Cited by 194Neurotransmitter Receptor Influence on BehaviorStress Responses and CortisolNeuropeptides and Animal Physiology

The DOI matches its Crossref record; 64 of the 64 references it cites were found in a registry or an index.

Nucleus accumbens corticotropin-releasing factor increases cue-triggered motivation for sucrose reward: paradoxical positive incentive effects in stress?

Open access

Peciña, Susana, Schulkin, Jay, Berridge, Kent C·2006·BMC Biology

DOI 10.1186/1741-7007-4-8PMC PMC1459217

Open this paper in CoChat — free account Open PDF

Abstract

Background: Corticotropin-releasing factor (CRF) is typically considered to mediate aversive aspects of stress, fear and anxiety. However, CRF release in the brain is also elicited by natural rewards and incentive cues, raising the possibility that some CRF systems in the brain mediate an independent function of positive incentive motivation, such as amplifying incentive salience. Here we asked whether activation of a limbic CRF subsystem magnifies the increase in positive motivation for reward elicited by incentive cues previously associated with that reward, in a way that might exacerbate cue-triggered binge pursuit of food or other incentives? We assessed the impact of CRF microinjections into the medial shell of nucleus accumbens using a pure incentive version of Pavlovian-Instrumental transfer, a measure specifically sensitive to the incentive salience of reward cues (which it separates from influences of aversive stress, stress reduction, frustration and other traditional explanations for stress-increased behavior). Rats were first trained to press one of two levers to obtain sucrose pellets, and then separately conditioned to associate a Pavlovian cue with free sucrose pellets. On test days, rats received microinjections of vehicle, CRF (250 or 500 ng/0.2 μl) or amphetamine (20 μg/0.2 μl). Lever pressing was assessed in the presence or absence of the Pavlovian cues during a half-hour test. Results: Microinjections of the highest dose of CRF (500 ng) or amphetamine (20 μg) selectively enhanced the ability of Pavlovian reward cues to trigger phasic peaks of increased instrumental performance for a sucrose reward, each peak lasting a minute or so before decaying after the cue. Lever pressing was not enhanced by CRF microinjections in the baseline absence of the Pavlovian cue or during the presentation without a cue, showing that the CRF enhancement could not be explained as a result of generalized motor arousal, frustration or stress, or by persistent attempts to ameliorate aversive states. Conclusion: We conclude that CRF in nucleus accumbens shell amplifies positive motivation for cued rewards, in particular by magnifying incentive salience that is attributed to Pavlovian cues previously associated with those rewards. CRF-induced magnification of incentive salience provides a novel explanation as to why stress may produce cue-triggered bursts of binge eating, drug addiction relapse, or other excessive pursuits of rewards.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1186/1741-7007-4-8

Cites

64 of 64 references verified0 citation errors · 0 not checkable

Statistics

Figure 1 Fos plumes. Coronal sections showing point sample positions used to identify local Fos plumes around microinjection site. A. Vehicle microinjection produces merely low elevation of Fos compared to normal virgin tissue. Radial arms extending from center show sampling points for Fos measurement (125 μm × 125 μm blocks; 5× magnification). B. CRF microinjection induces intense elevation over normal tissue levels (depicted by color: 10× elevation over normal denoted by yellow, 5× = dark orange; 2× = light orange). CRF also causes elevation compared to vehicle microinjection levels at equivalent points (depicted by dotted lines; 3× relative increase over vehicle-levels denoted by thick dotted line, 5× = thin dotted line; upper right; plume from CRF 500 ng dose in 0.2 μl microinjection volume).CC BY · PubMed Central

Figure 2 Fos plume maps of CRF (500 ng) amplification of cue-triggered increases in lever pressing. Fos plume maps of functional localization: CRF effects on cue-triggered incentive salience. Sagittal (A), horizontal (B), and coronal maps (C) show each Fos plume as colored symbol in medial shell of nucleus accumbens. Color depicts magnification effect of CRF (500 ng) microinjection at that site on peaks of lever pressing triggered by a 30 sec auditory CS+ previously associated with sucrose reward (within-subject percentage elevation of CRF versus vehicle in the same rat; 100%=vehicle). Size of central symbol depicts radius of intense Fos elevation; size of surrounding halos depict outer radius of moderate Fos elevation. For the sagittal map, bilateral accumbens sites from left and right sides of each rat brain are collapsed together into one combined sagittal map of accumbens for simplicity. Maps adapted from Paxinos and Watson [46].CC BY · PubMed Central

