Inhibition of food intake induced by acute stress in rats is due to satiation effects

Acute mild stress induces an inhibition of food intake in rats. In most studies, the cumulative daily food intake is measured but this only provides a quantitative assessment of ingestive behavior. The present study was designed to analyze the reduction in food intake induced by acute stress and to understand which behavioral and central mechanisms are responsible for it. Two different stressors, restraint stress (RS) and forced swimming stress (FSS), were applied acutely to male Wistar rats. We first measured corticosterone and ACTH in plasma samples collected immediately after acute RS and FSS in order to validate our stress models. We measured food intake after RS and FSS and determined meal patterns and behavioral satiety sequences. The expressions of CRF, NPY and POMC in the hypothalamus were also determined immediately after acute RS and FSS. The rise in corticosterone and ACTH levels after both acute RS and FSS validated our models. Furthermore, we showed that acute stress induced a reduction in cumulative food intake which lasted the whole day for RS but only for the first hour after FSS. For both stressors, this stress-induced food intake inhibition was explained by a decrease in meal size and duration, but there was no difference in ingestion speed. The behavioral satiety sequence was preserved after RS and FSS but grooming was markedly increased, which thus competed with, and could reduce, other behaviors, including eating. Lastly, we showed that RS induced an increase in hypothalamic POMC expression. These results suggest that acute stress may affect ingestive behavior by increasing satiation and to some extent by enhancing grooming, and this may be due to stimulation of the hypothalamic POMC neurons.

[1]  Gareth Williams,et al.  The hypothalamus and the control of energy homeostasis Different circuits, different purposes , 2001, Physiology & Behavior.

[2]  A. Armario,et al.  Comparison of the behavioural and endocrine response to forced swimming stress in five inbred strains of rats , 1995, Psychoneuroendocrinology.

[3]  D. Tomé,et al.  Yeast proteins enhance satiety in rats. , 2006, The Journal of nutrition.

[4]  B. McEwen,et al.  Acute stress increases neuropeptide Y mRNA within the arcuate nucleus and hilus of the dentate gyrus. , 2000, Brain research. Molecular brain research.

[5]  R. Cone Anatomy and regulation of the central melanocortin system , 2005, Nature Neuroscience.

[6]  R. Rodgers,et al.  Behavioural satiety sequence (BSS): Separating wheat from chaff in the behavioural pharmacology of appetite , 2010, Pharmacology Biochemistry and Behavior.

[7]  H. Grill,et al.  Printed in U.S.A. Copyright © 2000 by The Endocrine Society The Role of the Dorsal Vagal Complex and the Vagus Nerve in Feeding Effects of Melanocortin-3/4 Receptor Stimulation* , 2022 .

[8]  Kanji A. Takahashi,et al.  Cholecystokinin-mediated suppression of feeding involves the brainstem melanocortin system , 2004, Nature Neuroscience.

[9]  D. Tomé,et al.  Acute stress modifies food choice in Wistar male and female rats , 2008, Appetite.

[10]  Y. Taché,et al.  Neuroendocrine control of the gut during stress: corticotropin-releasing factor signaling pathways in the spotlight. , 2009, Annual review of physiology.

[11]  Alfio Bertolini,et al.  Brain effects of melanocortins. , 2009, Pharmacological research.

[12]  J. Kelly,et al.  Varying responses to the rat forced-swim test under diurnal and nocturnal conditions , 2000, Physiology & Behavior.

[13]  F. Milagro,et al.  Chronic mild stress induces variations in locomotive behavior and metabolic rates in high fat fed rats , 2007, Journal of Physiology and Biochemistry.

[14]  A. Kalueff,et al.  The grooming analysis algorithm discriminates between different levels of anxiety in rats: potential utility for neurobehavioural stress research , 2005, Journal of Neuroscience Methods.

[15]  S. Heinrichs,et al.  The role of corticotropin-releasing factor and urocortin in the modulation of ingestive behavior , 1999, Neuropeptides.

[16]  E. Roubos,et al.  Housekeeping genes revisited: Different expressions depending on gender, brain area and stressor , 2008, Neuroscience.

[17]  M. Hanson,et al.  Sensitivity of housekeeping genes in the hypothalamus to mismatch in diets between pre- and postnatal periods in mice , 2008, Neuroscience Letters.

