Role of brain norepinephrine in the behavioral response to stress

Morilak, David A.; Barrera, Gabe; Echevarria, David J.; Garcia, April S.; Hernandez, Angelica; Ma, Shuaike; Petre, Corina O.

doi:10.1016/j.pnpbp.2005.08.007

Cited by 570Stress Responses and CortisolNeurotransmitter Receptor Influence on BehaviorNeuroscience and Neuropharmacology Research

Role of brain norepinephrine in the behavioral response to stress

Morilak, David A., Barrera, Gabe, Echevarria, David J., Garcia, April S., Hernandez, Angelica, Ma, Shuaike, Petre, Corina O.·2005·Progress in Neuro-Psychopharmacology and Biological Psychiatry

DOI 10.1016/j.pnpbp.2005.08.007

Open this paper in CoChat — free account

Abstract

The brain noradrenergic system is activated by acute stress. The post-synaptic effects of norepinephrine (NE), exerted at a cellular or neural circuit level, have been described as modulatory in nature, as NE facilitates responses evoked in target cells by both excitatory and inhibitory afferent input. Over the past few years, we have undertaken a series of studies to understand how these cellular modulatory effects of NE, elicited by acute stress, might translate into modulation of the behavioral-affective components of the whole-animal response to stress. Using microdialysis, we have demonstrated that acute immobilization stress activates NE release in a number of stress-related limbic forebrain target regions, such as the central and medial amygdala, lateral bed nucleus of the stria terminalis, medial prefrontal cortex, and lateral septum. Using microinjections of adrenergic antagonist drugs directly into these regions, we have shown that this stress-induced release of NE facilitates a number of anxiety-like behavioral responses that are mediated in these regions, including stress-induced reduction of open-arm exploration on the elevated plus-maze, stress-induced reduction of social interaction behavior, and activation of defensive burying behavior by contact with an electrified probe. Dysregulation of the brain noradrenergic system may be a factor in determining vulnerability to stress-related pathology, or in the interaction of genetic vulnerability and environmental sensitization. Compared to outbred Sprague-Dawley rats, we have shown that the modulatory effect of NE is deficient in Wistar-Kyoto rats, which also exhibit attenuated behavioral reactivity to acute stress, as well as increased vulnerability to stress-induced gastric ulcers and exaggerated activation of the hypothalamic-pituitary-adrenal (HPA) stress axis. Further, repeated exposure to mild intermittent cold stress resulted in a much greater sensitization of both the brain noradrenergic system and the HPA axis in Wistar-Kyoto rats compared to Sprague-Dawley rats. The recruitment of a robust noradrenergic facilitatory influence following repeated cold exposure in this previously deficient strain resulted in an aberrant HPA response, which may be illustrative of the kinds of neurobiological changes that may contribute to the development of stress-related neuropsychiatric disorders such as depression, post-traumatic stress disorder, or other anxiety disorders in predisposed or susceptible individuals. On the other side of the same issue, regulatory alterations in noradrenergic neurotransmission, or in the stress-modulatory functions of NE, may be important in the behavioral effects of chronic antidepressant drug treatment. We present recent preliminary results addressing the effects of chronic treatment with the selective NE reuptake inhibitor, desipramine, on acute behavioral reactivity to stress. A better understanding of the role of NE in adaptive responses to acute stress, the pathological consequences of prolonged, repeated or severe stress, and the mechanisms of action of drugs used to treat stress-related diseases, may contribute to the future development of more effective strategies for the treatment or even prevention of such disorders.

