Amygdala mediates respiratory responses to sudden arousing stimuli and to restraint stress in rats

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 306, Issue 12, 2014, Pages

  Bondarenko, Evgeny ^a,b   Hodgson, Deborah M ^b   Nalivaiko, Eugene ^a  

^a UNIVERSITY OF NEWCASTLE   (Australia)

^b UNIVERSITY OF NEWCASTLE   (Australia)

Author keywords

Amygdala; Arousal; Respiratory rate; Stress; Tidal volume

Indexed keywords

MUSCIMOL;

ACCLIMATIZATION; ADULT; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANXIETY; AROUSAL; ARTICLE; AUDITORY STIMULATION; BODY PLETHYSMOGRAPHY; BREATHING; BREATHING MECHANICS; BREATHING PATTERN; BREATHING RATE; CAPSULA INTERNA; CONTROLLED STUDY; IMMOBILIZATION STRESS; MALE; MICROINJECTION; NERVE TRACT; NONHUMAN; PRIORITY JOURNAL; RAT; TIDAL VOLUME; VISUAL STIMULATION; WHITE NOISE;

AMYGDALA; AROUSAL; RESPIRATORY RATE; STRESS; TIDAL VOLUME;

AMYGDALA; ANIMALS; AROUSAL; GABA-A RECEPTOR AGONISTS; MALE; MODELS, ANIMAL; MUSCIMOL; NOISE; RATS; RATS, WISTAR; RESPIRATION; RESTRAINT, PHYSICAL; STRESS, PHYSIOLOGICAL; TIDAL VOLUME;

EID: 84902675071     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00528.2013     Document Type: Article

References (38)

