Chronic immobilization stress alters aspects of emotionality and associative learning in the rat.

Chronic stress significantly alters limbic neuroarchitecture and function, and potentiates emotionality in rats. Chronic restraint stress (CRS) increases aggression among familiar rats, potentiates anxiety, and enhances fear conditioning. Chronic immobilization stress (CIS) induces anxiety behavior and dendritic hypertrophy in the basolateral amygdala, which persist beyond a recovery period. However, little else is known about the emotional impact of CIS as a model of chronic stress or depression. Therefore, the authors present two experiments examining emotional and learned responses to CIS. In Experiment I, the authors examine individual differences in behaviors during and after CIS, specifically: struggling, aggression, learned helplessness, inhibitory avoidance, and escape behavior. In Experiment II, the authors confirm the effects of CIS on aggression and struggling during immobilization, and correlate individual responses with aspects of conditioned fear. Here the authors report significant effects of CIS on aggression, inhibitory avoidance, escape, as well as learned aspects of fear (i.e., fear conditioning) and inescapable stress (i.e., struggling and helplessness). These results emphasize the emotional and learned responses to CIS evident during and after the stress treatment, as well as the importance of individual differences.

[1]  B. McEwen Protective and damaging effects of stress mediators: central role of the brain , 2006, Dialogues in clinical neuroscience.

[2]  Bruce S. McEwen,et al.  The acute effects of corticosteroids on cognition: integration of animal and human model studies , 1997, Brain Research Reviews.

[3]  Joseph E LeDoux Emotion Circuits in the Brain , 2000 .

[4]  M. Seligman,et al.  Learned helplessness in the rat. , 1975, Journal of comparative and physiological psychology.

[5]  J. Morrison,et al.  Chronic behavioral stress induces apical dendritic reorganization in pyramidal neurons of the medial prefrontal cortex , 2004, Neuroscience.

[6]  Douglas W. Barrett,et al.  Behavioral characteristics of rats predisposed to learned helplessness: Reduced reward sensitivity, increased novelty seeking, and persistent fear memories , 2005, Behavioural Brain Research.

[7]  T. Robbins,et al.  Complementary roles for the amygdala and hippocampus in aversive conditioning to explicit and contextual cues , 1991, Neuroscience.

[8]  M. Seligman,et al.  Coping behavior: learned helplessness, physiological change and learned inactivity. , 1980, Behaviour research and therapy.

[9]  R. Bolles,et al.  Naloxone and shock-elicited freezing in the rat. , 1979 .

[10]  Robert M. Sapolsky,et al.  Stress and Plasticity in the Limbic System , 2003, Neurochemical Research.

[11]  J. Morrison,et al.  Reversibility of apical dendritic retraction in the rat medial prefrontal cortex following repeated stress , 2005, Experimental Neurology.

[12]  Stephen Maren,et al.  The Amygdala Is Essential for the Development of Neuronal Plasticity in the Medial Geniculate Nucleus during Auditory Fear Conditioning in Rats , 2001, The Journal of Neuroscience.

[13]  C. Sandi,et al.  Effects of chronic stress on contextual fear conditioning and the hippocampal expression of the neural cell adhesion molecule, its polysialylation, and L1 , 2001, Neuroscience.

[14]  B. McEwen,et al.  Acute and chronic restraint stress alter the incidence of social conflict in male rats , 2003, Hormones and Behavior.

[15]  D. Zhukov,et al.  Learned helplessness or learned inactivity after inescapable stress? Interpretation depends on coping styles , 2002, Integrative physiological and behavioral science : the official journal of the Pavlovian Society.

[16]  Masatoshi Tanaka,et al.  Expression of Aggression Attenuates Both Stress-Induced Gastric Ulcer Formation and Increases in Noradrenaline Release in the Rat Amygdala Assessed by Intracerebral Microdialysis , 1998, Pharmacology Biochemistry and Behavior.

[17]  Xin Zhao,et al.  Effects of the Chinese Traditional Prescription Xiaoyaosan Decoction on Chronic Immobilization Stress-induced Changes in Behavior and Brain BDNF, TrkB, and NT-3 in Rats , 2008, Cellular and Molecular Neurobiology.

[18]  J. W. Rudy,et al.  A selective role for corticosterone in contextual-fear conditioning. , 1997, Behavioral neuroscience.

[19]  M. Fanselow,et al.  Modality-specific retrograde amnesia of fear. , 1992, Science.