Integrity signals

Registry

Crossref · 10.1016/j.pnpbp.2005.08.007

Cites

56 of 56 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Neurotransmitters including norepinephrine, serotonin and glutamate, as well as stress-induced release of neuropeptides and steroids, can influence synapse number and function.
“Neurotransmitters, including norepinephrine,76, 77, 78 serotonin79, 80, 81 and glutamate,82,83 as well as stress-induced release of neuropeptides26,34,84,85 and steroids,86, 87, 88 can influence synapse number and function.”
From Preferential loss of dorsal-hippocampus synapses underlies memory impairments provoked by short, multimodal stress (2014) · cites this paper as [78]

Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat
Pellow, S., Chopin, P., File, S. E., & Briley, M. (1985) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(85)90031-7 · Cited by 5,822 · see citing works
Psychopharmacology: The Fourth Generation of Progress
Bloom, F. E., & Kupfer, D. J. (1995) · Medical Entomology and Zoology · Cited by 2,985 · see citing works
Neurocircuitry of stress: central control of the hypothalamo–pituitary–adrenocortical axis
Herman, J. P., & Cullinan, W. E. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)10069-2 · Cited by 2,270 · see citing works
Psychopharmacology: The Fourth Generation of Progress
Brophy, J. J. (1995) · JAMA · doi:10.1001/jama.1995.03530220079046 · Cited by 1,582 · see citing works
Role of locus coeruleus in attention and behavioral flexibility
Aston-Jones, G., Rajkowski, J., & Cohen, J. (1999) · Biological Psychiatry · doi:10.1016/s0006-3223(99)00140-7 · Cited by 900 · see citing works
Mechanisms of stress: a dynamic overview of hormonal and behavioral homeostasis.
Johnson, E. O., Kamilaris, T., Chrousos, G., & Gold, P. (1992) · Neuroscience and Biobehavioral Reviews · doi:10.1016/s0149-7634(05)80175-7 · Cited by 900 · see citing works
Discharge of noradrenergic locus coeruleus neurons in behaving rats and monkeys suggests a role in vigilance
Aston‐Jones, G., Chiang, C., & Alexinsky, T. (1991) · Progress in brain research · doi:10.1016/s0079-6123(08)63830-3 · Cited by 589 · see citing works
Abnormal Noradrenergic Function in Posttraumatic Stress Disorder
Southwick, S. M. (1993) · Archives of General Psychiatry · doi:10.1001/archpsyc.1993.01820160036003 · Cited by 561 · see citing works
Neuroanatomical basis for facilitation of hypothalamic-pituitary-adrenal responses to a novel stressor after chronic stress
Bhatnagar, S., & Dallman, M. (1998) · Neuroscience · doi:10.1016/s0306-4522(97)00577-0 · Cited by 511 · see citing works
Conditioned defensive burying: A new paradigm for the study of anxiolytic agents
Treit, D., Pinel, J. P. J., & Fibiger, H. C. (1981) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(81)90219-7 · Cited by 420 · see citing works
Locus coeruleus and regulation of behavioral flexibility and attention
(2000) · Progress in Brain Research · doi:10.1016/s0079-6123(00)26013-5 · Cited by 400 · see citing works
Stress-Induced Norepinephrine Release in the Hypothalamic Paraventricular Nucleus and Pituitary-Adrenocortical and Sympathoadrenal Activity: In Vivo Microdialysis Studies
Pacák, K., Palkovits, M., Kopin, I. J., & Goldstein, D. S. (1995) · Frontiers in Neuroendocrinology · doi:10.1006/frne.1995.1004 · Cited by 395 · see citing works
Single-unit response of noradrenergic neurons in the locus coeruleus of freely moving cats. I. Acutely presented stressful and nonstressful stimuli
Abercrombie, E., & Jacobs, B. (1987) · The Journal of Neuroscience · doi:10.1523/jneurosci.07-09-02837.1987 · Cited by 377 · see citing works
Circuits and mechanisms governing hypothalamic responses to stress: a tale of two paradigms