[18]  R. Ekman,et al.  Suppressed neuropeptide Y (NPY) mRNA in rat amygdala following restraint stress , 1998, Regulatory Peptides.

[19]  J. Halford,et al.  Acute effects of olanzapine on behavioural expression including the behavioural satiety sequence in female rats , 2010, Journal of psychopharmacology.

[20]  A. Armario,et al.  Influence of single or repeated experience of rats with forced swimming on behavioural and physiological responses to the stressor , 2000, Behavioural Brain Research.

[21]  M. Mengi,et al.  Different effects of tianeptine pretreatment in rats exposed to acute stress and repeated severe stress. , 2009, Methods and findings in experimental and clinical pharmacology.

[22]  H. Grill,et al.  A potential role for hypothalamomedullary POMC projections in leptin-induced suppression of food intake. , 2010, American journal of physiology. Regulatory, integrative and comparative physiology.

[23]  R. Harris,et al.  Chronic disruption of body weight but not of stress peptides or receptors in rats exposed to repeated restraint stress , 2006, Hormones and Behavior.

[24]  S. Bhatnagar,et al.  Changes in Hypothalamic‐Pituitary‐Adrenal Function, Body Temperature, Body Weight and Food Intake with Repeated Social Stress Exposure in Rats , 2006, Journal of neuroendocrinology.

[25]  C. Dayas,et al.  Stressor categorization: acute physical and psychological stressors elicit distinctive recruitment patterns in the amygdala and in medullary noradrenergic cell groups , 2001, The European journal of neuroscience.

[26]  M. Carli,et al.  Effect of 5-HT1A agonists on stress-induced deficit in open field locomotor activity of rats: Evidence that this model identifies anxiolytic-like activity , 1989, Neuropharmacology.

[27]  J. Velázquez-Moctezuma,et al.  Body weight gain and diurnal differences of corticosterone changes in response to acute and chronic stress in rats , 2003, Psychoneuroendocrinology.

[28]  V. Rodríguez-Sureda,et al.  Immobilization stress alters intermediate metabolism and circulating lipoproteins in the rat. , 2002, Metabolism: clinical and experimental.

[29]  J. Halford,et al.  Behavioral Satiety Sequence (BSS) for the Diagnosis of Drug Action on Food Intake , 1998, Pharmacology Biochemistry and Behavior.

[30]  HJ Grill,et al.  Interoceptive and integrative contributions of forebrain and brainstem to energy balance control , 2001, International Journal of Obesity.

[31]  H. Berthoud,et al.  Brain stem melanocortinergic modulation of meal size and identification of hypothalamic POMC projections. , 2005, American journal of physiology. Regulatory, integrative and comparative physiology.

[32]  K. Roth,et al.  Stress induced grooming in the rat — An endorphin mediated syndrome , 1979, Neuroscience Letters.

[33]  F. Holsboer,et al.  Behavioural profiles of two Wistar rat lines selectively bred for high or low anxiety-related behaviour , 1998, Behavioural Brain Research.

[34]  Molly Carnes,et al.  Pulsatile adrenocorticotropic hormone: An overview , 1997, Biological Psychiatry.

[35]  E. Timofeeva,et al.  The corticotropin-releasing factor family of peptides and CRF receptors: their roles in the regulation of energy balance. , 2002, European journal of pharmacology.

[36]  P. G. Reeves,et al.  AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. , 1993, The Journal of nutrition.

[37]  B. Spruijt,et al.  Ethology and neurobiology of grooming behavior. , 1992, Physiological reviews.

[38]  E. Zorrilla,et al.  Role of the corticotropin‐releasing factor receptor type 2 in the control of food intake in mice: a meal pattern analysis , 2007, The European journal of neuroscience.

[39]  P. Even,et al.  Feeding Patterns and Meal Microstructure During Development of a Taste Aversion to a Threonine Devoid Diet , 2002, Nutritional neuroscience.

[40]  S. Satoh,et al.  Glucoregulatory hormones in the immobilization stress-induced increase of plasma glucose in fasted and fed rats. , 1993, Endocrinology.

