Journal of Coloproctology Journal of Coloproctology
J Coloproctol. (Rio J.) 2017;37:88-94 - Vol. 37 Num.2 DOI: 10.1016/j.jcol.2016.12.006
Original Article
Acute physical and psychological stress effects on visceral hypersensitivity in male rat: role of central nucleus of the amygdala
Efeitos agudos do estresse físico e psicológico na hipersensibilidade visceral em rato macho: papel do núcleo central da amídala
Hamideh Afzalia, Fatemeh Nabavizadeha,, , Seyed Morteza Karimiana, Hamid Sohanakia, Jalal Vahedianb,c, Seyed Mehdi Mohamadib,c
a Tehran University of Medical Sciences, School of Medicine, Department of Physiology, Tehran, Iran
b Iran University of Medical Sciences, School of Medicine, Department of Physiology, Tehran, Iran
c Iran University of Medical Sciences, Firouzgar Hospital, Department of Surgery, Tehran, Iran
Received 19 November 2016, Accepted 21 December 2016
Abstract
Objective

The aim of this study was to investigate the effects of acute physical and psychological stress and temporary central nucleus of the amygdala (CeA) block on stress-induced visceral hypersensitivity.

Methods

Forty two male Wistar rats were used in this study. Animals were divided into 7 groups (n=6); 1 – Control, 2 – physical stress, 3 – psychological stress, 4 – sham, 5 – lidocaine, 6 – lidocaine+physical stress and 7 – lidocaine+psychological stress. Stress induction was done using a communication box.

Results

Abdominal withdrawal reflex (AWR) score was monitored one hour after stress exposure. AWR score significantly heightened at 20, 40 and 60mmHg in the psychological stress group compared with control (p<0.05), while, it was almost unchanged in other groups. This score was strikingly decreased at 20, 40 and 60mmHg in lidocaine+psychological stress group compared with psychological stress with no tangible response on physical stress. Total stool weight was significantly increased in psychological stress group compared with control (0.72±0.15, 0.1±0.06g) (p<0.05), but it did not change in physical stress compared to control group (0.16±0.12, 0.1±0.06g) (p<0.05). Concomitant use of lidocaine with stress followed the same results in psychological groups (0.18±0.2, 0.72±0.15g) (p<0.05), while it did not have any effect on physical stress group (0.25±0.1, 0.16±0.12g) (p<0.05).

Conclusions

Psychological stress could strongly affect visceral hypersensitivity. This effect is statistically comparable with physical stress. Temporary CeA block could also reduce visceral hypersensitivity post-acute psychological stress.

Resumen
Objetivo

O objetivo desse estudo foi investigar os efeitos do estresse físico e psicológico agudo e bloqueio temporário do núcleo central da amídala (CeA) na hipersensibilidade visceral induzida por estresse.

Métodos

Quarenta e dois ratos Wistar machos foram empregados nesse estudo. Os animais foram divididos em 7 grupos (n=6): 1 – Controle, 2 – estresse físico, 3 – estresse psicológico, 4 – simulacro, 5 – lidocaína, 6 – lidocaína+estresse físico e 7 – lidocaína+estresse psicológico. A indução do estresse foi feita com o uso de uma caixa de comunicação.

Resultados

O escore do reflexo de retirada abdominal (RRA) foi monitorado uma hora depois da exposição ao estresse. O escore RRA aumentou significativamente a 20, 40 e 60mmHg no grupo de estresse psicológico versus controle (p<0,05), enquanto que praticamente permaneceu inalterado nos demais grupos. Esse escore diminuiu drasticamente a 20, 40 e 60mmHg no grupo de lidocaína+estresse psicológico versus estresse psicológico, sem resposta tangível no estresse físico. O peso total das fezes aumentou significativamente no grupo de estresse psicológico versus controle (0,72±0,15, 0,1±0,06g) (p<0,05), mas não houve mudança no grupo de estresse físico versus controle (0,16±0,12, 0,1±0,06g) (p<0,05). O uso simultâneo da lidocaína com o estresse acompanhou os mesmos resultados nos grupos psicológicos (0,18±0,2, 0,72±0,15g) (p<0,05), enquanto que não foi observado qualquer efeito no grupo de estresse físico (0,25±0,1, 0,16±0,12g) (p<0,05).