Sawchenko, P. E., Li, H.-Y., & Ericsson, A. B. (2000) · Progress in brain research · doi:10.1016/s0079-6123(08)62131-7 · Cited by 353 · see citing works
Peripheral, autonomic regulation of locus coeruleus noradrenergic neurons in brain: putative implications for psychiatry and psychopharmacology
Svensson, T. H. (1987) · Psychopharmacology · doi:10.1007/bf00215471 · Cited by 334 · see citing works
Single unit activity of locus coeruleus neurons in the freely moving cat
Rasmussen, K., Morilak, D. A., & Jacobs, B. L. (1986) · Brain Research · doi:10.1016/0006-8993(86)90370-7 · Cited by 324 · see citing works
Self-citation
Neurobiological mechanisms of panic anxiety: biochemical and behavioral correlates of yohimbine-induced panic attacks
Charney, D. S., Woods, S. W., Goodman, W. K., & Heninger, G. R. (1987) · American Journal of Psychiatry · doi:10.1176/ajp.144.8.1030 · Cited by 301 · see citing works
The Endocrinology of Melancholic and Atypical Depression: Relation to Neurocircuitry and Somatic Consequences
Gold, P. W., & Chrousos, G. P. (1999) · Proceedings of the Association of American Physicians · doi:10.1046/j.1525-1381.1999.09423.x · Cited by 298 · see citing works
The Locus Coeruleus as a Site for Integrating Corticotropin‐Releasing Factor and Noradrenergic Mediation of Stress Responsesa
Valentino, R. J., Foote, S. L., & Page, M. E. (1993) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1993.tb49931.x · Cited by 292 · see citing works
Open field, learned helplessness, conditioned defensive burying, and forced-swim tests in WKY rats
Paré, W. P. (1994) · Physiology & Behavior · doi:10.1016/0031-9384(94)90097-3 · Cited by 264 · see citing works
The noradrenergic system in pathological anxiety: a focus on panic with relevance to generalized anxiety and phobias.
Sullivan, G., Coplan, J., Kent, J., & Gorman, J. (1999) · Biological Psychiatry · doi:10.1016/s0006-3223(99)00246-2 · Cited by 245 · see citing works
Modulatory effects of norepinephrine in the lateral bed nucleus of the stria terminalis on behavioral and neuroendocrine responses to acute stress.
Cecchi, M., Khoshbouei, H., Javors, M., & Morilak, D. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00062-3 · Cited by 243 · see citing works
Self-citation
Prior exposure to chronic stress results in enhanced synthesis and release of hippocampal norepinephrine in response to a novel stressor
Nisenbaum, L., Zigmond, M., Sved, A., & Abercrombie, E. (1991) · Journal of Neuroscience · doi:10.1523/jneurosci.11-05-01478.1991 · Cited by 238 · see citing works
Stress reactivity of the brain noradrenergic system in three rat strains differing in their neuroendocrine and behavioral responses to stress: implications for susceptibility to stress-related neuropsychiatric disorders.
Pardon, M.-C., Gould, G., Garcia, A., Phillips, L., Cook, M. C., Miller, S. A., Mason, P. A., & Morilak, D. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00364-0 · Cited by 218 · see citing works
Self-citation
Modulation of rat cortical area 17 neuronal responses to moving visual stimuli during norepinephrine and serotonin microiontophoresis
Waterhouse, B. D., Azizi, S. A., Burne, R. A., & Woodward, D. J. (1990) · Brain Research · doi:10.1016/0006-8993(90)91422-d · Cited by 194 · see citing works
Depressive behavior and stress ulcer in Wistar Kyoto rats
Paré, W. P., & Redei, E. E. (1993) · Journal of Physiology-Paris · doi:10.1016/0928-4257(93)90010-q · Cited by 150 · see citing works
Defining stress as a prelude to mapping its neurocircuitry: No help from allostasis
Day, T. A. (2005) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2005.08.005 · Cited by 147 · see citing works
