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Published in: EJNMMI Research 1/2020

01-12-2020 | Positron Emission Tomography | Short communication

[18F]MPPF and [18F]FDG μPET imaging in rats: impact of transport and restraint stress

Authors: Verena Buchecker, Ann-Marie Waldron, R. Maarten van Dijk, Ines Koska, Matthias Brendel, Barbara von Ungern-Sternberg, Simon Lindner, Franz Josef Gildehaus, Sibylle Ziegler, Peter Bartenstein, Heidrun Potschka

Published in: EJNMMI Research | Issue 1/2020

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Abstract

Background

Stress exposure can significantly affect serotonergic signaling with a particular impact on 5-HT1A receptor expression. Positron emission tomography (PET) provides opportunities for molecular imaging of alterations in 5-HT1A receptor binding following stress exposure. Considering the possible role of 5-HT1A receptors in stress coping mechanisms, respective imaging approaches are of particular interest.

Material and methods

For twelve consecutive days, Sprague Dawley rats were exposed to daily transport with a 1 h stay in a laboratory or daily transport plus 1 h restraint in a narrow tube. Following, animals were subjected to μPET imaging with 2′-methoxyphenyl-(N-2′-pyridinyl)-p-[18F]fluoro-benzamidoethylpiperazine ([18F]MPPF) and 2-deoxy-2-[18F]fluoro-D-glucose ([18F]FDG). Behavioral and biochemical parameters were analyzed to obtain additional information.

Results

In rats with repeated transport, hippocampal [18F]MPPF binding exceeded that in the naive group, while no difference in [18F]FDG uptake was detected between the groups. A transient decline in body weight was observed in rats with transport or combined transport and restraint. Thereby, body weight development correlated with [18F]MPPF binding.

