Stressor controllability and learned helplessness: the roles of the dorsal raphe nucleus, serotonin, and corticotropin-releasing factor.

Maier, Steven F.; Watkins, Linda R.

doi:10.1016/j.neubiorev.2005.03.021

Cited by 737Stress Responses and CortisolNeurotransmitter Receptor Influence on BehaviorNeuropeptides and Animal Physiology

Stressor controllability and learned helplessness: the roles of the dorsal raphe nucleus, serotonin, and corticotropin-releasing factor.

Maier, Steven F., Watkins, Linda R.·2005·Neuroscience & Biobehavioral Reviews

DOI 10.1016/j.neubiorev.2005.03.021

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Abstract

The term 'learned helplessness' refers to a constellation of behavioral changes that follow exposure to stressors that are not controllable by means of behavioral responses, but that fail to occur if the stressor is controllable. This paper discusses the nature of learned helplessness, as well as the role of the dorsal raphe nucleus, serotonin, and corticotropin-releasing hormone in mediating the behavioral effects of uncontrollable stressors. Recent research indicates that (a) uncontrollable stressors sensitize serotonergic neurons in the dorsal raphe, and that a corticotropin-releasing factor-related ligand, acting at the Type II receptor, is essential to this sensitization process, and (b) the consequent exaggerated release of serotonin in response to subsequent input is at least in part responsible for the behavioral changes that occur. Finally, implications for the general role of corticotropin-releasing hormone in stress-related phenomena and for the learned helplessness paradigm as an animal model of either depression or anxiety are discussed.

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Inescapable shock produces a broad suite of behavioral changes that do not occur when shocks are escapable.
“a wide range of other behavioral changes followed INESC including reduced aggression, reduced social dominance, reduced food and water intake, exaggerated attention to external cues, reduced preference for sweet tastes, potentiated fear conditioning, slowed fear extinction, neophobia, anxious behavior on measures such as juvenile social exploration, potentiated opioid reward, exaggerated stereotyp”
From Learned helplessness at fifty: Insights from neuroscience. (2016) · cites this paper as Maier & Watkins, 2005
Learned helplessness depends critically on pre- and infralimbic cortex in rats, and is known to be mediated by serotonin.
“Third, learned helplessness, which can be interpreted in goal-directed terms [17], depends critically on pre- and infralimbic cortex in rats [38], and is known to be mediated by serotonin [39].”
From Bonsai trees in your head: how the pavlovian system sculpts goal-directed choices by pruning decision trees (2012) · cites this paper as [39]

