinger, E., Buxbaum, J., Cash, D., Chapman, V., Chuang, K., Ciobanu, L., Coolen, B., Dalley, J., Dhenain, M., Dijkhuizen, R., Esteban, O., Faber, C., Febo, M., Feindel, K., Forloni, G., Fouquet, J., Garza-Villarreal, E., Gass, N., Glennon, J., Gozzi, A., Gröhn, O., Harkin, A., Heerschap, A., Helluy, X., Herfert , K., Heuser, A., Homberg, J., Houwing, D., Hyder, F., Ielacqua, G., Jelescu, I., Johansen-Berg, H., Kaneko, G., Kawashima, R., Keilholz, S., Keliris, G., Kelly, C., Kerskens, C., Khokhar, J., Kind, P., Langlois, J., Lerch, J., López-Hidalgo, M., Manahan-Vaughan, D., Marchand, F., Mars, R., Marsella, G., Micotti , E., Muñoz-Moreno , E., Near, J., Niendorf, T., Otte, W., Pan , W., Prado-Alcalá, R., Quirarte, G., Rodger , J., Rosenow, T., Sampaio-Baptista, C., Sartorius, A., Sawiak, S., Scheenen, T., Shemesh, Shih, Y., Shmuel, A., https://orcid.org/0000-0003-3028-6639, Soria, G., Stoop, R., https://orcid.org/0000-0002-3532-1512, Thompson, G., Till, S., Todd, N., Van Der Linden, A., van der Toorn, A., van Tilborg, G., Vanhove, C., Veltien, A., Verhoye, M., Wachsmuth, L., Weber-Fahr, W., Wenk , P., Yu, X., Zerbi , V., Zhang , N., Zhang, B., Zimmer, L., Devenyi, G., Chakravarty, M., and Hess, A.

Subjects
General Neuroscience, Medizin
Abstract

Weitere Nicht-UDE Autoren sind nicht mit aufgeführt. in press

Published
2023

3. New rat model of spinal cord infarction with long-lasting functional disabilities generated by intraspinal injection of endothelin-1.

Author

Otani M, Kushida Y, Kuroda Y, Wakao S, Oguma Y, Sasaki K, Katahira S, Terai R, Ryoke R, Nonaka H, Kawashima R, Saiki Y, and Dezawa M

Abstract

Background: The current method for generating an animal model of spinal cord (SC) infarction is highly invasive and permits only short-term observation, typically limited to 28 days., Objective: We aimed to establish a rat model characterised by long-term survival and enduring SC dysfunction by inducing selective ischaemic SC damage., Methods: In 8-week-old male Wistar rats, a convection-enhanced delivery technique was applied to selectively deliver endothelin-1 (ET-1) to the anterior horn of the SC at the Th13 level, leading to SC infarction. The Basso, Beattie and Bresnahan (BBB) locomotor score was assessed for 56 days. The SC was examined by a laser tissue blood flowmeter, MRI, immunohistochemistry, triphenyl tetrazolium chloride (TTC) staining, Western blots and TUNEL staining., Results: The puncture method was used to bilaterally inject 0.7 µL ET-1 (2.5 mg/mL) from the lateral SC into the anterior horns (40° angle, 1.5 mm depth) near the posterior root origin. Animals survived until day 56 and the BBB score was stably maintained (5.5±1.0 at day 14 and 6.2±1.0 at day 56). Rats with BBB scores ≤1 on day 1 showed stable scores of 5-6 after day 14 until day 56 while rats with BBB scores >1 on day 1 exhibited only minor dysfunction with BBB scores >12 after day 14. TTC staining, immunostaining and TUNEL staining revealed selective ischaemia and neuronal cell death in the anterior horn. T2-weighted MR images showed increasing signal intensity at the SC infarction site over time. Western blots revealed apoptosis and subsequent inflammation in SC tissue after ET-1 administration., Conclusions: Selective delivery of ET-1 into the SC allows for more precise localisation of the infarcted area at the targeted site and generates a rat SC infarction model with stable neurological dysfunction lasting 56 days., Competing Interests: Competing interests: None declared., (© Author(s) (or their employer(s)) 2024. Re-use permitted under CC BY-NC. No commercial re-use. See rights and permissions. Published by BMJ.)