Conclusions

Mild-to-moderate stress associated with daily transport and exposure to a laboratory environment can trigger significant alterations in hippocampal binding of the 5-HT1A receptor ligand [18F]MPPF. This finding indicates that utmost care is necessary to control and report transport and associated handling procedures for animals used in μPET studies analyzing the serotonergic system in order to enhance the robustness of conclusions and allow replicability of findings. In view of earlier studies indicating that an increase in hippocampal 5-HT1A receptor expression may be associated with a resilience to stress, it would be of interest to further evaluate 5-HT1A receptor imaging approaches as a candidate biomarker for the vulnerability to stress.
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Literature
1.
go back to reference Chaouloff F, Berton O, Mormede P. Serotonin and stress. Neuropsychopharmacology. 1999;21(2 Suppl):28S–32S.PubMedCrossRef Chaouloff F, Berton O, Mormede P. Serotonin and stress. Neuropsychopharmacology. 1999;21(2 Suppl):28S–32S.PubMedCrossRef
2.
3.
4.
5.
go back to reference Zangrossi H Jr, Graeff FG. Serotonin in anxiety and panic: contributions of the elevated T-maze. Neurosci Biobehav Rev. 2014;46(Pt 3):397–406.PubMedCrossRef Zangrossi H Jr, Graeff FG. Serotonin in anxiety and panic: contributions of the elevated T-maze. Neurosci Biobehav Rev. 2014;46(Pt 3):397–406.PubMedCrossRef
6.
go back to reference Akimova E, Lanzenberger R, Kasper S. The serotonin-1A receptor in anxiety disorders. Biol Psychiatry. 2009;66(7):627–35.PubMedCrossRef Akimova E, Lanzenberger R, Kasper S. The serotonin-1A receptor in anxiety disorders. Biol Psychiatry. 2009;66(7):627–35.PubMedCrossRef
7.
go back to reference Pare WP, Tejani-Butt SM. Effect of stress on the behavior and 5-HT system in Sprague-Dawley and Wistar Kyoto rat strains. Integr Physiol Behav Sci. 1996;31(2):112–21.PubMedCrossRef Pare WP, Tejani-Butt SM. Effect of stress on the behavior and 5-HT system in Sprague-Dawley and Wistar Kyoto rat strains. Integr Physiol Behav Sci. 1996;31(2):112–21.PubMedCrossRef
8.
go back to reference Flugge G, Kramer M, Rensing S, Fuchs E. 5HT1A-receptors and behaviour under chronic stress: selective counteraction by testosterone. Eur J Neurosci. 1998;10(8):2685–93.PubMedCrossRef Flugge G, Kramer M, Rensing S, Fuchs E. 5HT1A-receptors and behaviour under chronic stress: selective counteraction by testosterone. Eur J Neurosci. 1998;10(8):2685–93.PubMedCrossRef
9.
go back to reference Lakehayli S, Said N, El Khachibi M, El Ouahli M, Nadifi S, Hakkou F, et al. Prenatal stress alters diazepam withdrawal syndrome and 5HT1A receptor expression in the raphe nuclei of adult rats. Neuroscience. 2016;330:50–6.PubMedCrossRef Lakehayli S, Said N, El Khachibi M, El Ouahli M, Nadifi S, Hakkou F, et al. Prenatal stress alters diazepam withdrawal syndrome and 5HT1A receptor expression in the raphe nuclei of adult rats. Neuroscience. 2016;330:50–6.PubMedCrossRef
11.
go back to reference Choi JY, Shin S, Lee M, Jeon TJ, Seo Y, Kim CH, et al. Acute physical stress induces the alteration of the serotonin 1A receptor density in the hippocampus. Synapse. 2014;68(8):363–8.PubMedCrossRef Choi JY, Shin S, Lee M, Jeon TJ, Seo Y, Kim CH, et al. Acute physical stress induces the alteration of the serotonin 1A receptor density in the hippocampus. Synapse. 2014;68(8):363–8.PubMedCrossRef
12.