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Serotonin dysfunction disorders: a behavioral neurochemistry perspective.
Petty, F., Davis, L. L., Kabel, D., & Kramer, G. L. (1996) · PubMed · Cited by 73 · see citing works
The Effect of Stressor Controllability on Stress‐Induced Neuropeptide mRNA Expression within the Paraventricular Nucleus of the Hypothalamus
Helmreich, Watkins, Deak, Maier, Akil, & Watson (1999) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.1999.00300.x · Cited by 73 · see citing works
The dorsal raphe nucleus is a site of action mediating the behavioral effects of benzodiazepine receptor inverse agonist DMCM.
Maier, S. F., Busch, C. R., Maswood, S., Grahn, R. E., & al, E. (1995) · Behavioral Neuroscience · doi:10.1037//0735-7044.109.4.759 · Cited by 73 · see citing works
Self-citation
Differential Effects of Ipsapirone on 5‐Hydroxytryptamine Release in the Dorsal and Median Raphe Neuronal Pathways
Casanovas, J. M., & Artigas, F. (1996) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1996.67051945.x · Cited by 72 · see citing works
125I-Antisauvagine-30: a novel and specific high-affinity radioligand for the characterization of corticotropin-releasing factor type 2 receptors
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Noradrenergic modulation of serotonin release in rat dorsal and median raphé nuclei via α1 and α2A adrenoceptors
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Serotonin (5-HT) release in the dorsal raph� and ventral hippocampus: Raph� control of somatodendritic and terminal 5-HT release
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Low doses of corticotropin-releasing hormone injected into the dorsal raphe nucleus block the behavioral consequences of uncontrollable stress
Hammack, S. E., Pepin, J. L., DesMarteau, J. S., Watkins, L. R., & Maier, S. F. (2003) · Behavioural Brain Research · doi:10.1016/s0166-4328(03)00133-5 · Cited by 60 · see citing works
Self-citation
Chlordiazepoxide microinjected into the region of the dorsal raphe nucleus eliminates the interference with escape responding produced by inescapable shock whether administered before inescapable shock or escape testing.
Maier, S. F., Kalman, B. A., & Grahn, R. E. (1994) · Behavioral Neuroscience · doi:10.1037/0735-7044.108.1.121 · Cited by 55 · see citing works
Self-citation
The dorsal raphe nucleus is a site of action mediating the behavioral effects of the benzodiazepine receptor inverse agonist DMCM.
Maier, S. F., Busch, C. R., Maswood, S., Grahn, R. E., & Watkins, L. R. (1995) · Behavioral Neuroscience · doi:10.1037/0735-7044.109.4.759 · Cited by 53 · see citing works
Self-citation
The lesion of serotonergic neurons does not prevent antidepressant-induced reversal of escape failures produced by inescapable shocks in rats
Soubrié, P., Martin, P., Mestikawy, S. E., Thiébot, M.-H., Simon, P., & Hamon, M. (1986) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(86)90220-0 · Cited by 50 · see citing works
Antidepressants and receptor function.
Porter, R., Bock, G., Clark, S. M., et al. (1986) · PubMed · Cited by 49 · see citing works
Differential activation of the 5-hydroxytryptamine-containing neurons of the midbrain raphe of the rat in response to randomly presented inescapable sound
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Antidepressants and receptor function