Modulatory effects of norepinephrine, acting on alpha1 receptors in the central nucleus of the amygdala, on behavioral and neuroendocrine responses to acute immobilization stress
Cecchi, M., Khoshbouei, H., & Morilak, D. A. (2002) · Neuropharmacology · doi:10.1016/s0028-3908(02)00292-7 · Cited by 147 · see citing works
Self-citation
Reboxetine, a Selective Norepinephrine Reuptake Inhibitor, Is an Effective and Well-Tolerated Treatment for Panic Disorder
Versiani, M., Cassano, G. B., Perugi, G., Benedetti, A., Mastalli, L., Nardi, A. E., & Savino, M. (2002) · The Journal of Clinical Psychiatry · doi:10.4088/jcp.v63n0107 · Cited by 140 · see citing works
Activation of Locus Coeruleus Enhances the Responses of Olfactory Bulb Mitral Cells to Weak Olfactory Nerve Input
Jiang, M., Griff, E. R., Ennis, M. J., Zimmer, L. A., & Shipley, M. T. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-19-06319.1996 · Cited by 135 · see citing works
Behavioral reactivity to stress
Khoshbouei, H., Cecchi, M., Dove, S., Javors, M. A., & Morilak, D. A. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(01)00683-9 · Cited by 130 · see citing works
Self-citation
A review of the efficacy of serotonergic and noradrenergic reuptake inhibitors for treatment of major depression
Nelson, J. C. (1999) · Biological Psychiatry · doi:10.1016/s0006-3223(99)00173-0 · Cited by 125 · see citing works
Norepinephrine Release in Medial Amygdala Facilitates Activation of the Hypothalamic‐Pituitary‐Adrenal Axis in Response to Acute Immobilisation Stress
Ma, S., & Morilak, D. A. (2005) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2005.01279.x · Cited by 111 · see citing works
Self-citation
Effects of physiological manipulations on locus coeruleus neuronal activity in freely moving cats. II. Cardiovascular challenge.
Morilak, D., Fornal, C., & Jacobs, B. (1987) · Brain Research · doi:10.1016/0006-8993(87)90536-1 · Cited by 104 · see citing works
Self-citation
Strain differences in hypothalamic-pituitary-adrenal activity and stress ulcer
Redei, E., Paré, W. P., Aird, F., & Kluczynski, J. (1994) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1994.266.2.r353 · Cited by 102 · see citing works
Effects of physiological manipulations on locus coeruleus neuronal activity in freely moving cats. I. Thermoregulatory challenge
Morilak, D. A., Fornal, C. A., & Jacobs, B. L. (1987) · Brain Research · doi:10.1016/0006-8993(87)90535-x · Cited by 102 · see citing works
Self-citation
The treatment of postpartum depression: minimizing infant exposures.
Newport, D. J., Hostetter, A. L., Arnold, A., & Stowe, Z. N. (2002) · PubMed · Cited by 98 · see citing works
Chronic cold stress sensitizes brain noradrenergic reactivity and noradrenergic facilitation of the HPA stress response in Wistar Kyoto rats
Pardon, M., Ma, S., & Morilak, D. A. (2003) · Brain Research · doi:10.1016/s0006-8993(03)02355-2 · Cited by 97 · see citing works
Self-citation
Bladder distention activates noradrenergic locus coeruleus neurons by an excitatory amino acid mechanism
Page, M. E., Akaoka, H., Aston‐Jones, G., & Valentino, R. J. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90295-d · Cited by 92 · see citing works
The physiological role of α-adrenoceptors in the CNS: new concepts from single-cell studies
Aghajanian, G. K., & Rogawski, M. A. (1983) · Trends in Pharmacological Sciences · doi:10.1016/0165-6147(83)90417-0 · Cited by 89 · see citing works
Opposing roles for medial and central amygdala in the initiation of noradrenergic cell responses to a psychological stressor
Dayas, C. V., & Day, T. A. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2001.02011.x · Cited by 80 · see citing works
Animal models of different anxiety states.