go back to reference Le Francois B, Soo J, Millar AM, Daigle M, Le Guisquet AM, Leman S, et al. Chronic mild stress and antidepressant treatment alter 5-HT1A receptor expression by modifying DNA methylation of a conserved Sp4 site. Neurobiol Dis. 2015;82:332–41.PubMedPubMedCentralCrossRef Le Francois B, Soo J, Millar AM, Daigle M, Le Guisquet AM, Leman S, et al. Chronic mild stress and antidepressant treatment alter 5-HT1A receptor expression by modifying DNA methylation of a conserved Sp4 site. Neurobiol Dis. 2015;82:332–41.PubMedPubMedCentralCrossRef
13.
go back to reference Meller E, Goldstein M, Bohmaker K. Receptor reserve for 5-hydroxytryptamine1A-mediated inhibition of serotonin synthesis: possible relationship to anxiolytic properties of 5-hydroxytryptamine1A agonists. Mol Pharmacol. 1990;37(2):231–7.PubMed Meller E, Goldstein M, Bohmaker K. Receptor reserve for 5-hydroxytryptamine1A-mediated inhibition of serotonin synthesis: possible relationship to anxiolytic properties of 5-hydroxytryptamine1A agonists. Mol Pharmacol. 1990;37(2):231–7.PubMed
14.
go back to reference Altieri SC, Garcia-Garcia AL, Leonardo ED, Andrews AM. Rethinking 5-HT1A receptors: emerging modes of inhibitory feedback of relevance to emotion-related behavior. ACS Chem Neurosci. 2013;4(1):72–83.PubMedCrossRef Altieri SC, Garcia-Garcia AL, Leonardo ED, Andrews AM. Rethinking 5-HT1A receptors: emerging modes of inhibitory feedback of relevance to emotion-related behavior. ACS Chem Neurosci. 2013;4(1):72–83.PubMedCrossRef
15.
go back to reference Chaouloff F. Regulation of 5-HT receptors by corticosteroids: where do we stand? Fundam Clin Pharmacol. 1995;9(3):219–33.PubMedCrossRef Chaouloff F. Regulation of 5-HT receptors by corticosteroids: where do we stand? Fundam Clin Pharmacol. 1995;9(3):219–33.PubMedCrossRef
16.
go back to reference Pompili M, Serafini G, Innamorati M, Moller-Leimkuhler AM, Giupponi G, Girardi P, et al. The hypothalamic-pituitary-adrenal axis and serotonin abnormalities: a selective overview for the implications of suicide prevention. Eur Arch Psychiatry Clin Neurosci. 2010;260(8):583–600.PubMedCrossRef Pompili M, Serafini G, Innamorati M, Moller-Leimkuhler AM, Giupponi G, Girardi P, et al. The hypothalamic-pituitary-adrenal axis and serotonin abnormalities: a selective overview for the implications of suicide prevention. Eur Arch Psychiatry Clin Neurosci. 2010;260(8):583–600.PubMedCrossRef
17.
go back to reference Southwick SM, Vythilingam M, Charney DS. The psychobiology of depression and resilience to stress: implications for prevention and treatment. Annu Rev Clin Psychol. 2005;1:255–91.PubMedCrossRef Southwick SM, Vythilingam M, Charney DS. The psychobiology of depression and resilience to stress: implications for prevention and treatment. Annu Rev Clin Psychol. 2005;1:255–91.PubMedCrossRef
18.
go back to reference Pauwelyn G, Laeken NV, Verhoeven J, De Vos F, Peremans K, Dockx R, et al. The signature of the serotonin system in the chronic corticosterone depression model: a study with [18F] MPPF,[18F] Altanserin and [11C] DASB. Neuropsychiatry. 2018;8(04):1377–90.CrossRef Pauwelyn G, Laeken NV, Verhoeven J, De Vos F, Peremans K, Dockx R, et al. The signature of the serotonin system in the chronic corticosterone depression model: a study with [18F] MPPF,[18F] Altanserin and [11C] DASB. Neuropsychiatry. 2018;8(04):1377–90.CrossRef
19.
go back to reference van Dijk RM, Di Liberto V, Brendel M, Waldron AM, Moller C, Gildehaus FJ, et al. Imaging biomarkers of behavioral impairments: a pilot micro-positron emission tomographic study in a rat electrical post-status epilepticus model. Epilepsia. 2018;59(12):2194–205.PubMedCrossRef van Dijk RM, Di Liberto V, Brendel M, Waldron AM, Moller C, Gildehaus FJ, et al. Imaging biomarkers of behavioral impairments: a pilot micro-positron emission tomographic study in a rat electrical post-status epilepticus model. Epilepsia. 2018;59(12):2194–205.PubMedCrossRef