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Electrolytic lesions and pharmacological inhibition of the dorsal raphe nucleus prevent stressor potentiation of morphine conditioned place preference in rats
Will, M. J., Der-Avakian, A., Bland, S. T., Grahn, R. E., Hammack, S. E., Sparks, P. D., Pepin, J. L., Watkins, L. R., & Maier, S. F. (2004) · Psychopharmacology · doi:10.1007/s00213-003-1572-1 · Cited by 40 · see citing works
Self-citation
Blockade of alpha1 adrenoreceptors in the dorsal raphe nucleus prevents enhanced conditioned fear and impaired escape performance following uncontrollable stressor exposure in rats
Grahn, R. E., Hammack, S. E., Will, M. J., O'Connor, K. A., Deak, T., Sparks, P. D., Watkins, L. R., & Maier, S. F. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00061-x · Cited by 40 · see citing works
Self-citation
Opioid-dependent effects of inescapable shock on escape behavior and conditioned fear responding are mediated by the dorsal raphe nucleus
Grahn, R. E., Maswood, S., McQueen, M. B., Watkins, L. R., & Maier, S. F. (1999) · Behavioural Brain Research · doi:10.1016/s0166-4328(98)00101-6 · Cited by 37 · see citing works
Self-citation
Effect of blockade of corticotropin-releasing factor receptors in the median raphe nucleus on stress-induced c-fos mRNA in the rat brain
Funk, D. R., Li, Z., Shaham, Y., & Lê, A. D. (2003) · Neuroscience · doi:10.1016/j.neuroscience.2003.08.003 · Cited by 33 · see citing works
Editorial: Neuroendocrinology With Feeling
Russell, J. A. (2002) · Journal of Neuroendocrinology · doi:10.1046/j.0007-1331.2001.00760.x · Cited by 31 · see citing works
[Corticotropin releasing factor].
Cy, H., & Hu, B. (1986) · PubMed · Cited by 28 · see citing works
Factors that modulate inescapable shock-induced reductions in daily activity in the rat
Woodmansee, W. W., Silbert, L. H., & Maier, S. F. (1993) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(93)90505-n · Cited by 26 · see citing works
Self-citation
Involvement of corticotropin-releasing factor subtype 1 receptor in the acquisition phase of learned helplessness in rats
Takamori, K., Kawashima, N., Chaki, S., et al. (2001) · Life Sciences · doi:10.1016/s0024-3205(01)01217-6 · Cited by 25 · see citing works
Modulation of the locomotor properties of morphine and amphetamine by uncontrollable stress
Will, M. J., Der‐Avakian, A., Pepin, J. L., Durkan, B. T., Watkins, L. R., & Maier, S. F. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(01)00719-5 · Cited by 22 · see citing works
Self-citation
Inescapable shock-induced potentiation of morphine analgesia.
Sutton, L. C., Lea, S. E., Will, M. J., Schwartz, B., Hartley, C. E., Poole, J. C., Watkins, L. R., & Maier, S. F. (1997) · Behavioral Neuroscience · doi:10.1037//0735-7044.111.5.1105 · Cited by 17 · see citing works
Self-citation
Circling behavior induced by microinjection of serotonin reuptake inhibitors in the substantia nigra
Bata-García, J. L., Heredia-López, F. J., Álvarez-Cervera, F. J., et al. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(01)00721-3 · Cited by 12 · see citing works
Inescapable shock-induced potentiation of morphine analgesia.
Sutton, L. C., Lea, S. E., Will, M. J., et al. (1997) · Behavioral Neuroscience · doi:10.1037/0735-7044.111.5.1105 · Cited by 12 · see citing works

