#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Distraction of olfactory bulb-medial prefrontal cortex circuit may induce anxiety-like behavior in allergic rhinitis


Autoři: Morteza Salimi aff001;  Sepideh Ghazvineh aff001;  Meysam Zare aff001;  Tannaz Parsazadegan aff001;  Kolsum Dehdar aff001;  Milad Nazari aff002;  Javad Mirnajafi-Zadeh aff001;  Hamidreza Jamaati aff004;  Mohammad Reza Raoufy aff001
Působiště autorů: Department of Physiology, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran aff001;  Faculty of Electrical Engineering, Sharif University of Technology, Tehran, Iran aff002;  Institute for Brain Sciences and Cognition, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran aff003;  Chronic Respiratory Diseases Research Center, National Research Institute of Tuberculosis and Lung Diseases, Shahid Beheshti University of Medical Sciences, Tehran, Iran aff004
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0221978

Souhrn

Allergic rhinitis is a chronic inflammatory disease of the upper respiratory tract, which is associated with high incidence of anxiety symptom. There is evidence that medial prefrontal cortex modulates anxiety-related behaviors and receives projections from olfactory bulb. Since olfactory dysfunction has been reported in allergic rhinitis, we aimed to evaluate anxiety-like behavior and oscillations of olfactory bulb-medial prefrontal cortex circuit in an animal model of allergic rhinitis. The number of open arm entries in elevated zero maze was significantly reduced in sensitized rats exposed to intranasal ovalbumin compared to the control group, which was indicating the enhancement of anxiety-like behavior in allergic rhinitis animals. Analysis of local field potentials in olfactory bulb and medial prefrontal cortex during immobility and exploration state showed that anxiety-like behavior induced by allergic rhinitis was in association with increased activity of medial prefrontal cortex and enhancement of olfactory bulb-medial prefrontal cortex coupling in delta and theta bands. Moreover, in allergic rhinitis animals, theta strongly coordinates local gamma activity in olfactory bulb and medial prefrontal cortex, which means to have a strong local theta/gamma coupling. We suggested that disruption of olfactory bulb-medial prefrontal cortex circuit due to allergic reactions might have a governing role for inducing anxiety-like behavior in the allergic rhinitis experimental model.

Klíčová slova:

Biology and life sciences – Anatomy – Brain – Prefrontal cortex – Olfactory bulb – Psychology – Emotions – Anxiety – Behavior – Animal behavior – Allergies – Allergic diseases – Allergic rhinitis – Zoology – Organisms – Eukaryota – Animals – Vertebrates – Amniotes – Mammals – Rodents – Rats – Medicine and health sciences – Clinical medicine – Clinical immunology – Immunology – Otorhinolaryngology – Rhinology – Nasal diseases – Rhinitis – Social sciences – Research and analysis methods – Animal studies – Experimental organism systems – Model organisms – Animal models


Zdroje

1. Yang S, Wu J, Zhang Q, Li X, Liu D, Zeng B, et al. Allergic Rhinitis in Rats Is Associated with an Inflammatory Response of the Hippocampus. Behav Neurol. 2018;(2018):1–7.

2. Maurer M, Zuberbier T. Undertreatment of rhinitis symptoms in Europe: Findings from a cross-sectional questionnaire survey. Allergy Eur J Allergy Clin Immunol. 2007;62(9):1057–63.

3. Bousquet J, Van Cauwenberge P, Khaltaev N. Allergic rhinitis and its impact on asthma (ARIA)(ARIA Workshop Report). J Allergy Clin Immunol. 2001;108(5 Suppl):S147–334.

4. Bernstein DI, Schwartz G, Bernstein JA. Allergic rhinitis: mechanisms and treatment. Immunol Allergy Clin. 2016;36(2):261–78.

5. Wang XD, Zheng M, Lou HF, Wang CS, Zhang Y, Bo MY, et al. An increased prevalence of self‐reported allergic rhinitis in major Chinese cities from 2005 to 2011. Allergy. 2016;71(8):1170–80. doi: 10.1111/all.12874 26948849

6. Berger WE. Allergic rhinitis in children: diagnosis and management strategies. Pediatr Drugs. 2004;6(4):233–51.

7. Nathan RA. The burden of allergic rhinitis. In: Allergy and Asthma Proceedings. OceanSide Publications; 2007. p. 3. 17390749

8. Marshall PS. Allergy and depression: A neurochemical threshold model of the relation between the illnesses. Psychol Bull. 1993;113(1):23–43 8093981

9. Weeke ER. Epidemiology of hay fever and perennial allergic rhinitis. Monogr Allergy. 1987;21:1–20.

10. Ziering RW. Immediate and late side effects of hay fever: Physical and psychosocial problems. Postgrad Med. 1989;85(6):183–90. 2710725

11. Jolicoeur LM, Pharm D, Boyer JG, Reeder CE, Turner J. Influence of asthma or allergies on the utilization of health care resources and quality of life of college students. J Asthma. 1994;31(4):251–67. 8040151