1. Applegate CD, Frysinger RC, Kapp BS, Gallagher M. Multiple unit activity recorded from amygdala central nucleus during Pavlovian heartrate conditioning in rabbit. Brain Res 238: 457-462, 1982.
2. Applegate CD, Kapp BS, Underwood MD. Autonomic and somatomotor effects of amygdala central N. stimulation in awake rabbits. Physiol Behav 31: 353-360, 1983.
3. Bobrovskaya L, Beard D, Bondarenko E, Beig MI, Jobling P, Walker FR, Day TA, Nalivaiko E. Does exposure to chronic stress influence blood pressure in rats? Auton Neurosci 177: 217-223, 2013.
4. Boiten FA, Frijda NH, Wientjes C. Emotions and respiratory patterns: review and critical analysis. Int J Psychophysiol 17: 103-128, 1994.
5. Carnevali L, Sgoifo A, Trombini M, Landgraf R, Neumann ID, Nalivaiko E. Different patterns of respiration in rat lines selectively bred for high or low anxiety. PLoS One 8: e64519, 2013.
6. Chiou RJ, Kuo CC, Yen CT. Comparisons of terminal densities of cardiovascular function-related projections from the amygdala subnuclei. Auton Neurosci 181: 21-30, 2014.
7. Dampney RAL, Horiuchi J, McDowall LM. Hypothalamic mechanisms coordinating cardiorespiratory function during exercise and defensive behaviour. Auton Neurosci 142: 3-10, 2008.
8. de Carvalho MR, Dias GP, Cosci F, de-Melo-Neto VL, Bevilaqua MCdN, Gardino PF, Nardi AE. Current findings of fMRI in panic disorder: contributions for the fear neurocircuitry and CBT effects. Expert Rev Neurother 10: 291-303, 2010.
9. Dutschmann M, Dick TE. Pontine mechanisms of respiratory control. Compr Physiol 2: 2443-2469, 2012.
10. Evans KC, Dougherty DD, Schmid AM, Scannell E, McCallister A, Benson H, Dusek JA, Lazar SW. Modulation of spontaneous breathing via limbic/paralimbic-bulbar circuitry: An event-related fMRI study. Neuroimage 47: 961-971, 2009.
11. Genest SE, Balon N, Laforest S, Drolet G, Kinkead R. Neonatal maternal separation and enhancement of the hypoxic ventilatory response in rat: the role of GABAergic modulation within the paraventricular nucleus of the hypothalamus. J Physiol 583: 299-314, 2007.
12. Genest SE, Gulemetova R, Laforest S, Drolet G, Kinkead R. Neonatal maternal separation and sex-specific plasticity of the hypoxic ventilatory response in awake rat. J Physiol 554: 543-557, 2004.
13. Genest SE, Gulemetova R, Laforest S, Drolet G, Kinkead R. Neonatal maternal separation induces sex-specific augmentation of the hypercapnic ventilatory response in awake rat. J Appl Physiol 102: 1416-1421, 2006.
14. Homma I, Masaoka Y. Breathing rhythms and emotions. Exp Physiol 93: 1011-1021, 2008.
15. Iwata J, LeDoux JE, Meeley MP, Arneric S, Reis DJ. Intrinsic neurons in the amygdaloid field projected to by the medial geniculate body mediate emotional responses conditioned to acoustic stimuli. Brain Res 383: 195-214, 1986.
16. Kabir MM, Beig MI, Baumert M, Trombini M, Mastorci F, Sgoifo A, Walker FR, Day TA, Nalivaiko E. Respiratory pattern in awake rats: effects of motor activity and of alerting stimuli. Physiol Behav 101: 22-31, 2010.
17. Kalueff AV, Tuohimaa P. The grooming analysis algorithm discriminates between different levels of anxiety in rats: potential utility for neurobehavioural stress research. J Neurosci Methods 143: 169-177, 2005.
18. Kinkead R, Balon N, Genest SE, Gulemetova R, Laforest S, Drolet G. Neonatal maternal separation and enhancement of the inspiratory (phrenic) response to hypoxia in adult rats: disruption of GABAergic neurotransmission in the nucleus tractus solitarius. Eur J Neurosci 27: 1174-1188, 2008.
19. Kuwaki T. Orexin links emotional stress to autonomic functions. Auton Neurosci 161: 20-27, 2011.
20. Masaoka Y, Hirasawa K, Yamane F, Hori T, Homma I. Effects of left amygdala lesions on respiration, skin conductance, heart rate, anxiety, and activity of the right amygdala during anticipation of negative stimulus. Behav Modif 27: 607-619, 2003.
21. Masaoka Y, Homma I. Amygdala and emotional breathing in humans. In: Postgenomic Perspectives in Modeling and Control of Breathing, edited by Champagnat J, Denavit-Saubié M, Fortin G, Foutz A, and Thoby-Brisson M. New York: Springe, 2005, p. 9-14.
22. McDougall SJ, Widdop RE, Lawrence AJ. Central autonomic integration of psychological stressors. Focus on cardiovascular modulation. Auton Neurosci 123: 1-11, 2005.
23. Nalivaiko E, Bondarenko E, Carnevali L, Kindig AE, Sgoifo A, Hodgson D. Respiratory responses to acoustic stimulation and restraint stress are inhibited by diazepam: a novel index of anxiety in rats. FASEB J 25, 1111.4, 2011.
24. Nalivaiko E, Bondarenko E, Lidstrom A, Barry RJ. Respiratory component of the orienting reflex: a novel sensitive index of sensory-induced arousal in rats. Front Physiol 2: 114, 2011.
25. Nardi AE, Freire RC, Zin WA. Panic disorder and control of breathing. Respir Physiol Neurobiol 167: 133-143, 2009.
26. Paxinos G, Watson C. The Rat Brain: in Stereotaxic Coordinates: San Diego, CA: Academic, 1998.
27. Reyes del Paso, G., Vila J. Respiratory influences on the cardiac defense response. Int J Psychophysiol 15: 15-26, 1993.
28. Shekhar A. GABA receptors in the region of the dorsomedial hypothalamus of rats regulate anxiety in the elevated plus-maze test. I. Behavioral measures. Brain Res 627: 9-16, 1993.
29. Shekhar A, Sims LS, Bowsher RR. GABA receptors in the region of the dorsomedial hypothalamus of rats regulate anxiety in the elevated plusmaze test. II. Physiological measures. Brain Res 627: 17-24, 1993.
30. Smith JC, Abdala APL, Borgmann A, Rybak IA, Paton JFR. Brainstem respiratory networks: building blocks and microcircuits. Trends Neurosci 36: 152-162, 2013.
31. Soltis RP, Cook JC, Gregg AE, Sanders BJ. Interaction of GABA and excitatory amino acids in the basolateral amygdala: role in cardiovascular regulation. J Neurosci 17: 9367-9374, 1997.
32. Sominsky L, Fuller EA, Bondarenko E, Ong LK, Averell L, Nalivaiko E, Dunkley PR, Dickson PW, Hodgson DM. Functional programming of the autonomic nervous system by early life immune exposure: implications for anxiety. PLoS One 8: e57700, 2013.
33. Stekelenburg JJ, Boxtel A. Pericranial muscular, respiratory, and heart rate components of the orienting response. Psychophysiology 39: 707-722, 2002.
34. Suess WM, Alexander AB, Smith DD, Sweeney HW, Marion RJ. The effects of psychological stress on respiration: a preliminary study of anxiety and hyperventilation. Psychophysiology 17: 535-540, 1980.
35. Tanaka M, McAllen RM. Functional topography of the dorsomedial hypothalamus. Am J Physiol Regul Integr Comp Physiol 294: R477-R486, 2008.
36. Tulen JHM, Mulder G, Pepplinkhuizen L, Intveld AJM, Vansteenis HG, Moleman P. Effects of Lorazepam on cardiac vagal tone during rest and mental stress. Assessment by means of spectral-analysis. Psychopharmacology (Berl) 114: 81-89, 1994.
37. Vianna DML, Allen C, Carrive P. Cardiovascular and behavioral responses to conditioned fear after medullary raphe neuronal blockade. Neuroscience 153: 1344-1353, 2008.
38. Zhang W, Zhang N, Sakurai T, Kuwaki T. Orexin neurons in the hypothalamus mediate cardiorespiratory responses induced by disinhibition of the amygdala and bed nucleus of the stria terminalis. Brain Res 1262: 25-37, 2009.