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Animal models of neuropsychiatric disorders
Nestler, E. J., & Hyman, S. E. (2010) · Nature Neuroscience · doi:10.1038/nn.2647 · Cited by 2,023 · see citing works
The brain reward circuitry in mood disorders
Russo, S. J., & Nestler, E. J. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3381 · Cited by 1,870 · see citing works
The role of medial prefrontal cortex in memory and decision making
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The neuro-symphony of stress
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More than a feeling: A unified view of stress measurement for population science
Epel, E. S., Crosswell, A. D., Mayer, S. E., Prather, A. A., Slavich, G. M., Puterman, E., & Mendes, W. B. (2018) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2018.03.001 · Cited by 1,077 · see citing works
“Other work has focused on the degree of controllability that different stressors possess (Maier and Watkins, 2005).”
Background
The habenula: from stress evasion to value-based decision-making
Hikosaka, O. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2866 · Cited by 955 · see citing works
Learned helplessness at fifty: Insights from neuroscience.
Maier, S. F., & Seligman, M. E. P. (2016) · Psychological Review · doi:10.1037/rev0000033 · Cited by 919 · see citing works
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The Biological Effects of Childhood Trauma
De Bellis, M. D., & Zisk, A. (2014) · Child and Adolescent Psychiatric Clinics of North America · doi:10.1016/j.chc.2014.01.002 · Cited by 892 · see citing works
Computational psychiatry
Montague, P. R., Dolan, R. J., Friston, K. J., & Dayan, P. (2012) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2011.11.018 · Cited by 809 · see citing works
Stress, serotonin, and hippocampal neurogenesis in relation to depression and antidepressant effects
Mahar, I., Bambico, F. R., Mechawar, N., & Nobrega, J. N. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.11.009 · Cited by 694 · see citing works
The Effects of Psychological Stress on Depression
Yang, L., Zhao, Y., Wang, Y., Liu, L., Zhang, X., Li, B., & Cui, R. (2015) · Current Neuropharmacology · doi:10.2174/1570159x1304150831150507 · Cited by 589 · see citing works
Microglia serve as a neuroimmune substrate for stress-induced potentiation of CNS pro-inflammatory cytokine responses
Frank, M. G., Baratta, M. V., Sprunger, D. B., Watkins, L. R., & Maier, S. F. (2007) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2006.03.005 · Cited by 578 · see citing works
Self-citation
The ecology of human fear: survival optimization and the nervous system
Mobbs, D., Hagan, C. C., Dalgleish, T., Silston, B., & PrÃ©vost, C. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00055 · Cited by 498 · see citing works
Addiction as a stress surfeit disorder
Koob, G. F., Buck, C. L., Cohen, A., Edwards, S., Park, P. E., Schlosburg, J. E., Schmeichel, B., Vendruscolo, L. F., Wade, C. L., Whitfield, T. W., et al. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.05.024 · Cited by 483 · see citing works
Stress-induced prefrontal reorganization and executive dysfunction in rodents
Holmes, A., & Wellman, C. L. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.11.005 · Cited by 469 · see citing works
Stress-induced reinstatement of drug seeking: 20 years of progress
Mantsch, J. R., Baker, D. A., Funk, D., Lê, A. D., & Shaham, Y. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2015.142 · Cited by 438 · 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
Opponency revisited: competition and cooperation between dopamine and serotonin
Boureau, Y.-L., & Dayan, P. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.151 · Cited by 456 · see citing works
Bonsai trees in your head: how the pavlovian system sculpts goal-directed choices by pruning decision trees
Huys, Q. J. M., Eshel, N., O'Nions, E., Sheridan, L., Dayan, P., & Roiser, J. P. (2012) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002410 · Cited by 439 · see citing works
Addiction is a Reward Deficit and Stress Surfeit Disorder
Koob, G. F. (2013) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2013.00072 · Cited by 397 · see citing works
Serotonergic neurons signal reward and punishment on multiple timescales
Cohen, J. Y., Amoroso, M. W., & Uchida, N. (2015) · eLife · doi:10.7554/elife.06346 · Cited by 388 · see citing works
Serotonin in Affective Control