Published
2024
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4. Multiple Stressors Induce Amygdalohippocampal Volume Reduction in Adult Male Rats as Detected by Longitudinal Structural Magnetic Resonance Imaging.

Author

Ryoke R, Hashimoto T, and Kawashima R

Abstract

Background: Traumatic events can cause long-lasting and uncontrollable fear and anxiety. Posttraumatic stress disorder is an intractable mental disorder, and neurobiological mechanisms using animal models are expected to help development of posttraumatic stress disorder treatment. In this study, we combined multiple stress (MS) and longitudinal in vivo magnetic resonance imaging to reveal the effects of long-lasting anxiety-like behaviors on adult male rat brains., Methods: Twelve male Wistar rats (8 weeks old) were exposed to the MS of 1-mA footshocks and forced swimming, while 12 control rats were placed in a plastic cage. Contextual fear conditioning with 0.1-mA footshocks in a context different from the MS was conducted 15 days after the MS for both groups. Three retention tests were administered after 24 hours and 9 and 16 days. Two magnetic resonance imaging scans were conducted, one on the day before MS induction and one the day after the third retention test, with a 32-day interval., Results: The MS group showed greater freezing responses than the control group in all retention tests. Whole-brain voxel-based morphometry analyses revealed reduced gray matter volume in the anterior amygdalohippocampal area in MS group rats compared with control rats. These volume changes were negatively associated with freezing time in the third retention test in the MS group., Conclusions: These results suggest that individual variability in the amygdalohippocampal area may be related to long-lasting fear responses after severe stress., (© 2024 The Authors.)

Published
2024
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5. Beneficial Effects of Low-Intensity Pulsed Ultrasound Therapy on Right Ventricular Dysfunction in Animal Models.

Author

Nakata T, Shindo T, Ito K, Eguchi K, Monma Y, Ichijo S, Ryoke R, Satoh W, Kumasaka K, Sato H, Kurosawa R, Satoh K, Kawashima R, Miura M, Kanai H, Yasuda S, and Shimokawa H

Abstract

Right ventricular failure (RVF) is a leading cause of death in patients with pulmonary hypertension; however, effective treatment remains to be developed. We have developed low-intensity pulsed ultrasound therapy for cardiovascular diseases. In this study, we demonstrated that the expression of endothelial nitric oxide synthase (eNOS) in RVF patients was downregulated and that eNOS expression and its downstream pathway were ameliorated through eNOS activation in 2 animal models of RVF. These results indicate that eNOS is an important therapeutic target of RVF, for which low-intensity pulsed ultrasound therapy is a promising therapy for patients with RVF., Competing Interests: This research was supported in part by the Japan Agency for Medical Research and Development (grant nos. JP19lm0203047 and JP19lk1403011). The authors have reported that they have no relationships relevant to the contents of this paper to disclose., (© 2023 The Authors.)

Published
2022
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6. Author Correction: Nrf2 contributes to the weight gain of mice during space travel.

Author

Suzuki T, Uruno A, Yumoto A, Taguchi K, Suzuki M, Harada N, Ryoke R, Naganuma E, Osanai N, Goto A, Suda H, Browne R, Otsuki A, Katsuoka F, Zorzi M, Yamazaki T, Saigusa D, Koshiba S, Nakamura T, Fukumoto S, Ikehata H, Nishikawa K, Suzuki N, Hirano I, Shimizu R, Oishi T, Motohashi H, Tsubouchi H, Okada R, Kudo T, Shimomura M, Kensler TW, Mizuno H, Shirakawa M, Takahashi S, Shiba D, and Yamamoto M

Abstract

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Published
2020
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7. Nrf2 contributes to the weight gain of mice during space travel.