20.
go back to reference Di Liberto V, van Dijk RM, Brendel M, Waldron AM, Moller C, Koska I, et al. Imaging correlates of behavioral impairments: an experimental PET study in the rat pilocarpine epilepsy model. Neurobiol Dis. 2018;118:9–21.PubMedCrossRef Di Liberto V, van Dijk RM, Brendel M, Waldron AM, Moller C, Koska I, et al. Imaging correlates of behavioral impairments: an experimental PET study in the rat pilocarpine epilepsy model. Neurobiol Dis. 2018;118:9–21.PubMedCrossRef
21.
go back to reference Lothe A, Didelot A, Hammers A, Costes N, Saoud M, Gilliam F, et al. Comorbidity between temporal lobe epilepsy and depression: a [18F]MPPF PET study. Brain. 2008;131(Pt 10):2765–82.PubMedPubMedCentralCrossRef Lothe A, Didelot A, Hammers A, Costes N, Saoud M, Gilliam F, et al. Comorbidity between temporal lobe epilepsy and depression: a [18F]MPPF PET study. Brain. 2008;131(Pt 10):2765–82.PubMedPubMedCentralCrossRef
22.
go back to reference Rubins DJ, Melega WP, Lacan G, Way B, Plenevaux A, Luxen A, et al. Development and evaluation of an automated atlas-based image analysis method for microPET studies of the rat brain. Neuroimage. 2003;20(4):2100–18.PubMedCrossRef Rubins DJ, Melega WP, Lacan G, Way B, Plenevaux A, Luxen A, et al. Development and evaluation of an automated atlas-based image analysis method for microPET studies of the rat brain. Neuroimage. 2003;20(4):2100–18.PubMedCrossRef
23.
go back to reference Toga AW, Santori EM, Hazani R, Ambach K. A 3D digital map of rat brain. Brain Res Bull. 1995;38(1):77–85.PubMedCrossRef Toga AW, Santori EM, Hazani R, Ambach K. A 3D digital map of rat brain. Brain Res Bull. 1995;38(1):77–85.PubMedCrossRef
24.
go back to reference Overhoff F, Brendel M, Jaworska A, Korzhova V, Delker A, Probst F, et al. Automated spatial brain normalization and hindbrain white matter reference tissue give improved [(18)F]-Florbetaben PET quantitation in Alzheimer’s model mice. Front Neurosci. 2016;10:45 Available from: http://europepmc.org/abstract/MED/26973442 http://europepmc.org/articles/PMC4770021?pdf=render http://europepmc.org/articles/PMC4770021 https://doi.org/10.3389/fnins.2016.00045.PubMedPubMedCentralCrossRef Overhoff F, Brendel M, Jaworska A, Korzhova V, Delker A, Probst F, et al. Automated spatial brain normalization and hindbrain white matter reference tissue give improved [(18)F]-Florbetaben PET quantitation in Alzheimer’s model mice. Front Neurosci. 2016;10:45 Available from: http://​europepmc.​org/​abstract/​MED/​26973442 http://europepmc.org/articles/PMC4770021?pdf=render http://europepmc.org/articles/PMC4770021 https://doi.org/10.3389/fnins.2016.00045.PubMedPubMedCentralCrossRef
25.
go back to reference la Fougere C, Boning G, Bartmann H, Wangler B, Nowak S, Just T, et al. Uptake and binding of the serotonin 5-HT1A antagonist [18F]-MPPF in brain of rats: effects of the novel P-glycoprotein inhibitor tariquidar. Neuroimage. 2010;49(2):1406–15.PubMedCrossRef la Fougere C, Boning G, Bartmann H, Wangler B, Nowak S, Just T, et al. Uptake and binding of the serotonin 5-HT1A antagonist [18F]-MPPF in brain of rats: effects of the novel P-glycoprotein inhibitor tariquidar. Neuroimage. 2010;49(2):1406–15.PubMedCrossRef
26.
go back to reference Logan J, Fowler JS, Volkow ND, Wang GJ, Ding YS, Alexoff DL. Distribution volume ratios without blood sampling from graphical analysis of PET data. J Cereb Blood Flow Metab. 1996;16(5):834–40.PubMedCrossRef Logan J, Fowler JS, Volkow ND, Wang GJ, Ding YS, Alexoff DL. Distribution volume ratios without blood sampling from graphical analysis of PET data. J Cereb Blood Flow Metab. 1996;16(5):834–40.PubMedCrossRef