Dayan, P., & Huys, Q. J. M. (2009) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.051508.135607 · Cited by 381 · see citing works
Sex differences in anxiety and emotional behavior
Donner, N. C., & Lowry, C. A. (2013) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-013-1271-7 · Cited by 379 · see citing works
Presynaptic partners of dorsal raphe serotonergic and GABAergic neurons
Weissbourd, B., Ren, J., DeLoach, K. E., Guenthner, C. J., Miyamichi, K., & Luo, L. (2014) · Neuron · doi:10.1016/j.neuron.2014.06.024 · Cited by 337 · see citing works
Embracing diversity in the 5-HT neuronal system
Okaty, B. W., Commons, K. G., & Dymecki, S. M. (2019) · Nature Reviews Neuroscience · doi:10.1038/s41583-019-0151-3 · Cited by 319 · see citing works
Computational psychiatry: towards a mathematically informed understanding of mental illness
Adams, R. A., Huys, Q. J. M., & Roiser, J. P. (2015) · Journal of Neurology, Neurosurgery & Psychiatry · doi:10.1136/jnnp-2015-310737 · Cited by 285 · see citing works
Life Stress and Health: A Review of Conceptual Issues and Recent Findings
Slavich, G. M. (2016) · Teaching of Psychology · doi:10.1177/0098628316662768 · Cited by 300 · see citing works
Cascading effects of stressors and inflammatory immune system activation: Implications for major depressive disorder
Anisman, H. (2009) · Journal of Psychiatry and Neuroscience · doi:10.1139/jpn.0902 · Cited by 292 · see citing works
The neurobiology of individual differences in complex behavioral traits
Hariri, A. R. (2009) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.051508.135335 · Cited by 273 · see citing works
A Self‐Regulatory Model of Resource Scarcity
Cannon, C., Goldsmith, K., & Roux, C. (2019) · Journal of Consumer Psychology · doi:10.1002/jcpy.1035 · Cited by 280 · see citing works
Serotonin, inhibition, and negative mood
Dayan, P., & Huys, Q. J. M. (2008) · PLoS Computational Biology · doi:10.1371/journal.pcbi.0040004 · Cited by 263 · see citing works
The Biology of Human Resilience: Opportunities for Enhancing Resilience Across the Life Span
Feder, A., Fred-Torres, S., Southwick, S. M., & Charney, D. S. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.07.012 · Cited by 269 · see citing works
Raphe serotonin neurons are not homogenous: Electrophysiological, morphological and neurochemical evidence
Calizo, L. H., Akanwa, A., Ma, X., Pan, Y.-Z., Lemos, J. C., Craige, C., Heemstra, L. A., & Beck, S. G. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.04.008 · Cited by 252 · see citing works
IL-6 knockout mice exhibit resistance to stress-induced development of depression-like behaviors
Chourbaji, S., Urani, A., Inta, I., Sanchis-Segura, C., Brandwein, C., Zink, M., Schwaninger, M., & Gass, P. (2006) · Neurobiology of Disease · doi:10.1016/j.nbd.2006.05.001 · Cited by 241 · see citing works
Depression: a decision-theoretic analysis
Huys, Q. J. M., Daw, N. D., & Dayan, P. (2015) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-071714-033928 · Cited by 221 · see citing works
Reinforcement learning in depression: a review of computational research
Chen, C., Takahashi, T., Nakagawa, S., Inoue, T., & Kusumi, I. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.05.005 · Cited by 233 · see citing works
Impact of adolescent social experiences on behavior and neural circuits implicated in mental illnesses
Burke, A. R., McCormick, C. M., Pellis, S. M., & Lukkes, J. L. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.01.018 · Cited by 225 · see citing works
Paraventricular nucleus CRH neurons encode stress controllability and regulate defensive behavior selection
Daviu, N., Füzesi, T., Rosenegger, D. G., Rasiah, N. P., Sterley, T.-L., Peringod, G., & Bains, J. S. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-0591-0 · Cited by 217 · see citing works
Previous Experience with Behavioral Control over Stress Blocks the Behavioral and Dorsal Raphe Nucleus Activating Effects of Later Uncontrollable Stress: Role of the Ventral Medial Prefrontal Cortex
Amat, J., Paul, E., Zarza, C., Watkins, L. R., & Maier, S. F. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.3630-06.2006 · Cited by 249 · see citing works
Self-citation
The dorsal raphe nucleus and serotonin: implications for neuroplasticity linked to major depression and Alzheimer's disease
MICHELSEN, K., PRICKAERTS, J., & STEINBUSCH, H. (2008) · Progress in Brain Research · doi:10.1016/s0079-6123(08)00912-6 · Cited by 196 · see citing works
Individual Differences in the Effects of Perceived Controllability on Pain Perception: Critical Role of the Prefrontal Cortex