Conclusões

O estresse psicológico pode afetar fortemente a hipersensibilidade visceral. Esse efeito é estatisticamente comparável com o estresse físico. Um bloqueio temporário do CeA também pode reduzir a hipersensibilidade visceral pós-estresse psicológico agudo.

Keywords
Abdominal withdrawal reflex, Amygdala, Physical stress, Psychological stress, Visceral hypersensitivity
Introduction

Visceral hypersensitivity is now a common hypothesis used to explain the painful symptoms in patients suffering from irritable bowel syndrome (IBS). IBS is a prevalent gastrointestinal disorder characterized by abdominal pain and bowel habit changes with unexplored etiology.1 Almost 22% of the population experiences IBS symptoms.2 Difficulty in diagnosis and inadequate good treatment together with high social and medical costs changed IBS into a social concern.3,4

Psychological and physical stressors have been identified as important factors in IBS pathophysiology.5,6 Researchers have found a relationship between central pathways of stress and anxiety and peripheral mechanisms modulating gastrointestinal sensitivity. Amygdala, especially the central nucleus of amygdala (CeA), which has a pivotal role on this relationship; mainly affects endocrine and autonomic reply to stress and causes visceral hypersensitivity.7 Visceral hypersensitivity is commonly examined via different forms among which communication box seems to be an agreeable tool for concomitant study of physiological and behavioral changes under psychological and physical stresses.8

However, to the best of our knowledge, this is the first study which focuses on rat visceral hypersensitivity post induction in the communication box environment. Therefore, the aim of the current study was to investigate the role of CeA block in visceral hypersensitivity response post communication box induced physical and psychological stress model in male rats.

Materials and methodsAnimals

Forty two male Wistar rats (250–325g) purchased from physiology department of Tehran University of Medical Sciences (TUMS). Animals were kept under standard conditions of 12-h:12-h light/dark cycle with unlimited access to the standard rat chow and water. All experiments were performed upon TUMS ethical committee approval between 8 am up to 3 pm every day.

Experimental protocol

Experiments were performed on seven equally assigned animal groups (n=6) as per the following classification:

  • 1.

    Control; animals placed in stress box 15min without receiving electric foot shock.

  • 2.

    Physical stress; animals placed in stress box and received 5s electrical shock (2mA), then 55s rest for 15min.

  • 3.

    Psychological stress; animals placed in the safe compartments for 15min without receiving foot shock and then received visual, auditory and olfactory sensation cues from the neighboring animal,

  • 4.

    Sham; animals received bilateral microinjections of normal saline (0.5–1μl) into central nucleus of the amygdala (CeA) 5min before placing into the stress box followed by the same procedure as group 1.

  • 5.

    Lidocaine; animals received bilateral microinjections of lidocaine (0.5–1μl, 2%). into CeA

  • 6.

    Physical stress+lidocaine; animals received bilateral microinjections of lidocaine into CeA 5min before placing into the stress box followed by the same procedure as group 2.

  • 7.

    Psychological stress+lidocaine; animals received bilateral microinjections of lidocaine into CeA 5min before placing into the stress box followed by the same procedure as group 3.

Stereotaxic surgery

Animals anesthetized first with a mixture of ketamine (50mg/kg, ip) and xylazine (5mg/kg, ip) and placed in a stereotaxic apparatus. The skull was clean shaved and a midline incision made. Connective tissues were then removed to have the best access to lambda bregma landmarks. Two holes were made with a micro drill over the skull according to rat brain anatomical atlas (paxinos) coordinates (2.5mm posterior to the bregma, 4.4mm bilateral to midline and 8mm from the top. Two 23-gauge stainless steel guide cannulas were bilaterally lowered until their tips stood 2mm above CeA and fixed to the skull surface with dental cement. Cannula sites were confirmed via methylene blue color injection and tissue section studies. Upon completion, animals backed to their cages for a week recovery before handling stress accommodation.9 Normal saline (0.5–1μl) and lidocaine (0.5–1μl, 2%)10,11 delicately injected with a Hamilton syringe connected to a 30-gauge cannula extended 2mm below the guide cannula tip. Lidocaine acted as temporary blocker of both neurons and tracts in the amygdala region.11 Injections were made over 1min to allow maximal diffusion. The cannula was also slowly withdrawn during the same time period.9

Body temperature kept at 37°C with a homoeothermic heating pad.