Figure 3 Enhancement of incentive motivation by CRF. Effects on cue-triggered lever pressing during extinction test caused by CRF (250 and 500 ng) and amphetamine (20 μg) microinjections in the caudal medial accumbens shell. A. Lines show pressing in the presence of the CS+ (previously associated with sucrose- red circles); and CS- (never associated with sucrose- blue circles); and pre-CS+ baseline period (no-stimulus 30 sec period immediately prior to CS+ stimulus); and pre-CS- baseline period (30 sec immediately prior to CS- stimulus). The left panel depicts lever pressing on the control lever that had previously produced instrumental sucrose reward during training (but not during extinction test). The right panel depicts lever pressing on the control lever that was never had produced reward. Both 500 ng CRF and 20 μg amphetamine increased the ability of the sucrose CS+ cue (but not CS-) to trigger enhanced responding on the previously sucrose-associated lever (but not on the control lever). B. Transform scores show a direct contrast between CS+ and CS- effects of lever pressing. CS+ effects on cue-triggered lever pressing are amplified by CRF (500 ng) and by amphetamine (20 μg) microinjections.CC BY · PubMed Central

Figure 4 Temporal pattern of lever pressing within test session. Minute-by-minute time-course of lever pressing peaks on sucrose-associated lever after microinjections of (A) vehicle, (B) amphetamine 20 μg, (C) CRF 500 ng, and (D) CRF 250 ng. Open circles depict lever pressing during presentation of the 30-sec CS- and filled circles during presentation of the CS+. Lever pressing is also shown during the 30 sec period before each CS+ or CS- (precue baseline), and during the 30 sec period that followed each CS+ or CS- (post-cue period). Both CRF (500 ng) and amphetamine (20 μg) magnified intense, transient, reversible, and repeatable peaks in pressing on sucrose-associated lever each time the CS+ occurred. Magnified lever pressing after CRF (500 ng) or amphetamine (20 μg) was triggered by each presentation of the sucrose cue, but then was followed by a rapid descent back to normal baseline levels of pressing once the cue ended (B and C).CC BY · PubMed Central

Figure 5 Response competition between sucrose dish approach and lever pressing. A. Averaged time-course of approach responses to sucrose dish just before, during and after first CS+ cue presentation. B. Same information for pressing on sucrose-associated lever. Each panel compares cue-triggered responding after microinjections of vehicle (white circles), CRF 500 μg (green circles), CRF 250 μg (blue circles), or amphetamine 20 μg (red circles). Both CRF and amphetamine reduced the peak of cue-triggered approaches to the sucrose dish, but simultaneously increased cue-triggered lever pressing. It is impossible to perform both actions at exactly the same time, and so conditioned dish approaches may have been suppressed as a result of response competition from increased lever pressing that occurred during the same 30-sec period.CC BY · PubMed Central

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

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?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