Salomons, T. V., Johnstone, T., Backonja, M.-M., Shackman, A. J., & Davidson, R. J. (2007) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2007.19.6.993 · Cited by 195 · see citing works
Identification of an immune-responsive mesolimbocortical serotonergic system: potential role in regulation of emotional behavior
Lowry, C. A., Hollis, J. H., de Vries, A., Pan, B., Brunet, L. R., Hunt, J. R. F., Paton, J. F. R., van Kampen, E., Knight, D. M., Evans, A. K., et al. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.01.067 · Cited by 199 · 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
Twenty-Five Lessons from Computational Neuromodulation
Dayan, P. (2012) · Neuron · doi:10.1016/j.neuron.2012.09.027 · Cited by 190 · see citing works
Females do not express learned helplessness like males do
Dalla, C., Edgecomb, C., Whetstone, A. S., & Shors, T. J. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301533 · Cited by 174 · see citing works
Effects of HTR1A C(−1019)G on Amygdala Reactivity and Trait Anxiety
Fakra, E., Hyde, L. W., Gorka, A., Fisher, P. M., Muñoz, K. E., Kimak, M., Halder, I., Ferrell, R. E., Manuck, S. B., & Hariri, A. R. (2009) · Archives of General Psychiatry · doi:10.1001/archpsyc.66.1.33 · Cited by 159 · see citing works
Overlapping neurobiology of learned helplessness and conditioned defeat: Implications for PTSD and mood disorders
Hammack, S. E., Cooper, M. A., & Lezak, K. R. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.02.024 · Cited by 142 · see citing works
Agency and the Calibration of Motivated Behavior
Moscarello, J. M., & Hartley, C. A. (2017) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2017.06.008 · Cited by 137 · see citing works
Induction of ΔFosB in the Periaqueductal Gray by Stress Promotes Active Coping Responses
Berton, O., Covington, H. E., Ebner, K., Tsankova, N. M., Carle, T. L., Ulery, P., Bhonsle, A., Barrot, M., Krishnan, V., Singewald, G. M., et al. (2007) · Neuron · doi:10.1016/j.neuron.2007.06.033 · Cited by 129 · see citing works
Paraventricular thalamic nucleus: Subcortical connections and innervation by serotonin, orexin, and corticotropin‐releasing hormone in macaque monkeys
Hsu, D. T., & Price, J. L. (2009) · Journal of Comparative Neurology · doi:10.1002/cne.21934 · Cited by 127 · see citing works
Stress-evoked sterile inflammation, danger associated molecular patterns (DAMPs), microbial associated molecular patterns (MAMPs) and the inflammasome
Fleshner, M. (2013) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2012.08.012 · Cited by 126 · see citing works
Translational studies of goal-directed action as a framework for classifying deficits across psychiatric disorders
Griffiths, K. R., Morris, R. W., & Balleine, B. W. (2014) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2014.00101 · Cited by 118 · see citing works
Synaptic Modifications in the Medial Prefrontal Cortex in Susceptibility and Resilience to Stress
Wang, M., Perova, Z., Arenkiel, B. R., & Li, B. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.5294-13.2014 · Cited by 116 · see citing works
Exposure to early adversity: points of cross-species translation that can lead to improved understanding of depression
Andersen, S. L. (2015) · Development and Psychopathology · doi:10.1017/s0954579415000103 · Cited by 116 · see citing works
Stressor controllability modulates fear extinction in humans
Hartley, C. A., Gorun, A., Reddan, M. C., Ramirez, F., & Phelps, E. A. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.12.003 · Cited by 110 · see citing works
The response of neurons in the bed nucleus of the stria terminalis to serotonin: Implications for anxiety
Hammack, S. E., Guo, J.-D., Hazra, R., Dabrowska, J., Myers, K. M., & Rainnie, D. G. (2009) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2009.05.013 · Cited by 103 · see citing works
“…involvesmultiple CRF receptor subtypes expressed by both 5-HT and GABAergic neurons (Day et al., 2004; Hammack et al., 2003a; Kirby et al., 2008; Maier and Watkins, 2005)the caudal DRN is the DRN subregion in which putative serotonergic neurons are excited by CRF application (Kirby et al.,…”
Background
Environmental programming of susceptibility and resilience to stress in adulthood in male mice
Peña, C. J., Nestler, E. J., & Bagot, R. C. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00040 · Cited by 97 · see citing works
Selective activation of dorsal raphe nucleus‐projecting neurons in the ventral medial prefrontal cortex by controllable stress