File, S. E. (1995) · PubMed · Cited by 76 · see citing works
Single-unit and physiological analyses of brain norepinephrine function in behaving animals.
Jacobs, B. L., Abercrombie, E., Fornal, C., Levine, E., Morilak, D. A., & Stafford, I. (1991) · Progress in Brain Research · doi:10.1016/s0079-6123(08)63805-4 · Cited by 70 · see citing works
Self-citation
Noradrenergic modulation of sensorimotor processes in intact rats: the masseteric reflex as a model system
Morilak, D. A., & Jacobs, B. (1985) · Journal of Neuroscience · doi:10.1523/jneurosci.05-05-01300.1985 · Cited by 70 · see citing works
Self-citation
Chronic cold stress alters the basal and evoked electrophysiological activity of rat locus coeruleus neurons
Mana, M. J., & Grace, A. A. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00225-x · Cited by 66 · see citing works
Sensitization of norepinephrine release in medial prefrontal cortex: effect of different chronic stress protocols
Jedema, H. P., Sved, A. F., Zigmond, M. J., & Finlay, J. M. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01369-4 · Cited by 65 · see citing works
Effects of physiological manipulations on locus coeruleus neuronal activity in freely moving cats. III. Glucoregulatory challenge.
Morilak, D., Fornal, C., & Jacobs, B. (1987) · Brain Research · doi:10.1016/0006-8993(87)90537-3 · Cited by 62 · see citing works
Self-citation
Induction of FOS expression by acute immobilization stress is reduced in locus coeruleus and medial amygdala of Wistar–Kyoto rats compared to Sprague–Dawley rats
Ma, S., & Morilak, D. A. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2003.12.028 · Cited by 59 · see citing works
Self-citation
Noradrenergic modulation of the masseteric reflex in behaving cats. II. Physiological studies
Stafford, I., & Jacobs, B. L. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-01-00099.1990 · Cited by 56 · see citing works
The cerebellar norepinephrine system: inhibition, modulation, and gating
Woodward, D. J., Moises, H. C., Waterhouse, B. D., Yeh, H. H., & Cheun, J. E. (1991) · Progress in brain research · doi:10.1016/s0079-6123(08)63820-0 · Cited by 55 · see citing works
Modulatory Actions of Norepinephrine on Neural Circuits
Woodward, D. J., Moises, H. C., Waterhouse, B. D., Yeh, H. H., & Cheun, J. E. (1991) · Advances in experimental medicine and biology · doi:10.1007/978-1-4684-5907-4_16 · Cited by 54 · see citing works
Effects of reboxetine on Hamilton Depression Rating Scale factors from randomized, placebo-controlled trials in major depression
Ferguson, J. M., MENDELS, J., & Schwartz, G. E. (2002) · International Clinical Psychopharmacology · doi:10.1097/00004850-200203000-00001 · Cited by 39 · see citing works
Autoreceptor‐mediated inhibition of norepinephrine release in rat medial prefrontal cortex is maintained after chronic desipramine treatment
Garcia, A. S., Barrera, G., Burke, T. F., Ma, S., Hensler, J. G., & Morilak, D. A. (2004) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2004.02748.x · Cited by 35 · see citing works
Self-citation
Selected Models of Anxiety, Depression and Psychosis
Simon, P., Soubrié, P., & Widlöcher, D. (1988) · KARGER eBooks · doi:10.1159/isbn.978-3-8055-4667-6 · Cited by 32 · see citing works
Noradrenergic modulation of the masseteric reflex in behaving cats. I. Pharmacological studies
Stafford, I., & Jacobs, B. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-01-00091.1990 · Cited by 17 · see citing works
P.2.16 Noradrenergic facilitation of shock-probe defensive burying in lateral septum
Petre, C. O., Barrera, G., & Morilak, D. A. (2005) · European Neuropsychopharmacology · doi:10.1016/s0924-977x(05)80156-7 · Cited by 6 · see citing works
Self-citation