[20]  J. Ray,et al.  Styles of dominance and their endocrine correlates among wild olive baboons (Papio anubis) , 1989, American journal of primatology.

[21]  P. Han,et al.  Optimization of chronic stress paradigms using anxiety‐ and depression‐like behavioral parameters , 2006, Journal of neuroscience research.

[22]  T. Gregg,et al.  Brain structures and neurotansmitters regulating aggression in cats: implications for human aggression , 2001, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[23]  R. A. Fuchs,et al.  Influence of chronic corticosterone and glucocorticoid receptor antagonism in the amygdala on fear conditioning , 2004, Neurobiology of Learning and Memory.

[24]  M. Davis,et al.  Using pavlovian higher-order conditioning paradigms to investigate the neural substrates of emotional learning and memory. , 2000, Learning & memory.

[25]  Eberhard Fuchs,et al.  Chronic social stress: effects on limbic brain structures , 2003, Physiology & Behavior.

[26]  J. W. Rudy,et al.  Type II Glucocorticoid Receptor Antagonists Impair Contextual but Not Auditory-Cue Fear Conditioning in Juvenile Rats , 1997, Neurobiology of Learning and Memory.

[27]  F. Graeff,et al.  The elevated T-maze as an experimental model of anxiety , 1998, Neuroscience & Biobehavioral Reviews.

[28]  Joseph E LeDoux,et al.  Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. , 1992, Behavioral neuroscience.

[29]  B. McEwen,et al.  Stress-induced structural remodeling in hippocampus: prevention by lithium treatment. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[30]  J. Falk Physiology and Behavior. , 1973 .

[31]  C. Conrad,et al.  The effects of chronic stress on hippocampal morphology and function: An evaluation of chronic restraint paradigms , 2007, Brain Research.

[32]  S. D. de Boer,et al.  Coping with stress in rats and mice: differential peptidergic modulation of the amygdala-lateral septum complex. , 1998, Progress in brain research.

[33]  S. Chattarji,et al.  Recovery after chronic stress fails to reverse amygdaloid neuronal hypertrophy and enhanced anxiety-like behavior , 2004, Neuroscience.

[34]  J. Haller,et al.  Acute effects of glucocorticoids: behavioral and pharmacological perspectives , 1998, Neuroscience & Biobehavioral Reviews.

[35]  C. Wellman,et al.  Dendritic reorganization in pyramidal neurons in medial prefrontal cortex after chronic corticosterone administration. , 2001, Journal of neurobiology.

[36]  E. Vinogradova,et al.  Agonistic behavior during stress prevents the development of learned helplessness in rats , 1998, Neuroscience and Behavioral Physiology.

[37]  S. Chattarji,et al.  Modulation of different states of anxiety-like behavior by chronic stress. , 2004, Behavioral neuroscience.

[38]  M. Seligman,et al.  Learned helplessness in the rat: time course, immunization, and reversibility. , 1975, Journal of comparative and physiological psychology.

[39]  W. Korzan,et al.  Behavioral and neuroendocrine correlates of displaced aggression in trout , 2004, Hormones and Behavior.

[40]  Susan C. Cook,et al.  Chronic stress alters dendritic morphology in rat medial prefrontal cortex. , 2004, Journal of neurobiology.

[41]  C. Sandi,et al.  Prior exposure to a single stress session facilitates subsequent contextual fear conditioning in rats Evidence for a role of corticosterone , 2003, Hormones and Behavior.

[42]  Greg D. Gale,et al.  Hippocampus and contextual fear conditioning: Recent controversies and advances , 2001, Hippocampus.

[43]  Joseph E LeDoux,et al.  Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy. , 1999, Behavioral neuroscience.

[44]  Joseph E LeDoux,et al.  Corticosterone Potentiation of Conditioned Fear in Rats a , 1994, Annals of the New York Academy of Sciences.

[45]  S. Chattarji,et al.  Chronic Stress Induces Contrasting Patterns of Dendritic Remodeling in Hippocampal and Amygdaloid Neurons , 2002, The Journal of Neuroscience.

[46]  L. Eroǧlu,et al.  L-NAME prevents anxiety-like and depression-like behavior in rats exposed to restraint stress. , 2006, Methods and findings in experimental and clinical pharmacology.

[47]  S. Maier,et al.  Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus , 2005, Nature Neuroscience.