27.
go back to reference Klein S, Bankstahl JP, Loscher W, Bankstahl M. Sucrose consumption test reveals pharmacoresistant depression-associated behavior in two mouse models of temporal lobe epilepsy. Exp Neurol. 2015;263:263–71.PubMedCrossRef Klein S, Bankstahl JP, Loscher W, Bankstahl M. Sucrose consumption test reveals pharmacoresistant depression-associated behavior in two mouse models of temporal lobe epilepsy. Exp Neurol. 2015;263:263–71.PubMedCrossRef
28.
go back to reference Team RC. R: a language and environment for statistical computing; 2013. Team RC. R: a language and environment for statistical computing; 2013.
29.
go back to reference Wei T, Simko V, Levy M, Xie Y, Jin Y, Zemla J. Package ‘corrplot’. Statistician. 2017;56:316–24. Wei T, Simko V, Levy M, Xie Y, Jin Y, Zemla J. Package ‘corrplot’. Statistician. 2017;56:316–24.
30.
go back to reference Monteiro S, Roque S, de Sa-Calcada D, Sousa N, Correia-Neves M, Cerqueira JJ. An efficient chronic unpredictable stress protocol to induce stress-related responses in C57BL/6 mice. Front Psychiatry. 2015;6:6.PubMedPubMedCentralCrossRef Monteiro S, Roque S, de Sa-Calcada D, Sousa N, Correia-Neves M, Cerqueira JJ. An efficient chronic unpredictable stress protocol to induce stress-related responses in C57BL/6 mice. Front Psychiatry. 2015;6:6.PubMedPubMedCentralCrossRef
31.
go back to reference Talbot SR, Biernot S, Bleich A, van Dijk RM, Ernst L, Hager C, et al. Defining body-weight reduction as a humane endpoint: a critical appraisal. Lab Anim. 2019;23677219883319. Talbot SR, Biernot S, Bleich A, van Dijk RM, Ernst L, Hager C, et al. Defining body-weight reduction as a humane endpoint: a critical appraisal. Lab Anim. 2019;23677219883319.
32.
go back to reference Carnevali L, Montano N, Statello R, Coude G, Vacondio F, Rivara S, et al. Social stress contagion in rats: behavioural, autonomic and neuroendocrine correlates. Psychoneuroendocrinology. 2017;82:155–63.PubMedCrossRef Carnevali L, Montano N, Statello R, Coude G, Vacondio F, Rivara S, et al. Social stress contagion in rats: behavioural, autonomic and neuroendocrine correlates. Psychoneuroendocrinology. 2017;82:155–63.PubMedCrossRef
33.
go back to reference Ono M, Sasaki H, Nagasaki K, Torigoe D, Ichii O, Sasaki N, et al. Does the routine handling affect the phenotype of disease model mice? Jpn J Vet Res. 2016;64(4):265–71.PubMed Ono M, Sasaki H, Nagasaki K, Torigoe D, Ichii O, Sasaki N, et al. Does the routine handling affect the phenotype of disease model mice? Jpn J Vet Res. 2016;64(4):265–71.PubMed
34.
go back to reference Deutsch-Feldman M, Picetti R, Seip-Cammack K, Zhou Y, Kreek MJ. Effects of handling and vehicle injections on adrenocorticotropic and corticosterone concentrations in Sprague-Dawley compared with Lewis rats. J Am Assoc Lab Anim Sci. 2015;54(1):35–9.PubMedPubMedCentral Deutsch-Feldman M, Picetti R, Seip-Cammack K, Zhou Y, Kreek MJ. Effects of handling and vehicle injections on adrenocorticotropic and corticosterone concentrations in Sprague-Dawley compared with Lewis rats. J Am Assoc Lab Anim Sci. 2015;54(1):35–9.PubMedPubMedCentral
35.
go back to reference Nayanatara A, Nagaraja H, Anupama B. The effect of repeated swimming stress on organ weights and lipid peroxidation in rats. Thai J Pharm Sci. 2005;18(1):3–9. Nayanatara A, Nagaraja H, Anupama B. The effect of repeated swimming stress on organ weights and lipid peroxidation in rats. Thai J Pharm Sci. 2005;18(1):3–9.