Flagged first, then by citations

Sorted by citations

The neurobiology of stress and development.
Gunnar, M., & Quevedo, K. (2007) · Annual Review of Psychology · doi:10.1146/annurev.psych.58.110405.085605 · Cited by 2,011 · see citing works
The neuro-symphony of stress
Joëls, M., & Baram, T. Z. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2632 · Cited by 1,521 · see citing works
Effects of the probiotic Bifidobacterium infantis in the maternal separation model of depression
Desbonnet, L., Garrett, L., Clarke, G., Kiely, B., Cryan, J. F., & Dinan, T. G. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.08.005 · Cited by 999 · see citing works
Acute psychological stress reduces working memory-related activity in the dorsolateral prefrontal cortex
Qin, S., Hermans, E. J., van Marle, H. J. F., Luo, J., & Fernández, G. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.03.006 · Cited by 675 · see citing works
Dynorphin, stress, and depression
Knoll, A. T., & Carlezon, W. A. (2010) · Brain Research · doi:10.1016/j.brainres.2009.09.074 · Cited by 465 · see citing works
Chronic stress: Implications for neuronal morphology, function and neurogenesis
Joëls, M., Karst, H., Krugers, H. J., & Lucassen, P. J. (2007) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2007.04.001 · Cited by 381 · see citing works
Campylobacter jejuni infection increases anxiety-like behavior in the holeboard: possible anatomical substrates for viscerosensory modulation of exploratory behavior
Goehler, L. E., Park, S. M., Opitz, N., Lyte, M., & Gaykema, R. P. A. (2008) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2007.08.009 · Cited by 287 · see citing works
Noradrenergic transmission in the extended amygdala: role in increased drug-seeking and relapse during protracted drug abstinence
Smith, R. J., & Aston-Jones, G. (2008) · Brain Structure and Function · doi:10.1007/s00429-008-0191-3 · Cited by 206 · see citing works
Glucocorticoids, chronic stress, and obesity
Dallman, M. F., Pecoraro, N. C., La Fleur, S. E., Warne, J. P., Ginsberg, A. B., Akana, S. F., Laugero, K. C., Houshyar, H., Strack, A. M., Bhatnagar, S., et al. (2006) · Progress in Brain Research · doi:10.1016/s0079-6123(06)53004-3 · Cited by 198 · see citing works
Prefrontal cortex executive processes affected by stress in health and disease
Girotti, M., Adler, S. M., Bulin, S. E., Fucich, E. A., Paredes, D., & Morilak, D. A. (2018) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.07.004 · Cited by 176 · see citing works
Self-citation
Gut Vagal Afferents Differentially Modulate Innate Anxiety and Learned Fear
Klarer, M., Arnold, M., Günther, L., Winter, C., Langhans, W., & Meyer, U. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.0252-14.2014 · Cited by 159 · see citing works
Chronic intermittent cold stress and serotonin depletion induce deficits of reversal learning in an attentional set-shifting test in rats
Lapiz-Bluhm, M. D. S., Soto-Piña, A. E., Hensler, J. G., & Morilak, D. A. (2009) · Psychopharmacology · doi:10.1007/s00213-008-1224-6 · Cited by 163 · see citing works
Self-citation
Neurobiology of dysregulated motivational systems in drug addiction
Edwards, S., & Koob, G. F. (2010) · Future Neurology · doi:10.2217/fnl.10.14 · Cited by 157 · see citing works
Different stressors produce excitation or inhibition of mesolimbic dopamine neuron activity: response alteration by stress pre‐exposure
Valenti, O., Gill, K. M., & Grace, A. A. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08038.x · Cited by 131 · see citing works
Prenatal stress induces long term stress vulnerability, compromising stress response systems in the brain and impairing extinction of conditioned fear after adult stress
Green, M. K., Rani, C. S. S., Joshi, A., Soto-Piña, A. E., Martinez, P. A., Frazer, A., Strong, R., & Morilak, D. A. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.06.041 · Cited by 124 · see citing works
Self-citation
REM Sleep Rebound as an Adaptive Response to Stressful Situations
Suchecki, D., Tiba, P. A., & Machado, R. B. (2012) · Frontiers in Neurology · doi:10.3389/fneur.2012.00041 · Cited by 119 · see citing works
Neurobiological correlates of social functioning in autism