Stress box and electrical shock device

Communication box apparatus was designed for stress stimulus application. The apparatus consists of nine compartments of 50cm×16cm×16cm, separated by transparent plastic walls. To apply psychological stress, each rat is individually placed into one compartment and isolated from others by transparent walls with no physical contact, but free to receive visual, auditory and olfactory sensation cues from the neighboring rat. The floor of each compartment was covered with metal grids made up of 5mm diameter stainless steel rods placed 1.3cm apart connected to an electric shock generator (current of 2mA) (Borj Sanat Co., Iran, sensitivity 0.1–10mA) to apply foot shock with 5s duration and 55s interval.12 Four compartments grids were insulated with plastic rolls to serve as shock-free compartments for psychological stress group.13

Total stool weight measurement

Each rat backed to an individual cage immediately after stress exposure for 30min with free access to standard chow and water. Feces were collected, weighed and reported as total stool weight.12

Behavioral tests

Visceral hypersensitivity was monitored 1 hour after stress exposure using visual observation of animal response to graded colorectal distention (CRD), as previously described.14,15 Animals inhaled diethyl ether inhalation under a glass bell for a light anesthesia. A 5cm balloon made up of surgical glove finger attached to a tygon tube, inserted into the anal canal and advanced 8cm into the descending colon and fixed to the animal tail with an adhesive tape. The tube end attached to a sphygmomanometer via a Y-connector. Rats were then recovered from anesthesia and allowed to adapt for about 30min. CRD was carried out through rapidly inflating the balloon to different pressure amount including 20, 40, 60 and 80mmHg for a 20s followed by 2min rest. Behavioral responses to CRD were monitored by an observer blind to the experiment and recorded as abdominal withdrawal reflex (AWR) score as follows: 0, no behavioral response; 1, brief head movement followed by immobile status; 2, abdominal muscle contraction; 3, abdominal wall lifting; 4, body arching and pelvic structures lifting.

Determination of plasma corticosterone level

At the end of the experiments, animals were anesthetized with diethyl ether. Blood samples were collected by cardiac puncture and kept in EDTA coated tubes for further plasma separation. Samples stored at −70°C till morning assay. Corticosterone ELISA kit (DRG, Germany) was used to determine corticosterone level.

Histology

At the end of the experiment, injection sites were evaluated for accuracy with methylene blue microinjections (0.25μL/each side). Animals were then decapitated under diethyl ether inhalation. Brains were removed and fixed in formalin (10%) solution. Coronal sections (50μm) were also prepared and examined for CeA injection site.16

Statistical analysis

Data represented as mean±SEM. Statistical analysis was performed by SPSS software, version 19.0. Nonparametric Friedman test used to asses AWR scores at respective pressures within each group. Averaged AWR score at each CRD pressure were compared among groups using Kruskal–Wallis one-way analysis of variance. Hormone levels and total stools weight were compared with analysis of variance (ANOVA) followed by Tukey post hoc test. p<0.05 was considered as significant statistical level.

Results

Acute physical and psychological stresses and temporary CeA block effects on AWR scores were shown in (Fig. 1). AWR scores significantly increased at 20, 40 and 60mmHg in psychological stress group compared with control (p<0.05). AWR scores in other groups were slightly increased at 20, 40, 60 and 80mmHg compared with control (p>0.05). These scores were significantly decreased at 20, 40 and 60mmHg in lidocaine+psychological stress group compared with the psychological stress group. No significant differences were observed between AWR scores of lidocaine+physical stress compared with physical stress group.

Fig. 1.
(0.13MB).

Effect of acute physical and psychological stresses and temporary central nucleus of amygdala (CeA) block on withdrawal reflex (AWR) scores. Control, physical (phy), psychological (psy), sham, lidocain (lid), lidocain+physical (lid+phy), lidocain+psychological (lid+psy) stresses. *p<0.05 comparison of psy stress group with control and #p<0.05 lid+psy with psy.