Author

Suzuki T, Uruno A, Yumoto A, Taguchi K, Suzuki M, Harada N, Ryoke R, Naganuma E, Osanai N, Goto A, Suda H, Browne R, Otsuki A, Katsuoka F, Zorzi M, Yamazaki T, Saigusa D, Koshiba S, Nakamura T, Fukumoto S, Ikehata H, Nishikawa K, Suzuki N, Hirano I, Shimizu R, Oishi T, Motohashi H, Tsubouchi H, Okada R, Kudo T, Shimomura M, Kensler TW, Mizuno H, Shirakawa M, Takahashi S, Shiba D, and Yamamoto M

Subjects
Abdominal Fat pathology, Adipose Tissue, White pathology, Aging blood, Aging metabolism, Animals, Bone and Bones pathology, Gene Expression Regulation, Homeostasis, Metabolome, Mice, Knockout, Muscles pathology, NF-E2-Related Factor 2 deficiency, NF-E2-Related Factor 2 genetics, Sequence Analysis, RNA, Stress, Physiological, NF-E2-Related Factor 2 metabolism, Space Flight, Weight Gain genetics
Abstract

Space flight produces an extreme environment with unique stressors, but little is known about how our body responds to these stresses. While there are many intractable limitations for in-flight space research, some can be overcome by utilizing gene knockout-disease model mice. Here, we report how deletion of Nrf2, a master regulator of stress defense pathways, affects the health of mice transported for a stay in the International Space Station (ISS). After 31 days in the ISS, all flight mice returned safely to Earth. Transcriptome and metabolome analyses revealed that the stresses of space travel evoked ageing-like changes of plasma metabolites and activated the Nrf2 signaling pathway. Especially, Nrf2 was found to be important for maintaining homeostasis of white adipose tissues. This study opens approaches for future space research utilizing murine gene knockout-disease models, and provides insights into mitigating space-induced stresses that limit the further exploration of space by humans.

Published
2020
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8. Nrf2 Suppresses Oxidative Stress and Inflammation in App Knock-In Alzheimer's Disease Model Mice.

Author

Uruno A, Matsumaru D, Ryoke R, Saito R, Kadoguchi S, Saigusa D, Saito T, Saido TC, Kawashima R, and Yamamoto M

Subjects
Amyloid beta-Peptides metabolism, Animals, Avoidance Learning drug effects, Avoidance Learning physiology, Calcium-Binding Proteins metabolism, Cognition drug effects, Cognitive Dysfunction genetics, Cognitive Dysfunction metabolism, Disease Models, Animal, Glutathione blood, Inflammation pathology, Isothiocyanates pharmacology, Mice, Mice, Inbred C57BL, Mice, Transgenic, Microfilament Proteins metabolism, NF-E2-Related Factor 2 metabolism, Phosphatidylethanolamines metabolism, Plaque, Amyloid genetics, Plaque, Amyloid pathology, Plasmalogens metabolism, Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization, Alzheimer Disease genetics, Amyloid beta-Protein Precursor genetics, Kelch-Like ECH-Associated Protein 1 genetics, NF-E2-Related Factor 2 genetics, Oxidative Stress physiology
Abstract

Nrf2 (NF-E2-related-factor 2) is a stress-responsive transcription factor that protects cells against oxidative stresses. To clarify whether Nrf2 prevents Alzheimer's disease (AD), AD model App NL-G-F/NL-G-F knock-in ( App NLGF ) mice were studied in combination with genetic Nrf2 induction model Keap1 FA/FA mice. While App NLGF mice displayed shorter latency to escape than wild-type mice in the passive-avoidance task, the impairment was improved in App NLGF :: Keap1 FA/FA mice. Matrix-assisted laser desorption ionization-mass spectrometry imaging revealed that reduced glutathione levels were elevated by Nrf2 induction in App NLGF :: Keap1 FA/FA mouse brains compared to App NLGF mouse brains. Genetic Nrf2 induction in App NLGF mice markedly suppressed the elevation of the oxidative stress marker 8-OHdG and Iba1-positive microglial cell number. We also determined the plasmalogen-phosphatidylethanolamine (PlsPE) level as an AD biomarker. PlsPE containing polyunsaturated fatty acids was decreased in the App NLGF mouse brain, but Nrf2 induction attenuated this decline. To evaluate whether pharmacological induction of Nrf2 elicits beneficial effects for AD treatment, we tested the natural compound 6-MSITC [6-(methylsulfinyl)hexyl isothiocyanate]. Administration of 6-MSITC improved the impaired cognition of App NLGF mice in the passive-avoidance task. These results demonstrate that the induction of Nrf2 ameliorates cognitive impairment in the AD model mouse by suppressing oxidative stress and neuroinflammation, suggesting that Nrf2 is an important therapeutic target of AD., (Copyright © 2020 American Society for Microbiology.)

Published
2020
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