Neuhaus, E., Beauchaine, T. P., & Bernier, R. (2010) · Clinical Psychology Review · doi:10.1016/j.cpr.2010.05.007 · Cited by 122 · see citing works
Preferential loss of dorsal-hippocampus synapses underlies memory impairments provoked by short, multimodal stress
Maras, P. M., Molet, J., Chen, Y., Rice, C., Ji, S. G., Solodkin, A., & Baram, T. Z. (2014) · Molecular Psychiatry · doi:10.1038/mp.2014.12 · Cited by 118 · see citing works
Evaluation of the Wistar-Kyoto rat model of depression and the role of synaptic plasticity in depression and antidepressant response
Aleksandrova, L. R., Wang, Y. T., & Phillips, A. G. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.07.007 · Cited by 114 · see citing works
Real-world stress resilience is associated with the responsivity of the locus coeruleus
Grueschow, M., Stenz, N., Thörn, H., Ehlert, U., Breckwoldt, J., Brodmann Maeder, M., Exadaktylos, A. K., Bingisser, R., Ruff, C. C., & Kleim, B. (2021) · Nature Communications · doi:10.1038/s41467-021-22509-1 · Cited by 116 · see citing works
Chronic treatment with desipramine improves cognitive performance of rats in an attentional set-shifting test
Lapiz, M. D. S., Bondi, C. O., & Morilak, D. A. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301235 · Cited by 95 · see citing works
Self-citation
Recent Progress in Understanding the Pathophysiology of Post-Traumatic Stress Disorder: Implications for Targeted Pharmacological Treatment
Bailey, C. R., Cordell, E., Sobin, S. M., & Neumeister, A. (2013) · CNS Drugs · doi:10.1007/s40263-013-0051-4 · Cited by 89 · see citing works
Beneficial effects of desipramine on cognitive function of chronically stressed rats are mediated by α1-adrenergic receptors in medial prefrontal cortex
Bondi, C. O., Jett, J. D., & Morilak, D. A. (2010) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2010.04.016 · Cited by 88 · see citing works
Self-citation
Maternal attenuation of hypothalamic paraventricular nucleus norepinephrine switches avoidance learning to preference learning in preweanling rat pups
Shionoya, K., Moriceau, S., Bradstock, P., & Sullivan, R. M. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.06.004 · Cited by 85 · see citing works
Noradrenergic facilitation of shock-probe defensive burying in lateral septum of rats, and modulation by chronic treatment with desipramine
Bondi, C. O., Barrera, G., Lapiz, M. D. S., Bedard, T., Mahan, A., & Morilak, D. A. (2007) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2006.11.015 · Cited by 56 · see citing works
Self-citation
Repeated Stressor Exposure Regionally Enhances Beta-Adrenergic Receptor-Mediated Brain IL-1β Production
Porterfield, V. M., Gabella, K. M., Simmons, M. A., & Johnson, J. D. (2012) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2012.08.001 · Cited by 42 · see citing works
Too Much of a Good Thing: Blocking Noradrenergic Facilitation in Medial Prefrontal Cortex Prevents the Detrimental Effects of Chronic Stress on Cognition
Jett, J. D., & Morilak, D. A. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2012.216 · Cited by 41 · see citing works
Self-citation
Sleep allostasis in chronic sleep restriction: The role of the norepinephrine system
Kim, Y., Chen, L., McCarley, R. W., & Strecker, R. E. (2013) · Brain Research · doi:10.1016/j.brainres.2013.07.048 · Cited by 34 · see citing works
Sex Differences in the Regulation of Brain IL-1β in Response to Chronic Stress
Barnard, D. F., Gabella, K. M., Kulp, A. C., Parker, A. D., Dugan, P. B., & Johnson, J. D. (2019) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2019.01.026 · Cited by 35 · see citing works
Selective preservation of MeCP2 in catecholaminergic cells is sufficient to improve the behavioral phenotype of male and female Mecp2-deficient mice
Lang, M., Wither, R. G., Brotchie, J. M., Wu, C., Zhang, L., & Eubanks, J. H. (2013) · Human Molecular Genetics · doi:10.1093/hmg/dds433 · Cited by 30 · see citing works
Tyrosine ameliorates heat induced delay in event related potential P300 and contingent negative variation
Kishore, K., Ray, K., Anand, J. P., Thakur, L., Kumar, S., & Panjwani, U. (2013) · Brain and Cognition · doi:10.1016/j.bandc.2013.09.005 · Cited by 19 · see citing works