12. Parsazadegan T, Salimi M, Ghazvineh S, Raoufy MR. Cognitive disorders in allergic rhinitis may be induced by decline of respiration entrained rhythm in the brain. Med Hypotheses. 2018;121:89–90. doi: 10.1016/j.mehy.2018.09.037 30396502

13. Bell IR, Jasnoski ML, Kagan J, King DS. Depression and allergies: survey of a nonclinical population. Psychother Psychosom. 1991;55(1):24–31. 1866437

14. Wamboldt MZ, Schmitz S, Mrazek D. Genetic association between atopy and behavioral symptoms in middle childhood. J Child Psychol Psychiatry. 1998;39(7):1007–16. 9804033

15. Kovács M, Stauder A, Szedmák S. Severity of allergic complaints: The importance of depressed mood. J Psychosom Res. 2003;54(6):549–57. 12781309

16. Nanda MK, LeMasters GK, Levin L, Rothenberg ME, Assa’ad AH, Newman N, et al. Allergic diseases and internalizing behaviors in early childhood. Pediatrics. 2016;137(1) e20151922.

17. Tonelli LH, Katz M, Kovacsics CE, Gould TD, Joppy B, Hoshino A, et al. Allergic rhinitis induces anxiety-like behavior and altered social interaction in rodents. Brain Behav Immun. 2009;23(6):784–93. doi: 10.1016/j.bbi.2009.02.017 19268702

18. Suzuki M, Zheng X, Zhang X, Li M, Vladau C, Ichim TE, et al. Novel Vaccination for Allergy through Gene Silencing of CD40 Using Small Interfering RNA. J Immunol. 2014;180(12):8461–9.

19. Ozaki S, Toida K, Suzuki M, Nakamura Y, Ohno N, Ohashi T, et al. Impaired olfactory function in mice with allergic rhinitis. Auris Nasus Larynx. 2010;37(5):575–83. doi: 10.1016/j.anl.2009.12.004 20346605

20. Basso AS, Costa Pinto FA, Russo M, Giorgetti Britto LR, De Sá-Rocha LC, Palermo Neto J. Neural correlates of IgE-mediated food allergy. J Neuroimmunol. 2003;140(1–2):69–77. 12864973

21. Galli SJ, Tsai M, Piliponsky AM. The development of allergic inflammation. Nature. 2008;454(7203):445–54. doi: 10.1038/nature07204 18650915

22. Moberly AH, Schreck M, Bhattarai JP, Zweifel LS, Luo W, Ma M. Olfactory inputs modulate respiration-related rhythmic activity in the prefrontal cortex and freezing behavior. Nat Commun. 2018;9(1):1528. doi: 10.1038/s41467-018-03988-1 29670106

23. Christopher S. Monk PD, Eric E. Nelson PD, Erin B. McClure PD, Karin Mogg PD, Brendan P. Bradley PD, Ellen Leibenluft MD, et al. Ventrolateral Prefrontal Cortex Activation and Attentional Bias in Response to Angry Faces in Adolescents With Generalized Anxiety Disorder. Am J Psychiatry. 2006;65(5):568–76.

24. Kim MJ, Loucks RA, Palmer AL, Brown AC, Solomon KM, Marchante AN, et al. The structural and functional connectivity of the amygdala: From normal emotion to pathological anxiety. Behavioural Brain Research. Elsevier B.V.2011;223(2): 403–10.

25. Likhtik E, Stujenske JM, Topiwala MA, Harris AZ, Gordon JA. Prefrontal entrainment of amygdala activity signals safety in learned fear and innate anxiety. 2014;17(1):106–13. doi: 10.1038/nn.3582 24241397

26. Tort ABL, Brankačk J, Draguhn A. Respiration-Entrained Brain Rhythms Are Global but Often Overlooked. Trends Neurosci. 2018;41(4):186–97. doi: 10.1016/j.tins.2018.01.007 29429805

27. Hendriksen H, Korte SM, Olivier B, Oosting RS. The olfactory bulbectomy model in mice and rat: one story or two tails? Eur J Pharmacol. 2015;753(2015):105–13.

28. Jancsár S, Leonard BE. The olfactory bulbectomized rat as a model of depression. Front Neuropsychiatr Res. 2015;29(4–5):357–72.

29. Altuntaş E, Yener G, Doğan R, Aksoy F, Şerif Aydın M, Karataş E. Effects of a Thermosensitive In Situ Gel Containing Mometasone Furoate on a Rat Allergic Rhinitis Model. American Journal of Rhinology and Allergy. 2018;32:(3)1–7

30. Paxinos G, Watson C. The rat brain in stereotaxic coordinates: hard cover edition. Elsevier; 2006.

31. Mikulovic S, Restrepo CE, Siwani S, Bauer P, Pupe S, Tort ABL, et al. Ventral hippocampal OLM cells control type 2 theta oscillations and response to predator odor. Nat Commun. 2018;9(1)1–15. doi: 10.1038/s41467-017-02088-w 29317637

32. Tort ABL, Komorowski R, Eichenbaum H, Kopell N. Measuring phase-amplitude coupling between neuronal oscillations of different frequencies. J Neurophysiol. 2010;104(2):1195–210. doi: 10.1152/jn.00106.2010 20463205

33. Chida Y, Hamer M, Steptoe A. A bidirectional relationship between psychosocial factors and atopic disorders: a systematic review and meta-analysis. Psychosom Med. 2008;70(1):102–16. 18158379

34. Marshall GD, Roy SR. Stress and allergic diseases. In: Psychoneuroimmunology. Elsevier; 2007. p. 799–824.

35. Chrousos GP. Stress, chronic inflammation, and emotional and physical well-being: concurrent effects and chronic sequelae. J Allergy Clin Immunol. 2000;106(5):275–91.