36.
go back to reference Selye H. A syndrome produced by diverse nocuous agents. 1936. J Neuropsychiatr Clin Neurosci. 1998;10(2):230–1.CrossRef Selye H. A syndrome produced by diverse nocuous agents. 1936. J Neuropsychiatr Clin Neurosci. 1998;10(2):230–1.CrossRef
37.
go back to reference Zurawek D, Gruca P, Antkiewicz-Michaluk L, Dziedzicka-Wasylewska M. Resilient phenotype in chronic mild stress paradigm is associated with altered expression levels of miR-18a-5p and serotonin 5-HT1a receptor in dorsal part of the hippocampus. Mol Neurobiol. 2019;56(11):7680–93.PubMedPubMedCentralCrossRef Zurawek D, Gruca P, Antkiewicz-Michaluk L, Dziedzicka-Wasylewska M. Resilient phenotype in chronic mild stress paradigm is associated with altered expression levels of miR-18a-5p and serotonin 5-HT1a receptor in dorsal part of the hippocampus. Mol Neurobiol. 2019;56(11):7680–93.PubMedPubMedCentralCrossRef
38.
go back to reference Zimmer L, Rbah L, Giacomelli F, Le Bars D, Renaud B. A reduced extracellular serotonin level increases the 5-HT1A PET ligand 18F-MPPF binding in the rat hippocampus. J Nucl Med. 2003;44(9):1495–501.PubMed Zimmer L, Rbah L, Giacomelli F, Le Bars D, Renaud B. A reduced extracellular serotonin level increases the 5-HT1A PET ligand 18F-MPPF binding in the rat hippocampus. J Nucl Med. 2003;44(9):1495–501.PubMed
39.
go back to reference Pare WP, Glavin GB. Restraint stress in biomedical research: a review. Neurosci Biobehav Rev. 1986;10(3):339–70.PubMedCrossRef Pare WP, Glavin GB. Restraint stress in biomedical research: a review. Neurosci Biobehav Rev. 1986;10(3):339–70.PubMedCrossRef
40.
go back to reference Calcia MA, Bonsall DR, Bloomfield PS, Selvaraj S, Barichello T, Howes OD. Stress and neuroinflammation: a systematic review of the effects of stress on microglia and the implications for mental illness. Psychopharmacology. 2016;233(9):1637–50.PubMedPubMedCentralCrossRef Calcia MA, Bonsall DR, Bloomfield PS, Selvaraj S, Barichello T, Howes OD. Stress and neuroinflammation: a systematic review of the effects of stress on microglia and the implications for mental illness. Psychopharmacology. 2016;233(9):1637–50.PubMedPubMedCentralCrossRef
41.
go back to reference Bonfils S. “Restraint ulcer” as a model of stress-induced gastric lesion. A historical note. Ann N Y Acad Sci. 1993;697:229–32.PubMedCrossRef Bonfils S. “Restraint ulcer” as a model of stress-induced gastric lesion. A historical note. Ann N Y Acad Sci. 1993;697:229–32.PubMedCrossRef
42.
go back to reference Scorrano F, Carrasco J, Pastor-Ciurana J, Belda X, Rami-Bastante A, Bacci ML, et al. Validation of the long-term assessment of hypothalamic-pituitary-adrenal activity in rats using hair corticosterone as a biomarker. FASEB J. 2015;29(3):859–67.PubMedCrossRef Scorrano F, Carrasco J, Pastor-Ciurana J, Belda X, Rami-Bastante A, Bacci ML, et al. Validation of the long-term assessment of hypothalamic-pituitary-adrenal activity in rats using hair corticosterone as a biomarker. FASEB J. 2015;29(3):859–67.PubMedCrossRef
43.
go back to reference Pijlman FT, Wolterink G, Van Ree JM. Physical and emotional stress have differential effects on preference for saccharine and open field behaviour in rats. Behav Brain Res. 2003;139(1-2):131–8.PubMedCrossRef Pijlman FT, Wolterink G, Van Ree JM. Physical and emotional stress have differential effects on preference for saccharine and open field behaviour in rats. Behav Brain Res. 2003;139(1-2):131–8.PubMedCrossRef
44.