Combination of Microdialysis and Glucose Sensor for Continuous On Line Measurement of the Subcutaneous Glucose Concentration: Theory and Practical Application
Meyerhoff, C., Mennel, F. J., Bischof, F., Sternberg, F., & Pfeiffer, E. F. (1994) · Hormone and Metabolic Research · doi:10.1055/s-2007-1001752 · Cited by 23 · see citing works
P1‐029: A comparison of conventional versus push‐pull microdialysis for the detection of amyloid β in the mouse brain
Motter, R. N., Veinbergs, I., Cremers, T. I. F. H., et al. (2011) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2011.05.309
Decreased activity of locus coeruleus neurons in the rat after DSP-4 treatment
Olpe, H. R., Laszlo, J., Dooley, D. J., Heid, J., & Steinmann, M. (1983) · Neuroscience Letters · doi:10.1016/0304-3940(83)90096-4 · Cited by 29 · see citing works
Exposure to hot and cold environments increases noradrenaline release in the bed nucleus of the stria terminalis in rats
Minami, S., Nomura, H., & Minami, M. (2018) · Neuropsychopharmacology Reports · doi:10.1002/npr2.12036 · Cited by 7 · see citing works
Biochemical evidence for simultaneous activation of multiple locus coeruleus efferents
Crawley, J. N., Maas, J. W., & Roth, R. H. (1980) · Life Sciences · doi:10.1016/0024-3205(80)90039-9 · Cited by 39 · see citing works

Authors: Morilak, D. A., Barrera, G., Echevarria, D. J., Garcia, A. S., Hernandez, A., Ma, S., & Petre, C. O.
Affiliations: The University of Texas at San Antonio Health Science Center (US)
Corresponding author: Morilak, David A.
ORCID: Morilak, David A.
Venue: Progress in Neuro-Psychopharmacology and Biological Psychiatry
Publisher: Elsevier BV
Published: 2005-12
Volume: 29
Issue: 8
Pages: 1214-1224
ISSN: 0278-5846 (ISSN-L)
DOI: 10.1016/j.pnpbp.2005.08.007
OpenAlex: W2019284117
Cited by: 570
References: 56
Citations by year: 2026: 16 · 2025: 19 · 2024: 17 · 2023: 16 · 2022: 29 · 2021: 27 · 2020: 21 · 2019: 33 · 2018: 23 · 2017: 25 · 2016: 30 · 2015: 37 · 2014: 36 · 2013: 39 · 2012: 34
FWCI: 1.36
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Progress in Neuro-Psychopharmacology and Biological Psychiatry (publishedVersion)
PubMed (publishedVersion)
Funders: U.S. Department of Defense
National Institutes of Health (5r01mh060118-05)
University of Texas Health Science Center at San Antonio
National Institute of Mental Health (MH 60118, MH 53851)
Topics: Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: norepinephrine, noradrenergic system, acute stress, restraint stress, anxiety-like behavior, hypothalamic-pituitary-adrenal axis, stress sensitization, cold stress, Wistar-Kyoto rats, Sprague-Dawley rats, amygdala, bed nucleus of the stria terminalis, medial prefrontal cortex, lateral septum, adrenergic antagonists, stress-induced gastric ulcer
MeSH terms: Animals, Anxiety, Behavior, Behavior, Animal, Brain Chemistry, Environment, Humans, Synaptic Transmission, Norepinephrine, Stress, Psychological

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Role of brain norepinephrine in the behavioral response to stress

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks