Cited by 377Stress Responses and CortisolNeurotransmitter Receptor Influence on BehaviorNeuroscience of respiration and sleep

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Single-unit response of noradrenergic neurons in the locus coeruleus of freely moving cats. I. Acutely presented stressful and nonstressful stimuli

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Abercrombie, ED, Jacobs, BL·1987·The Journal of Neuroscience

DOI 10.1523/jneurosci.07-09-02837.1987PMC PMC6569145

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Abstract

The present experiment was designed to explore the stress-relatedness of activity in noradrenergic neurons of the locus coeruleus (LC) of behaving cats. A stressor was defined as a stimulus that elicited a significant sympathoadrenal activation as measured by plasma norepinephrine level and heart rate. According to this definition, exposure to 15 min of 100 dB white noise or 15 min of restraint was stressful in cats. In contrast, exposure to inaccessible rats for 15 min was behaviorally activating but nonstressful. The single-unit activity of noradrenergic neurons in the LC of behaving cats was examined under these conditions. The stressful stimuli elicited a significant increase in LC neuronal activity for the entire 15 min stressor duration, whereas the behaviorally activating but nonstressful stimulus elicited no significant change in the activity of these neurons. These results provide evidence that behavioral activation per se is not sufficient to evoke a tonic activation of these neurons. Rather, these data support the hypothesis that the LC is involved in the CNS response to stress and provide additional evidence that the activity of LC noradrenergic neurons increases in association with sympathoadrenal activation.

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Nonrepinephrine-containing locus coeruleus neurons in behaving rats exhibit pronounced responses to non-noxious environmental stimuli
Aston‐Jones, G., & Bloom, F. E. (1981) · Journal of Neuroscience · doi:10.1523/jneurosci.01-08-00887.1981 · Cited by 1,072 · cited 1×
“These characteristics have been observed in LC neurons of both the behaving rat (Aston-Jones and Bloom, 1981a) and cat (Rasmussen et al., 1986).”
Background
Impulse activity of locus coeruleus neurons in awake rats and monkeys is a function of sensory stimulation and arousal
Foote, S. L., Aston-Jones, G., & Bloom, F. E. (1980) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.77.5.3033 · Cited by 857 · cited 2×
“…electrophysiological studies of LC neurons in unanesthetized animals have shown that these neurons are activated by a wide variety of environmental stimuli of many modalities (Foote and Bloom, 1979; Foote et al., 1980; Aston-Jones and Bloom, 198 lb; Rasmussen et al., 1986).”
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Raphe unit activity in freely moving cats: correlation with level of behavioral arousal.
Trulson, M., & Jacobs, B. (1979) · Brain Research · doi:10.1016/0006-8993(79)90157-4 · Cited by 815 · cited 1×
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THE EMERGENCY FUNCTION OF THE ADRENAL MEDULLA IN PAIN AND THE MAJOR EMOTIONS
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Monoamine cell distribution in the cat brain stem. A fluorescence histochemical study with quantification of indolaminergic and locus coeruleus cell groups
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Single unit activity of locus coeruleus neurons in the freely moving cat
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“These characteristics have been observed in LC neurons of both the behaving rat (Aston-Jones and Bloom, 1981a) and cat (Rasmussen et al., 1986).”
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Harro, J., & Oreland, L. (2001) · Brain Research Reviews · doi:10.1016/s0165-0173(01)00082-0 · Cited by 150
Dual Effects of d-Amphetamine on Dopamine Neurons Mediated by Dopamine and Nondopamine Receptors
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Sensitivity of Locus Ceruleus Neurons to Reward Value for Goal-Directed Actions
Bouret, S., & Richmond, B. J. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.4553-14.2015 · Cited by 163
“What process does LC activation subserve? Activation of LC neurons has long been associated with salient events and the associated orienting responses (Foote et al., 1980; Aston-Jones and Bloom, 1981; Abercrombie and Jacobs, 1987; Berridge and Waterhouse, 2003; Bouret and Richmond, 2009; Sara and Bouret, 2012).”
Background
Noradrenergic Modulation of Basolateral Amygdala Neuronal Activity: Opposing Influences of α-2 and β Receptor Activation
Buffalari, D., & Grace, A. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.2007-07.2007 · Cited by 157
“LC neurons are activated by stressful stimuli (Rasmussen et al., 1986; Abercrombie and Jacobs, 1987; Grant et al., 1988; Aston-Jones et al., 1991), and presumably mediate the stress-induced increase in NE in the BLA.”
Background
Central noradrenergic neurones and stress
Stanford, S. C. (1995) · Pharmacology & Therapeutics · doi:10.1016/0163-7258(95)02010-1 · Cited by 152
Noradrenergic Innervation of the Dorsal Medial Prefrontal Cortex Modulates Hypothalamo-Pituitary-Adrenal Responses to Acute Emotional Stress
Radley, J. J., Williams, B., & Sawchenko, P. E. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0552-08.2008 · Cited by 148
“Electrophysiologic activity and immediate-early gene responses of LC neurons are enhanced by exposure to a variety of acute emotional stressors, as is NE release in mPFC (Abercrombie and Jacobs, 1987; Ceccatelli et al., 1989; Cullinan et al., 1995; Palkovits et al., 1997; Passerin et al., 2000).”
Background
Multiple immediate-early gene expression during physiological and endocrine adaptation to repeated stress
Stamp, J. A., & Herbert, J. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00368-1 · Cited by 145
Neurobiological factors in personality and depression
Depue, R. A. (1995) · European Journal of Personality · doi:10.1002/per.2410090509 · Cited by 145
A function for REM sleep: regulation of noradrenergic receptor sensitivity.
Siegel, J. M., & Rogawski, M. A. (1988) · Brain Research · doi:10.1016/0165-0173(88)90007-0 · Cited by 151
Corticosterone-Sensitive Monoamine Transport in the Rat Dorsomedial Hypothalamus: Potential Role for Organic Cation Transporter 3 in Stress-Induced Modulation of Monoaminergic Neurotransmission
Gasser, P., Lowry, C., & Orchinik, M. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0570-06.2006 · Cited by 145
“Both of these groups of neurons are activated during stress (Abercrombie and Jacobs, 1987; Daugherty et al., 2001) and are proposed to contribute to the regulation of stress responses (Graeff et al.”
Background
Neuropeptide and small transmitter coexistence: Fundamental studies and relevance to mental illness
Hökfelt, T., Barde, S., Xu, Z.-Q. D., Kuteeva, E., Rüegg, J., Le Maitre, E., Risling, M., Kehr, J., Ihnatko, R., Theodorsson, E., et al. (2018) · Frontiers in Neural Circuits · doi:10.3389/fncir.2018.00106 · Cited by 139
“…the LC: stress increases NA turnover, as well as tyrosine hydroxylase activity and transcription in the LC (Korf et al., 1973; Zigmond et al., 1974; Abercrombie and Jacobs, 1987; Komori et al., 1990; Smith et al., 1991; Melia et al., 1992; Aston-Jones et al., 1996; Rusnak et al., 1998; Chang et…”
Background
Locus coeruleus activation by colon distention: role of corticotropin-releasing factor and excitatory amino acids
Lechner, S. M., Curtis, A. L., Brons, R., & Valentino, R. J. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00116-9 · Cited by 137
Behavioral and autonomic responses to intermittent social stress: differential protection by clonidine and metoprolol
Tornatzky, W., & Miczek, K. A. (1994) · Psychopharmacology · doi:10.1007/bf02245339 · Cited by 168
Adrenergic and noradrenergic innervation of the midbrain ventral tegmental area and retrorubral field: Prominent inputs from medullary homeostatic centers
Mejias-Aponte, C., Drouin, C., & Aston-Jones, G. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.4632-08.2009 · Cited by 137
“Physiological stressors such as cardiovascular, osmotic and immune challenges, as well as psychological stressors including restraint and intermittent footshock, activate these adrenergic cells (Abercrombie and Jacobs, 1987; Morilak et al., 1987; Sawchenko et al., 2000).”
Background
Partial injury to central noradrenergic neurons: reduction of tissue norepinephrine content is greater than reduction of extracellular norepinephrine measured by microdialysis
Abercrombie, E. D., & Zigmond, M. J. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-11-04062.1989 · Cited by 125
Self-citation
Early Life Trauma and Attachment: Immediate and Enduring Effects on Neurobehavioral and Stress Axis Development