36. Wright RJ. Stress and atopic disorders. J Allergy Clin Immunol. 2005;116(6):1301–6. 16337463

37. Chida Y, Sudo N, Sonoda J, Hiramoto T, Kubo C. Early-life psychological stress exacerbates adult mouse asthma via the hypothalamus–pituitary–adrenal axis. Am J Respir Crit Care Med. 2007;175(4):316–22. 17110645

38. Pawlak CR, Schwarting RKW, Bauhofer A. Cytokine mRNA levels in brain and peripheral tissues of the rat: Relationships with plus-maze behavior. Mol Brain Res. 2005;137(1–2):159–65. 15950774

39. Wright RJ, Cohen RT, Cohen S. The impact of stress on the development and expression of atopy. Curr Opin Allergy Clin Immunol. 2005;5(1):23–9. 15643340

40. Raoufy MR, Ghafari T, Darooei R, Nazari M, Mahdaviani SA, Eslaminejad AR, et al. Classification of asthma based on nonlinear analysis of breathing pattern. PLoS One. 2016;11(1):e0147976. doi: 10.1371/journal.pone.0147976 26824900

41. Kern RC. Candidate’s Thesis: Chronic Sinusitis and Anosmia: Pathologic Changes in the Olfactory Mucosa. Laryngoscope. 2000;110(7):1071–7. 10892672

42. Kern RC, Conley DB, Haines GK III, Robinson AM. Pathology of the olfactory mucosa: implications for the treatment of olfactory dysfunction. Laryngoscope. 2004;114(2):279–85. 14755203

43. Miller TP, Zeiss CR. Allergic Rhinitis. Allergy Asthma Proc. 2006;14(2):116–116.

44. Bishop S, Duncan J, Brett M, Lawrence AD. Prefrontal cortical function and anxiety: Controlling attention to threat-related stimuli. Nat Neurosci. 2004;7(2):184–8. 14703573

45. Li AA, Gong L, Liu Q, Li X, Xu F. State-dependent coherences between the olfactory bulbs for delta and theta oscillations. Neurosci Lett. 2010;480(1):44–8. doi: 10.1016/j.neulet.2010.05.093 20594948

46. Felix-Ortiz AC, Burgos-Robles A, Bhagat ND, Leppla CA, Tye KM. Bidirectional modulation of anxiety-related and social behaviors by amygdala projections to the medial prefrontal cortex [Elevated plus maze example with optogenetics]. Neuroscience 2016;321:197–209. doi: 10.1016/j.neuroscience.2015.07.041 26204817

47. Bi L-L, Wang J, Luo Z-Y, Chen S-P, Geng F, Chen Y, et al. Enhanced excitability in the infralimbic cortex produces anxiety-like behaviors. Neuropharmacology. 2013;72:148–56. doi: 10.1016/j.neuropharm.2013.04.048 23643746

48. Oliveira JF, Dias NS, Correia M, Gama-Pereira F, Sardinha VM, Lima A, et al. Chronic stress disrupts neural coherence between cortico-limbic structures. Front Neural Circuits. 2013;7(February):1–12.

49. Jensen O, Colgin LL. Cross-frequency coupling between neuronal oscillations. Trends Cogn Sci. 2007;11(7):267–9. 17548233

50. Miskovic V, Ashbaugh AR, Santesso DL, McCabe RE, Antony MM, Schmidt LA. Frontal brain oscillations and social anxiety: A cross-frequency spectral analysis during baseline and speech anticipation. Biol Psychol. 2010;83(2):125–32. doi: 10.1016/j.biopsycho.2009.11.010 19945500

51. Knyazev GG. Cross-frequency coupling of brain oscillations: An impact of state anxiety. 2011;80(3):236–45.

52. Young CK, Eggermont JJ. Coupling of mesoscopic brain oscillations: recent advances in analytical and theoretical perspectives. Prog Neurobiol. 2009;89(1):61–78. doi: 10.1016/j.pneurobio.2009.06.002 19549556


Článek vyšel v časopise

PLOS One


2019 Číslo 9
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Svět praktické medicíny 1/2024 (znalostní test z časopisu)
nový kurz

Koncepce osteologické péče pro gynekology a praktické lékaře
Autoři: MUDr. František Šenk

Sekvenční léčba schizofrenie
Autoři: MUDr. Jana Hořínková

Hypertenze a hypercholesterolémie – synergický efekt léčby
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Význam metforminu pro „udržitelnou“ terapii diabetu
Autoři: prof. MUDr. Milan Kvapil, CSc., MBA

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#