Total stool weight post stress exposure in psychological stress group was significantly higher than control group (0.72±0.15, 0.1±0.06g), but it did not statistically change in physical stress compared to control group (0.16±0.12, 0.1±0.06g) (Fig. 2). Rats in psychological+lidocaine stress group showed a significant decrease in total stool weight compared with psychological stress group (0.18±0.2, 0.72±0.15g). No significant difference was observed between total stool weights in lidocaine+physical group compared with physical one (0.25±0.1, 0.16±0.12g) (Fig. 2).

Fig. 2.
(0.08MB).

Effect of acute physical and psychological stresses and temporary central nucleus of amygdala (CeA)block on total stool weight post stress exposure during 30min. Control, physical (phy), psychological (psy), sham, lidocain (lid), lidocain+physical (lid+phy), lidocain+psychological (lid+psy) stresses (Mean±SE, n=6). *p<0.05 comparison of psy stress groups with control and #p<0.05 05 comparison of psy+lid stress with psy stress group.

The effect of acute physical and psychological stresses and temporary CeA block on plasma corticosterone level were shown in (Fig. 3). Significant differences were seen in plasma corticosterone levels of control, physical and psychological stress groups (1258.17±11.9, 1723.50±5.7, 1700.50±5.5ng/ml) (p<0.05). Plasma corticosterone level significantly decreased in lidocaine group compared with the sham animals (1235.50±8.6, 1622±1.6ng/ml) (p<0.05).

Fig. 3.
(0.07MB).

Effect of acute physical and psychological stresses and temporary central nucleus of amygdala (CeA) block on plasma corticosterone level. Control, physical (phy), psychological (psy), sham, lidocain (lid), lidocain+physical (lid+phy), lidocain+psychological (lid+psy) stresses (Mean±SE, n=6). *p<0.05 comparison of phy and psy stress groups with Control, $lid with sham p<0.05 and #p<0.05 lid+phy, lid+psy with phy and psy.

Plasma corticosterone level was significantly decreased in lidocaine+physical group compared with physical group (1132.33±13.6, 1723.50±5.7ng/ml), whereas no significant changes were observed between corticosterone level of the lidocaine+psychological group compared with psychological group (1391.67±9.9, 1700.50±5.5ng/ml) (Fig. 3).

Discussion

In the present study, we investigated the acute physical and psychological stress effects on visceral hypersensitivity together with temporary CeA block response to stress-induced visceral hypersensitivity in male rat. One clinical study reported when IBS patient faced with acute stress, decreased significantly rectal threshold perception and pain, As a result of increased visceral sensitivity in these patients.17

Our results showed that acute psychological stress could significantly increase abdominal contraction responses to CRD especially at 20, 40, and 60mmHg. This is in congruent with other preceding studies showing increased visceral sensitivity post-acute physical and psychological stresses.17–19

Some studies have shown limbic system involvement including amygdala in response to visceral stimulation,20–22 also the techniques that examined brain activity have shown that in patients with IBS activity of limbic regions including the amygdala increased in response to rectosigmoid Stimulation.22,23

Amygdala is a central integrator for emotion, nociception, emotional pain behavior, and emotional evaluation of sensory stimuli and is vital for fear and anxiety senses.20,24

It consists of many nuclei and receives versatile information from different somatosensory, olfactory, auditory, visual, gustatory and visceral senses. The lateral nucleus (LA) is its main input of the amygdala while the central nucleus (CeA) acts as the output. CeA projects mainly to cortical, hypothalamic, and brain stem regions.25 In this study we temporary blocked the output tracks and assessed stress-induced colonic hypersensitivity after temporary CeA block, especially at lower pressures. In addition, we noted that temporary CeA block could decrease visceral hypersensitivity clearly among animals exposed to psychological stress.