The rat brain in stereotaxic coordinates
Palkovits, M. (1983) · Neuropeptides · doi:10.1016/0143-4179(83)90049-5 · Cited by 28,959
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · cited 4×
“Cannulae were aimed at the caudal half of the accumbens: 2.8-2.2 mm anterior to bregma, 0.9 mm lateral to the midline, and 5.7 mm ventral to the skull surface (2.0 mm above the injection site), based on the atlas of Paxinos and Watson (1996).”
Influential
AChE-stained horizontal sections of the rat brain in stereotaxic coordinates
Paxinos, G., WATSON, C. R. R., & Emson, P. C. (1980) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(80)90021-7 · Cited by 4,514
Classical conditioning II: Current research and theory.
Black, A. H., & Prokasy, W. F. (1972) · Appleton-Century-Crofts eBooks · Cited by 4,449
What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience?
Berridge, K. C., & Robinson, T. E. (1998) · Brain Research Reviews · doi:10.1016/s0165-0173(98)00019-8 · Cited by 4,127
Self-citation
Drug Addiction, Dysregulation of Reward, and Allostasis
Koob, G. (2001) · Neuropsychopharmacology · doi:10.1016/s0893-133x(00)00195-0 · Cited by 2,953 · cited 3×
“For example, cocaine administration also activates CRF expression in CRH-producing neurons in hypothalamus and amygdala [13] and CRF given intracerebroventricularly (ICV) or into the ventrolateral BNST can induce reinstatement of drug self-administration behavior in the absence of external stressors (though this last…”
Organization of ovine corticotropin-releasing factor immunoreactive cells and fibers in the rat brain: an immunohistochemical study
Swanson, L. W., Sawchenko, P. E., Rivier, J., & Vale, W. W. (2008) · Neuroendocrinology · doi:10.1159/000123454 · Cited by 1,953 · cited 1×
“The medial shell of nucleus accumbens also contains substantial distributions of CRF-immunoreactive and fibers, which might arise in part from hypothalamic CRF systems linked to stress, as well as cell bodies (particularly in its caudal half, and thus we focused on caudal shell here) [26].”
An opponent-process theory of motivation. I. Temporal dynamics of affect
Solomon, R. L., & Corbit, J. D. (1974) · Psychological Review · doi:10.1037/h0036128 · Cited by 1,704 · cited 2×
“Such appetitive behaviors have often been viewed as attempts to reduce or avoid unpleasant stress or as overflow from general motor arousal or frustration ([ 12-14 ] but see [8-11]).”
Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo–pituitary–adrenocortical responsiveness
Herman, J. P., Figueiredo, H., Mueller, N. K., Ulrich-Lai, Y., Ostrander, M. M., Choi, D. C., & Cullinan, W. E. (2003) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2003.07.001 · Cited by 1,586 · cited 2×
“Corticotropin-releasing factor (CRF) is involved in mediating the physiological and behavioral responses to stress [ 1-5 ].”
Addiction
Robinson, T. E., & Berridge, K. C. (2003) · Annual Review of Psychology · doi:10.1146/annurev.psych.54.101601.145237 · Cited by 1,509
Self-citation