go back to reference Plaznik A, Stefanski R, Kostowski W. Restraint stress-induced changes in saccharin preference: the effect of antidepressive treatment and diazepam. Pharmacol Biochem Behav. 1989;33(4):755–9.PubMedCrossRef Plaznik A, Stefanski R, Kostowski W. Restraint stress-induced changes in saccharin preference: the effect of antidepressive treatment and diazepam. Pharmacol Biochem Behav. 1989;33(4):755–9.PubMedCrossRef
45.
go back to reference Sung KK, Jang DP, Lee S, Kim M, Lee SY, Kim YB, et al. Neural responses in rat brain during acute immobilization stress: a [F-18]FDG micro PET imaging study. Neuroimage. 2009;44(3):1074–80.PubMedCrossRef Sung KK, Jang DP, Lee S, Kim M, Lee SY, Kim YB, et al. Neural responses in rat brain during acute immobilization stress: a [F-18]FDG micro PET imaging study. Neuroimage. 2009;44(3):1074–80.PubMedCrossRef
46.
go back to reference Mirrione MM, Schulz D, Lapidus KA, Zhang S, Goodman W, Henn FA. Increased metabolic activity in the septum and habenula during stress is linked to subsequent expression of learned helplessness behavior. Front Hum Neurosci. 2014;8:29.PubMedPubMedCentralCrossRef Mirrione MM, Schulz D, Lapidus KA, Zhang S, Goodman W, Henn FA. Increased metabolic activity in the septum and habenula during stress is linked to subsequent expression of learned helplessness behavior. Front Hum Neurosci. 2014;8:29.PubMedPubMedCentralCrossRef
47.
go back to reference Wei K, Bao W, Zhao Z, Zhou W, Liu J, Wei Y, et al. Changes of the brain activities after chronic restraint stress in rats: a study based on (18)F-FDG PET. Neurosci Lett. 2018;665:104–9.PubMedCrossRef Wei K, Bao W, Zhao Z, Zhou W, Liu J, Wei Y, et al. Changes of the brain activities after chronic restraint stress in rats: a study based on (18)F-FDG PET. Neurosci Lett. 2018;665:104–9.PubMedCrossRef
48.
go back to reference Abbott BB, Schoen LS, Badia P. Predictable and unpredictable shock: behavioral measures of aversion and physiological measures of stress. Psychol Bull. 1984;96(1):45–71.PubMedCrossRef Abbott BB, Schoen LS, Badia P. Predictable and unpredictable shock: behavioral measures of aversion and physiological measures of stress. Psychol Bull. 1984;96(1):45–71.PubMedCrossRef
49.
go back to reference Belda X, Rotllant D, Fuentes S, Delgado R, Nadal R, Armario A. Exposure to severe stressors causes long-lasting dysregulation of resting and stress-induced activation of the hypothalamic-pituitary-adrenal axis. Ann N Y Acad Sci. 2008;1148:165–73.PubMedCrossRef Belda X, Rotllant D, Fuentes S, Delgado R, Nadal R, Armario A. Exposure to severe stressors causes long-lasting dysregulation of resting and stress-induced activation of the hypothalamic-pituitary-adrenal axis. Ann N Y Acad Sci. 2008;1148:165–73.PubMedCrossRef
50.
go back to reference Marti O, Marti J, Armario A. Effects of chronic stress on food intake in rats: influence of stressor intensity and duration of daily exposure. Physiol Behav. 1994;55(4):747–53.PubMedCrossRef Marti O, Marti J, Armario A. Effects of chronic stress on food intake in rats: influence of stressor intensity and duration of daily exposure. Physiol Behav. 1994;55(4):747–53.PubMedCrossRef
Metadata
Title
[18F]MPPF and [18F]FDG μPET imaging in rats: impact of transport and restraint stress
Authors
Verena Buchecker
Ann-Marie Waldron
R. Maarten van Dijk
Ines Koska
Matthias Brendel
Barbara von Ungern-Sternberg
Simon Lindner
Franz Josef Gildehaus
Sibylle Ziegler
Peter Bartenstein
Heidrun Potschka
Publication date
01-12-2020
Publisher
Springer Berlin Heidelberg
Published in
EJNMMI Research / Issue 1/2020
Electronic ISSN: 2191-219X
DOI
https://doi.org/10.1186/s13550-020-00693-3

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