Rincón‐Cortés, M., & Sullivan, R. M. (2014) · Frontiers in Endocrinology · doi:10.3389/fendo.2014.00033 · Cited by 147
Repeated Immobilization Stress Alters Tyrosine Hydroxylase, Corticotropin‐Releasing Hormone and Corticosteroid Receptor Messenger Ribonucleic Acid Levels in Rat Brain
Mamalaki, E., Kvetnan̆ský, R., Brady, L., Gold, P., & Herkenham, M. (1992) · Journal of neuroendocrinology · doi:10.1111/j.1365-2826.1992.tb00220.x · Cited by 131
From Malthus to motive: How the HPA axis engineers the phenotype, yoking needs to wants
Pecoraro, N. C., Dallman, M. F., Warne, J. P., Ginsberg, A. B., Laugero, K. D., la Fleur, S. E., Houshyar, H., Gómez-Oliver, F., Bhargava, A., & Akana, S. F. (2006) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2006.07.004 · Cited by 125
Adrenergic receptors mediate changes in c-fos mRNA levels in brain
Gubits, R. M., Smith, T. M., Fairhurst, J. L., & Yu, H. H. (1989) · Molecular Brain Research · doi:10.1016/0169-328x(89)90026-0 · Cited by 126
Role of the basolateral amygdala in memory consolidation
Paré, D. (2003) · Progress in Neurobiology · doi:10.1016/s0301-0082(03)00104-7 · Cited by 296
“Abundant evidence indicates that the discharge rate of locus coeruleus neurons increases during stress (Abercrombie and Jacobs, 1987a,b).”
Background
Antagonism of endogenous CRH systems attenuates stress-induced freezing behavior in rats
Kalin, N. H., Sherman, J. E., & Takahashi, L. K. (1988) · Brain Research · doi:10.1016/0006-8993(88)90064-9 · Cited by 122
Maternal and child posttraumatic stress disorder in cases of child maltreatment
Famularo, R., Fenton, T., Kinscherff, R. T., AYOUB, C. C., & Barnum, R. (1994) · Child Abuse & Neglect · doi:10.1016/0145-2134(94)90093-0 · Cited by 117
Human amygdala reactivity is diminished by the β-noradrenergic antagonist propranolol
Hurlemann, R., Walter, H., Rehme, A. K., Kukolja, J., Santoro, S. C., Schmidt, C., Schnell, K., Mußhoff, F., Keysers, C., Maier, W., et al. (2010) · Psychological Medicine · doi:10.1017/s0033291709992376 · Cited by 119
Effects of stress and adrenalectomy on tyrosine hydroxylase mRNA levels in the locus ceruleus by in situ hybridization.
Smith, M. A., Brady, L., Glowa, J., Gold, P., & Herkenham, M. (1991) · Brain Research · doi:10.1016/0006-8993(91)90881-u · Cited by 122
Differential Role of Galanin Receptors in the Regulation of Depression-Like Behavior and Monoamine/Stress-Related Genes at the Cell Body Level
Kuteeva, E., Wardi, T., Lundström, L., Sollenberg, U. E., Langel, Ü., Hökfelt, T. G. M., & Ögren, S. O. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301660 · Cited by 110
“In the DR, neither TPH2 nor galanin mRNA transcript levels were significantly affected by the swim/ injection stress, consistent with the view that the LC NA system is more sensitive to acute stress than the DR (Abercrombie and Jacobs, 1987; Wilkinson and Jacobs, 1988).”
Background
Comparison of Stress‐induced Changes in Noradrenergic and Serotonergic Neurons in the Rat Hippocampus Using Microdialysis
Vahabzadeh, A., & Fillenz, M. (1994) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1994.tb00619.x · Cited by 117
Effect of tyrosine on cognitive function and blood pressure under stress.
Deijen, J., & Orlebeke, J. F. (1994) · Brain Research Bulletin · doi:10.1016/0361-9230(94)90200-3 · Cited by 116
Involvement of melanocortin-4 receptor in anxiety and depression
Chaki, S., & Okuyama, S. (2005) · Peptides · doi:10.1016/j.peptides.2004.11.029 · Cited by 114
Tyrosine improves cognitive performance and reduces blood pressure in cadets after one week of a combat training course
Deijen, J. B., Wientjes, C. J. E., Vullinghs, H. F. M., Cloin, P. A., & Langefeld, J. J. (1999) · Brain Research Bulletin · doi:10.1016/s0361-9230(98)00163-4 · Cited by 110
“Noradrenergic projections from the locus coeruleus (LC), which show an increased electrical activity during stress, provide a main innervation to the frontal cortex [1,31].”
Background
Activity of cat locus coeruleus noradrenergic neurons during the defense reaction.
Levine, E., Litto, W., & Jacobs, B. (1990) · Brain Research · doi:10.1016/0006-8993(90)90773-5 · Cited by 113
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Predator stress engages corticotropin-releasing factor and opioid systems to alter the operating mode of locus coeruleus norepinephrine neurons
Curtis, A. L., Leiser, S. C., Snyder, K., & Valentino, R. J. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.11.020 · Cited by 120
“Because of technical limitations, fewer studies have recorded LC discharge during stress and most of these have examined the effect of physiological stressors on tonic (i.e., spontaneous), but not phasic LC activity (Abercrombie and Jacobs, 1987; Curtis et al., 1993; Morilak et al., 1987a, b).”
Background
Noradrenergic enhancement of amygdala responses to fear
Onur, O. A., Walter, H., Schlaepfer, T. E., Rehme, A. K., Schmidt, C., Keysers, C., Maier, W., & Hurlemann, R. (2009) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsn049 · Cited by 111
“Neurons in the LC are activated by stressful stimuli (Abercrombie and Jacobs, 1987) and mediate the stress-induced enhancement of NE neurotransmission in the BLA (Buffalari and Grace, 2007).”
Corticotropin-releasing factor in the locus coeruleus mediates EEG activation associated with hypotensive stress
Page, M. E., Berridge, C. W., Foote, S. L., & Valentino, R. J. (1993) · Neuroscience Letters · doi:10.1016/0304-3940(93)90862-f · Cited by 107
Corticotropin‐Releasing Factor Neurones of the Central Nucleus of the Amygdala Mediate Locus Coeruleus Activation by Cardiovascular Stress
Curtis, A., Bello, N. T., Connolly, K., & Valentino, R. (2002) · Journal of neuroendocrinology · doi:10.1046/j.1365-2826.2002.00821.x · Cited by 110
Corticotropin-releasing factor administered into the locus coeruleus, but not the parabrachial nucleus, stimulates norepinephrine release in the prefrontal cortex.
Smagin, G., Świergiel, A., & Dunn, A. (1995) · Brain Research Bulletin · doi:10.1016/0361-9230(94)00166-x · Cited by 110
Discrete local application of corticotropin-releasing factor increases locus coeruleus discharge and extracellular norepinephrine in rat hippocampus
Page, M. E., & Abercrombie, E. D. (1999) · Synapse · doi:10.1002/(sici)1098-2396(19990915)33:4 · Cited by 100
Self-citation
Dopamine and noradrenaline release in the prefrontal cortex in relation to unconditioned and conditioned stress and reward
Feenstra, M. G. P. (2000) · Progress in brain research · doi:10.1016/s0079-6123(00)26012-3 · Cited by 103
Region-Specific Regulation of RGS4 (Regulator of G-Protein–Signaling Protein Type 4) in Brain by Stress and Glucocorticoids: In Vivo and In VitroStudies
Ni, Y., Gold, S., Iredale, P., Terwilliger, R. Z., Duman, R., & Nestler, E. J. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-10-03674.1999 · Cited by 105
“Acute or chronic stress increases the spontaneous firing rate of LC neurons (Abercrombie and Jacobs, 1987; Simson and Weiss, 1988; Pavcovich and Ramirez, 1991) and the expression of tyrosine hydroxylase, the rate-limiting enzyme for norepinephrine biosynthesis (Thoenen, 1970; Zigmond et al., 1974;…”
Background