Baratta, M. V., Zarza, C. M., Gomez, D. M., Campeau, S., Watkins, L. R., & Maier, S. F. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06867.x · Cited by 106 · see citing works
Self-citation
The Sensory Insular Cortex Mediates the Stress-Buffering Effects of Safety Signals But Not Behavioral Control
Christianson, J. P., Benison, A. M., Jennings, J., Sandsmark, E. K., Amat, J., Kaufman, R. D., Baratta, M. V., Paul, E. D., Campeau, S., Watkins, L. R., et al. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.4270-08.2008 · Cited by 97 · see citing works
Self-citation
Environmental and pharmacological modulations of cellular plasticity: Role in the pathophysiology and treatment of depression
Ota, K. T., & Duman, R. S. (2013) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.05.022 · Cited by 94 · see citing works
Role of dorsal medial prefrontal cortex dopamine D1-family receptors in relapse to high-fat food seeking induced by the anxiogenic drug yohimbine
Nair, S. G., Navarre, B. M., Cifani, C., Pickens, C. L., Bossert, J. M., & Shaham, Y. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.181 · Cited by 85 · see citing works
Decreased SGK1 Expression and Function Contributes to Behavioral Deficits Induced by Traumatic Stress
Licznerski, P., Duric, V., Banasr, M., Alavian, K. N., Ota, K. T., Kang, H. J., Jonas, E. A., Ursano, R., Krystal, J. H., Duman, R. S., et al. (2015) · PLOS Biology · doi:10.1371/journal.pbio.1002282 · Cited by 79 · see citing works
Sensitivity shift theory: a developmental model of positive affect and motivational deficits in social anxiety disorder
Richey, J. A., Brewer, J. A., Sullivan-Toole, H., Strege, M. V., Kim-Spoon, J., White, S. W., & Ollendick, T. H. (2019) · Clinical Psychology Review · doi:10.1016/j.cpr.2019.101756 · Cited by 79 · see citing works
Endocannabinoids suppress excitatory synaptic transmission to dorsal raphe serotonin neurons through the activation of presynaptic CB1 receptors.
Haj-Dahmane, S., & Shen, R.-Y. (2009) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.109.153858 · Cited by 69 · see citing works
Current understanding of fear learning and memory in humans and animal models and the value of a linguistic approach for analyzing fear learning and memory in humans
Raber, J., Arzy, S., Bertolus, J. B., Depue, B., Haas, H. E., Hofmann, S. G., Kangas, M., Kensinger, E., Lowry, C. A., Marusak, H. A., et al. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.03.015 · Cited by 62 · see citing works
“This effect is thought to be dependent on desensitization of inhibitory 5-HT1A autoreceptors that normally inhibit serotonergic neuronal firing within the anxietyand fear-related dorsomedial part of the dorsal raphe nucleus (Maier and Watkins, 2005; Rozeske et al., 2011).”
Learned helplessness is independent of levels of brain-derived neurotrophic factor in the hippocampus
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Authors: Maier, S. F., & Watkins, L. R.
Affiliations: University of Colorado Boulder (US)
Corresponding author: Maier, Steven F.
ORCID: Maier, Steven F.
Watkins, Linda R.
Venue: Neuroscience & Biobehavioral Reviews
Publisher: Elsevier BV
Published: 2005-01
Volume: 29
Issue: 4-5
Pages: 829-841
ISSN: 0149-7634 (ISSN-L)
DOI: 10.1016/j.neubiorev.2005.03.021
OpenAlex: W2116777802
Semantic Scholar: a0eb0424476a0d533d4e5c27e3d5e517c6e61a09
Cited by: 737
References: 105
Citations by year: 2026: 14 · 2025: 22 · 2024: 23 · 2023: 29 · 2022: 33 · 2021: 38 · 2020: 29 · 2019: 37 · 2018: 30 · 2017: 32 · 2016: 35 · 2015: 46 · 2014: 41 · 2013: 56 · 2012: 47
FWCI: 1.96
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neuroscience & Biobehavioral Reviews (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute of Mental Health (MH 50479)
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 › Neuropeptides and Animal Physiology
Keywords: learned helplessness, stressor controllability, dorsal raphe nucleus, serotonin, corticotropin-releasing factor, uncontrollable stress, depression, anxiety, animal models of depression
MeSH terms: Animals, Anxiety, Behavior, Animal, Corticotropin-Releasing Hormone, Helplessness, Learned, Humans, Raphe Nuclei, Serotonin, Stress, Physiological

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Stressor controllability and learned helplessness: the roles of the dorsal raphe nucleus, serotonin, and corticotropin-releasing factor.

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