Show all 64 references

Research works printed but not linked: 1

Toates FM: Motivational Systems. 1986, Cambridge: Cambridge University Press

Sorted by citations

The debate over dopamine’s role in reward: the case for incentive salience
Berridge, K. C. (2007) · Psychopharmacology · doi:10.1007/s00213-006-0578-x · Cited by 2,347
Self-citation
Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex
Ikemoto, S. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.05.004 · Cited by 1,477
“Liking” and “wanting” food rewards: Brain substrates and roles in eating disorders
Berridge, K. C. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2009.02.044 · Cited by 1,147
Self-citation
The tempted brain eats: Pleasure and desire circuits in obesity and eating disorders
Berridge, K. C., Ho, C.-Y., Richard, J. M., & DiFeliceantonio, A. G. (2010) · Brain Research · doi:10.1016/j.brainres.2010.04.003 · Cited by 873
Self-citation
Reward mechanisms in obesity: new insights and future directions
Kenny, P. J. (2011) · Neuron · doi:10.1016/j.neuron.2011.02.016 · Cited by 748
From prediction error to incentive salience: mesolimbic computation of reward motivation.
Berridge, K. C. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.07990.x · Cited by 700
Self-citation
Hedonic Hot Spots in the Brain
Peciña, S., Smith, K. S., & Berridge, K. C. (2006) · The Neuroscientist · doi:10.1177/1073858406293154 · Cited by 441
Self-citation
“Liking” and “wanting” in eating and food reward: Brain mechanisms and clinical implications
Morales, I., & Berridge, K. C. (2020) · Physiology & Behavior · doi:10.1016/j.physbeh.2020.113152 · Cited by 346
Self-citation
An integrative theoretical framework for understanding sexual motivation, arousal, and behavior
Toates, F. (2009) · Journal of Sex Research · doi:10.1080/00224490902747768 · Cited by 339
Pavlovian to instrumental transfer: a neurobehavioural perspective.
Holmes, N. M., Marchand, A., & Coutureau, E. (2010) · Neuroscience and Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.03.007 · Cited by 327
Appetitive Pavlovian-instrumental Transfer: A review
Cartoni, E., Balleine, B. W., & Baldassarre, G. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.09.020 · Cited by 346
Addiction and Stress: An Allostatic View
Koob, G. F., & Schulkin, J. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.09.008 · Cited by 315
Self-citation
The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction
Burkett, J. P., & Young, L. J. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2794-x · Cited by 307
“CRF in the NACs can also enhance the positive motivational value and salience of incentive cues (Pecina et al. 2006; Kreibich et al. 2009).”
Severe stress switches CRF action in the nucleus accumbens from appetitive to aversive
Lemos, J. C., Wanat, M. J., Smith, J. S., Reyes, B. A. S., Hollon, N. G., Bockstaele, E. J. V., Chavkin, C., & Phillips, P. E. M. (2012) · Nature · doi:10.1038/nature11436 · Cited by 319
A Motivational and Neuropeptidergic Hub: Anatomical and Functional Diversity within the Nucleus Accumbens Shell
Castro, D. C., & Bruchas, M. R. (2019) · Neuron · doi:10.1016/j.neuron.2019.03.003 · Cited by 306
The psychobiology of comfort eating: implications for neuropharmacological interventions
Gibson, E. L. (2012) · Behavioural Pharmacology · doi:10.1097/fbp.0b013e328357bd4e · Cited by 262
Corticotropin‐releasing factor increases mouse ventral tegmental area dopamine neuron firing through a protein kinase C‐dependent enhancement of Ih
Wanat, M. J., Hopf, F. W., Stuber, G. D., Phillips, P. E. M., & Bonci, A. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2007.150078 · Cited by 256
The dark side of food addiction
Parylak, S. L., Koob, G. F., & Zorrilla, E. P. (2011) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.04.063 · Cited by 257
Roles of "wanting" and "liking" in motivating behavior: gambling, food, and drug addictions
Robinson, M. J. F., Fischer, A. M., Ahuja, A., Lesser, E. N., & Maniates, H. (2015) · Current topics in behavioral neurosciences · doi:10.1007/7854_2015_387 · Cited by 247
Calculating utility: preclinical evidence for cost–benefit analysis by mesolimbic dopamine
Phillips, P. E. M., Walton, M. E., & Jhou, T. C. (2007) · Psychopharmacology · doi:10.1007/s00213-006-0626-6 · Cited by 237
Measuring wanting and liking from animals to humans: a systematic review