[41]  G. Debilly,et al.  Effects of an acute immobilization stress upon proopiomelanocortin (POMC) mRNA levels in the mediobasal hypothalamus: a quantitative in situ hybridization study. , 1994, Brain research. Molecular brain research.

[42]  D. Ryan,et al.  Rats fed only during the light period are resistant to stress-induced weight loss , 2002, Physiology & Behavior.

[43]  G. Chrousos,et al.  Stressors, Stress, and Neuroendocrine Integration of the Adaptive Response: The 1997 Hans Selye Memorial Lecture , 1998, Annals of the New York Academy of Sciences.

[44]  C. Gaudichon,et al.  A very high 70%-protein diet does not induce conditioned taste aversion in rats. , 2004, The Journal of nutrition.

[45]  J. Morley,et al.  Effect of neuropeptide Y on ingestive behaviors in the rat. , 1987, The American journal of physiology.

[46]  G. Koob,et al.  Corticotropin-releasing factor in the paraventricular nucleus modulates feeding induced by neuropeptide Y , 1993, Brain Research.

[47]  B D Sachs,et al.  The Development of Grooming and Its Expression in Adult Animals a , 1988, Annals of the New York Academy of Sciences.

[48]  B. McEwen,et al.  Age- and Stress-Induced Changes in Corticotropin-Releasing Hormone mRNA Expression in the Paraventricular Nucleus of the Hypothalamus , 2007, Neuroendocrinology.

[49]  Evangelia Charmandari,et al.  Endocrinology of the stress response. , 2005, Annual review of physiology.

[50]  J. Ps,et al.  Forced swimming stress induced alterations in ingestive behavior in rats. , 2003 .

[51]  G. Aguilera,et al.  Role of Alpha-1-Adrenergic Receptors in the Regulation of Corticotropin-Releasing Hormone mRNA in the Paraventricular Nucleus of the Hypothalamus During Stress , 2000, Cellular and Molecular Neurobiology.

[52]  C. Tsigos,et al.  Stress hormones: physiological stress and regulation of metabolism. , 2009, Current opinion in pharmacology.

[53]  P. J. Larsen,et al.  Effect of acute stress on the expression of hypothalamic messenger ribonucleic acids encoding the endogenous opioid precursors preproenkephalin A and proopiomelanocortin , 1994, Peptides.

[54]  S. Lightman,et al.  The Neuroendocrinology of Stress: A Never Ending Story , 2008, Journal of neuroendocrinology.

[55]  N. Geary A new way of looking at eating. , 2005, American journal of physiology. Regulatory, integrative and comparative physiology.

[56]  D. Krahn,et al.  CRF antagonist partially reverses CRF- and stress-induced effects on feeding , 1986, Brain Research Bulletin.

[57]  P. Even,et al.  A high-protein diet enhances satiety without conditioned taste aversion in the rat , 2003, Physiology & Behavior.

[58]  M. Kruk,et al.  Effect of environmental stressors on time course, variability and form of self-grooming in the rat: Handling, social contact, defeat, novelty, restraint and fur moistening , 1994, Behavioural Brain Research.

[59]  Gold,et al.  Differential Regulation of Neuropeptide Y mRNA Expression in the Arcuate Nucleus and Locus Coeruleus by Stress and Antidepressants , 2000, Journal of neuroendocrinology.

[60]  G. Millington,et al.  The role of proopiomelanocortin (POMC) neurones in feeding behaviour , 2007, Nutrition & metabolism.

[61]  I. Neumann,et al.  Attenuation of the neuronal stress responsiveness and corticotrophin releasing hormone synthesis after sexual activity in male rats , 2010, Hormones and Behavior.

[62]  N. Kalin,et al.  Rapid stress-induced elevations in corticotropin-releasing hormone mRNA in rat central amygdala nucleus and hypothalamic paraventricular nucleus: An in situ hybridization analysis , 1998, Brain Research.

[63]  A. Armario,et al.  The serum glucose response to acute stress is sensitive to the intensity of the stressor and to habituation , 1990, Psychoneuroendocrinology.

[64]  Wei Zhang,et al.  The melanocortinergic pathway is rapidly recruited by emotional stress and contributes to stress-induced anorexia and anxiety-like behavior. , 2007, Endocrinology.