Sever stress is outcomes life car and predispose to diseases such as IBS. Stress first activates hypothalamic–pituitary–adrenal (HPA) axis. This causes hypothalamic corticotropin releasing hormone (CRH) secretion at the next step and finally pituitary adrenocorticotropin (ACTH) secretion and corticosterone release.26

In this study, plasma corticosterone level was significantly increased in physical and psychological stress groups in comparison to control. These results are in congruent with previous studies indicating increased level of plasma corticosterone as the most important signs of physical & psychological stress.27,28

Stimulation of CeA has been shown to ease the HPA axis activation,29,30 while its lesions could block the axis and plasma corticosterone secretion.31

In this study increased plasma corticosterone level post physical stress was blocked by bilateral CeA lidocaine microinjections, but it was unaffected post psychological stress. This notable finding may raise the probability that an alternative modulatory pathway except that CeA is involved. Such a pathway may relate either to another central integration center or to shifted peripheral responses of visceral stimuli. Expression of different subtypes of CRH receptors with versatile regulatory response in gut functions may also explain diverse response post psychological stress application. Some studies have shown expression of two CRH receptor subtypes with quite opposite gut functions post maternal separation.32

Studies have depicted that autonomic imbalance including low vagal tone and increased sympathetic activity may also change visceral sensitivity.33 Our data showed that the autonomic system may be more contributed in visceral perception to luminal distension than the HPA axis since colonic hypersensitivity decreased after temporary CeA block, but increased plasma corticosterone level was unaffected.

In the present study, we also assessed the acute physical and psychological stress effects on total stool weight and found a significant increase post psychological stress application. This finding is in agreement with previous results showing that both stressors could enhance colonic motor activity and defecation.12,34 However, total stool weight was not significantly increased in animals exposed to physical stress.

Previous studies stated that major CeA output to solitary tract nucleus and neurons in dorsal motor nucleus of the vagus regulates colonic motility.35,36 We observed that temporary CeA block could significantly decrease total stool weight in rats exposed to psychological stress.

In conclusion, the present study showed the effects of acute physical and psychological stress together with temporary CeA block on visceral hypersensitivity, plasma corticosterone level and, total stool weight in studied rats. We also depicted that psychological stress is much more effective than physical stress on visceral hypersensitivity and total stool weight, whereas both stress types have similar effects on plasma corticosterone level.

Temporary CeA block could decrease plasma corticosterone level in acute physical stress, with no effect on plasma corticosterone level in acute psychological stress.

Visceral sensitivity and defecation clearly reduced after temporary CeA block in acute psychological stress especially at lower pressures but remained unchanged in acute physical stress.

Visceral hypersensitivity is common in IBS patients and stress is one of the factors reinforcing visceral sensitivity. In conclusion, visceral hypersensitivity is an interesting topic for researchers and a target for the discovery of a novel drug for the treatment of IBS.37

Our findings highlighted the importance of psychological stress on visceral hypersensitivity and may help in evaluating the patients suffering from IBS under psychological stress or designing therapeutical modalities with more emphasis on the autonomic dysregulation.

Conflicts of interest

The authors declare no conflicts of interest.

Acknowledgment

This research was supported by Tehran University of Medical Sciences.

References
1
D. Keszthelyi,F.J. Troost,A.A. Masclee
Irritable bowel syndrome: methods, mechanisms, and pathophysiology. Methods to assess visceral hypersensitivity in irritable bowel syndrome
Am J Physiol Gastrointest Liver Physiol, 303 (2012), pp. G141-G154 http://dx.doi.org/10.1152/ajpgi.00060.2012
2
J. Fassov,L. Lundby,J. Worsøe,S. Buntzen,S. Laurberg,K. Krogh
A randomised, controlled study of small intestinal motility in patients treated with sacral nerve stimulation for irritable bowel syndrome
BMC Gastroenterol, 14 (2014), pp. 1 http://dx.doi.org/10.1186/1471-230X-14-1
3
H.-K. Jung,Y.H. Kim,J.Y. Park,B.H. Jang,S.-Y. Park,M.-H. Nam
Estimating the burden of irritable bowel syndrome: analysis of a nationwide korean database
J Neurogastroenterol Motil, 20 (2014), pp. 242-252 http://dx.doi.org/10.5056/jnm.2014.20.2.242
4
J.-F. Ricci,P. Jhingran,T. McLaughlin,E.G. Carter
Costs of care for irritable bowel syndrome in managed care
JCOM – Wayne PA, 7 (2000), pp. 23-34
5
E.A. Mayer,B.D. Naliboff,L. Chang,S.V.V. Coutinho
Stress and irritable bowel syndrome
Am J Physiol Gastrointest Liver Physiol, 280 (2001), pp. G519-G524
6
H.-Y. Qin,C.-W. Cheng,X.-D. Tang,Z.-X. Bian
Impact of psychological stress on irritable bowel syndrome
World J Gastroenterol, 20 (2014), pp. 14126-14131 http://dx.doi.org/10.3748/wjg.v20.i39.14126
7
B. Myers,B. Greenwood-Van Meerveld
Role of anxiety in the pathophysiology of irritable bowel syndrome: importance of the amygdala
8
Y. Endo,K. Yamauchi,Y. Fueta,M. Irie
Changes of body temperature and plasma corticosterone level in rats during psychological stress induced by the communication box
Med Sci Monit, 7 (2001), pp. 1161-1165
9
M. Rashvand,A. Khajavai,M. Parviz,P. Hasanein,M. Keshavarz
GABAA receptors are involved in the analgesic effects of morphine microinjected into the central nucleus of the amygdala
Clin Exp Pharmacol Physiol, 41 (2014), pp. 338-344 http://dx.doi.org/10.1111/1440-1681.12223
10
S. Ahn,A.G. Phillips
Modulation by central and basolateral amygdalar nuclei of dopaminergic correlates of feeding to satiety in the rat nucleus accumbens and medial prefrontal cortex
J Neurosci, 22 (2002), pp. 10958-10965
11
P. Carrive,J. Lee,A. Su
Lidocaine blockade of amygdala output in fear-conditioned rats reduces Fos expression in the ventrolateral periaqueductal gray
Neuroscience, 95 (2000), pp. 1071-1080
12
T. Hirata,T. Funatsu,Y. Keto,S. Akuzawa,M. Sasamata,K. Miyata
Inhibitory effects of ramosetron, a potent and selective 5-HT3-receptor antagonist, on conditioned fear stress-induced abnormal defecation and normal defecation in rats: comparative studies with antidiarrheal and spasmolytic agents
J Pharmacol Sci, 106 (2008), pp. 264-270
13
N. Fatemeh,V. Mohammad,S. Hedayat,A. Soheila,S. Ehsan
Physical and psychological stress have similar effects on gastric acid and pepsin secretions in rat
J Stress Physiol Biochem, (2011), pp. 7164-7174
14
E.D. Al-Chaer,M. Kawasaki,P.J. Pasricha
A new model of chronic visceral hypersensitivity in adult rats induced by colon irritation during postnatal development
Gastroenterology, 119 (2000), pp. 1276-1285
15
X. Guo,J. Chen,Y. Lu,L. Wu,Z. Weng,L. Yang
Electroacupuncture at He-Mu points reduces P2X4 receptor expression in visceral hypersensitivity
Neural Regen Res, 8 (2013), pp. 2069-2077 http://dx.doi.org/10.3969/j.issn.1673-5374.2013.22.006
16
G. Paxinos,C. Watson
The rat brain in stereotaxic coordinates
Academic, (1986)
17
C.D. Murray,J. Flynn,L. Ratcliffe,M.R. Jacyna,M.A. Kamm,A.V. Emmanuel
Effect of acute physical and psychological stress on gut autonomic innervation in irritable bowel syndrome
Gastroenterology, 127 (2004), pp. 1695-1703
18
S. Bradesi,H. Eutamene,R. Garcia-Villar,J. Fioramonti,L. Bueno
Acute and chronic stress differently affect visceral sensitivity to rectal distension in female rats
Neurogastroenterol Motil, 14 (2002), pp. 75-82
19
Y. Sun,F.L. Liu,G.Q. Song,W. Qian,X.H. Hou
Effects of acute and chronic restraint stress on visceral sensitivity and neuroendocrine hormones in rats
Chin J Dig Dis, 7 (2006), pp. 149-155 http://dx.doi.org/10.1111/j.1443-9573.2006.00260.x
20
M. Davis
Neurobiology of fear responses: the role of the amygdala
J Neuropsychiatry Clin Neurosci, 9 (1997), pp. 382-402 http://dx.doi.org/10.1176/jnp.9.3.382
21
V.D. Felice,S.M. Gibney,R.D. Gosselin,T.G. Dinan,S.M. O’Mahony,J.F. Cryan
Differential activation of the prefrontal cortex and amygdala following psychological stress and colorectal distension in the maternally separated rat
22
B.D. Naliboff,S.W. Derbyshire,J. Munakata,S. Berman,M. Mandelkern,L. Chang
Cerebral activation in patients with irritable bowel syndrome and control subjects during rectosigmoid stimulation
Psychosom Med, 63 (2001), pp. 365-375
23
C. Wilder-Smith,D. Schindler,K. Lovblad,S. Redmond,A. Nirkko
Brain functional magnetic resonance imaging of rectal pain and activation of endogenous inhibitory mechanisms in irritable bowel syndrome patient subgroups and healthy controls
24
C. Strobel,S. Hunt,R. Sullivan,J. Sun,P. Sah
Emotional regulation of pain: the role of noradrenaline in the amygdala
Sci China Life Sci, 57 (2014), pp. 384-390 http://dx.doi.org/10.1007/s11427-014-4638-x
25
V. Neugebauer,W. Li,G.C. Bird,J.S. Han
The amygdala and persistent pain
Neurosci: Rev J Neurobiol Neurol Psychiatry Neurosci, 10 (2004), pp. 221-234
26
S.M. Smith,W.W. Vale
The role of the hypothalamic–pituitary–adrenal axis in neuroendocrine responses to stress
Dialogues Clin Neurosci, 8 (2006), pp. 383-395
27
G.P. Chrousos,P.W. Gold
The concepts of stress and stress system disorders. Overview of physical and behavioral homeostasis
JAMA, 267 (1992), pp. 1244-1252
28
M. Jafari,M. Salehi,H. Zardooz,F. Rostamkhani
Response of liver antioxidant defense system to acute and chronic physical and psychological stresses in male rats
EXCLI J, 13 (2014), pp. 161-171
29
S. Ma,D.A. Morilak
Norepinephrine release in medial amygdala facilitates activation of the hypothalamic–pituitary–adrenal axis in response to acute immobilisation stress
J Neuroendocrinol, 17 (2005), pp. 22-28 http://dx.doi.org/10.1111/j.1365-2826.2005.01279.x
30
E.S. Redgate,E.E. Fahringer
A comparison of the pituitary adrenal activity elicited by electrical stimulation of preoptic, amygdaloid and hypothalamic sites in the rat brain
Neuroendocrinology, 12 (1973), pp. 334-343
31
S. Feldman,N. Conforti,A. Itzik,J. Weidenfeld
Differential effect of amygdaloid lesions on CRF-41, ACTH and corticosterone responses following neural stimuli
Brain Res, 658 (1994), pp. 21-26
32
D. O’Malley,T.G. Dinan,J.F. Cryan
Alterations in colonic corticotropin-releasing factor receptors in the maternally separated rat model of irritable bowel syndrome: differential effects of acute psychological and physical stressors
33
G. Tougas
The autonomic nervous system in functional bowel disorders
Can J Gastroenterol, 13 (1999), pp. 15A-17A
34
S.S. Rao,R.A. Hatfield,J.M. Suls,M.J. Chamberlain
Psychological and physical stress induce differential effects on human colonic motility
Am J Gastroenterol, 93 (1998), pp. 985-990 http://dx.doi.org/10.1111/j.1572-0241.1998.00293.x
35
O.A. Lyubashina
Possible mechanisms of involvement of the amygdaloid complex in the control of gastric motor function
Neurosci Behav Physiol, 34 (2004), pp. 379-388
36
K. Venkova,A.C. Johnson,B. Myers,B. Greenwood-Van Meerveld
Exposure of the amygdala to elevated levels of corticosterone alters colonic motility in response to acute psychological stress
Neuropharmacology, 58 (2010), pp. 1161-1167 http://dx.doi.org/10.1016/j.neuropharm.2010.02.012
37
M. Kanazawa,M. Hongo,S. Fukudo
Visceral hypersensitivity in irritable bowel syndrome
J Gastroenterol Hepatol, 26 (2011), pp. 119-121 http://dx.doi.org/10.1111/j.1440-1746.2011.06640.x
Corresponding author. (Fatemeh Nabavizadeh nabavizadeh@tums.ac.ir)
J Coloproctol. (Rio J.) 2017;37:88-94 - Vol. 37 Num.2 DOI: 10.1016/j.jcol.2016.12.006