Pool, E., Sennwald, V., Delplanque, S., Brosch, T., & Sander, D. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.01.006 · Cited by 211
Stress and CRF gate neural activation of BDNF in the mesolimbic reward pathway
Walsh, J. J., Friedman, A. K., Sun, H., Heller, E. A., Ku, S. M., Juarez, B., Burnham, V. L., Mazei-Robison, M. S., Ferguson, D., Golden, S. A., et al. (2014) · Nature Neuroscience · doi:10.1038/nn.3591 · Cited by 210
Dopamine or opioid stimulation of nucleus accumbens similarly amplify cue‐triggered ‘wanting’ for reward: entire core and medial shell mapped as substrates for PIT enhancement
Peciña, S., & Berridge, K. C. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12174 · Cited by 216
Self-citation
Corticotropin-releasing factor projections from limbic forebrain and paraventricular nucleus of the hypothalamus to the region of the ventral tegmental area
Rodaros, D., Caruana, D. A., Amir, S., & Stewart, J. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.09.043 · Cited by 194
Stress, habits, and drug addiction: A psychoneuroendocrinological perspective.
Schwabe, L., Dickinson, A., & Wolf, O. T. (2011) · Experimental and Clinical Psychopharmacology · doi:10.1037/a0022212 · Cited by 202
Palatable Foods, Stress, and Energy Stores Sculpt Corticotropin-Releasing Factor, Adrenocorticotropin, and Corticosterone Concentrations after Restraint
Foster, M. T., Warne, J. P., Ginsberg, A. B., Horneman, H. F., Pecoraro, N. C., Akana, S. F., & Dallman, M. F. (2008) · Endocrinology · doi:10.1210/en.2008-1426 · Cited by 187
Dopamine D1 and D2 receptors in the nucleus accumbens core and shell mediate Pavlovian-instrumental transfer.Preprint
Lex, A., & Hauber, W. (2008) · Learning & memory (Cold Spring Harbor, N.Y.) · doi:10.1101/lm.978708 · Cited by 190
Reward uncertainty enhances incentive salience attribution as sign-tracking
Anselme, P., Robinson, M. J. F., & Berridge, K. C. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.10.006 · Cited by 170
Self-citation
What and when to "want"? Amygdala-based focusing of incentive salience upon sugar and sex
Mahler, S. V., & Berridge, K. C. (2012) · Psychopharmacology · doi:10.1007/s00213-011-2588-6 · Cited by 170
“In this version of PIT the task (Peciña et al. 2006; Wyvell and Berridge 2000, 2001), a noncontingent 30 s Pavlovian CS+ stimulus (which rats previously learned to associate with sucrose) is presented intermittently in the presence of a lever that previously earned sucrose pellets.”
InfluentialSelf-citation
The nucleus accumbens as a nexus between values and goals in goal-directed behavior: a review and a new hypothesis
Mannella, F., Gurney, K., & Baldassarre, G. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00135 · Cited by 166
Social allostasis: anticipatory regulation of the internal milieu
Schulkin, J. (2011) · Frontiers in Evolutionary Neuroscience · doi:10.3389/fnevo.2010.00111 · Cited by 157
Self-citation
Current perspectives on incentive salience and applications to clinical disorders
Olney, J. J., Warlow, S. M., Naffziger, E. E., & Berridge, K. C. (2018) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2018.01.007 · Cited by 157
Self-citation
Caloric Restriction Experience Reprograms Stress and Orexigenic Pathways and Promotes Binge Eating
Pankevich, D. E., Teegarden, S. L., Hedin, A. D., Jensen, C. L., & Bale, T. L. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1955-10.2010 · Cited by 157
Neuronal correlates of depression
Chaudhury, D., Liu, H., & Han, M. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-015-2044-6 · Cited by 150
Neural Mechanisms of Reward in Insects
Perry, C. J., & Barron, A. B. (2013) · Annual Review of Entomology · doi:10.1146/annurev-ento-120811-153631 · Cited by 135
Behavioural characterisation of chronic unpredictable stress based on ethologically relevant paradigms in rats
Sequeira‐Cordero, A., Salas-Bastos, A., Fornaguera, J., & Brenes, J. C. (2019) · Scientific Reports · doi:10.1038/s41598-019-53624-1 · Cited by 151
Epigenetic programming of the neuroendocrine stress response by adult life stress
Dirven, B. C. J., Homberg, J. R., Kozicz, T., & Henckens, M. J. A. G. (2017) · Journal of Molecular Endocrinology · doi:10.1530/jme-17-0019 · Cited by 135
Alterations in Reward, Fear and Safety Cue Discrimination after Inactivation of the Rat Prelimbic and Infralimbic Cortices
Sangha, S., Robinson, P. D., Greba, Q., Davies, D. A., & Howland, J. G. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.89 · Cited by 135