Authors: Abercrombie, E., & Jacobs, B.
Affiliations: University of Pittsburgh (US)
Venue: The Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 1987-09-01
Volume: 7
Issue: 9
Pages: 2837-2843
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.07-09-02837.1987
PMC: PMC6569145
OpenAlex: W1924384005
Cited by: 377
References: 38
Citations by year: 2026: 3 · 2025: 3 · 2024: 2 · 2022: 5 · 2021: 7 · 2020: 8 · 2019: 5 · 2018: 7 · 2017: 5 · 2016: 11 · 2015: 5 · 2014: 12 · 2013: 12 · 2012: 10
FWCI: 6.22
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-sa
creativecommons.org/licenses/by-nc-sa/4.0/ (vor, 182 d)
Locations: Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Rutgers University Community Repository (Rutgers University) (submittedVersion)
Funders: National Institute of Mental Health (MH23433, MH09256)
Air Force Office of Scientific Research
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 › Endocrine and Autonomic Systems › Neuroscience of respiration and sleep
Keywords: locus coeruleus, noradrenergic neurons, stress response, single-unit activity, plasma norepinephrine, heart rate, restraint stress, white noise, behavioral activation, cats
MeSH terms: Animals, Behavior, Animal, Cats, Female, Heart Rate, Locus Coeruleus, Male, Neurons, Norepinephrine, Stress, Physiological

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Single-unit response of noradrenergic neurons in the locus coeruleus of freely moving cats. I. Acutely presented stressful and nonstressful stimuli

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