“Cue-triggered effects on fear and reward behavior were assessed as follows (Morrow et al, 2011; Pecina et al, 2006).”
Opioid reward ‘liking’ and ‘wanting’ in the nucleus accumbens
Peciña, S. (2008) · Physiology & Behavior · doi:10.1016/j.physbeh.2008.04.006 · Cited by 132
Self-citation
CRF1 receptor antagonists attenuate escalated cocaine self-administration in rats
Specio, S. E., Wee, S., O’Dell, L. E., Boutrel, B., Zorrilla, E. P., & Koob, G. F. (2007) · Psychopharmacology · doi:10.1007/s00213-007-0983-9 · Cited by 132
Corticotropin-releasing factor 1 and 2 receptors in the dorsal raphé differentially affect serotonin release in the nucleus accumbens
Lukkes, J. L., Forster, G. L., Renner, K. J., & Summers, C. H. (2007) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2007.09.024 · Cited by 126
The Incentive-Sensitization Theory of Addiction 30 Years On
Robinson, T. E., & Berridge, K. C. (2024) · Annual Review of Psychology · doi:10.1146/annurev-psych-011624-024031 · Cited by 146
Self-citation
Initial uncertainty in Pavlovian reward prediction persistently elevates incentive salience and extends sign-tracking to normally unattractive cues
Robinson, M. J. F., Anselme, P., Fischer, A. M., & Berridge, K. C. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.03.004 · Cited by 123
Self-citation
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
Learning and Motivational Processes Contributing to Pavlovian–Instrumental Transfer and Their Neural Bases: Dopamine and Beyond
Corbit, L. H., & Balleine, B. W. (2015) · Current topics in behavioral neurosciences · doi:10.1007/7854_2015_388 · Cited by 118
From Stress to Anhedonia: Molecular Processes through Functional Circuits
Stanton, C. H., Holmes, A. J., Chang, S. W. C., & Joormann, J. (2018) · Trends in Neurosciences · doi:10.1016/j.tins.2018.09.008 · Cited by 128
Stress effects on the neural substrates of motivated behavior
Hollon, N. G., Burgeno, L. M., & Phillips, P. E. M. (2015) · Nature Neuroscience · doi:10.1038/nn.4114 · Cited by 129
Striatal dopamine D2/3 receptor-mediated neurotransmission in major depression: Implications for anhedonia, anxiety and treatment response
Peciña, M., Sikora, M., Avery, E. T., Heffernan, J., Peciña, S., Mickey, B. J., & Zubieta, J.-K. (2017) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2017.08.427 · Cited by 125
“Furthermore, CRF injections in NAc shell have shown to amplify positive motivation for cued rewards, in particular by magnifying incentive salience (Pecina et al., 2006).”
Self-citation
Effects of stress on dietary preference and intake are dependent on access and stress sensitivity
Teegarden, S. L., & Bale, T. L. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.11.030 · Cited by 115
Plasticity of the Reward Circuitry After Early-Life Adversity: Mechanisms and Significance
Birnie, M. T., Kooiker, C. L., Short, A. K., Bolton, J. L., Chen, Y., & Baram, T. Z. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.12.018 · Cited by 123
Brain mechanisms mediating effects of stress on reward sensitivity
Ironside, M., Kumar, P., Kang, M. S., & Pizzagalli, D. A. (2018) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2018.01.016 · Cited by 110
“Novel molecular targets Although corticotropin release factor (CRF) has been traditionally associated with behavioral and physiological responses to stress, recent data indicate that CRF release in the NAc plays a key role in potentiating motivation for cued rewards [32].”
Abundance and co‐occurrence patterns of core and satellite species of ground beetles on small lake islands
Ulrich, W., & Zalewski, M. (2006) · Oikos · doi:10.1111/j.2006.0030-1299.14773.x · Cited by 103
How foraging works: Uncertainty magnifies food-seeking motivation
Anselme, P., & Güntürkün, O. (2018) · Behavioral and Brain Sciences · doi:10.1017/s0140525x18000948 · Cited by 109
Psychological and neural mechanisms of relapse
Stewart, J. (2008) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2008.0084 · Cited by 113
“…responses to stress including fear and anxiety (Schulkin et al. 2005; Davis 2006); in addition, CRF has been shown to facilitate locomotor activity (Kalivas et al. 1987; Cador et al. 1993) and responses to positive incentive stimuli (Pecina et al. 2006), responses involved in appetitive behaviour.”
Neurogenetics of depression: A focus on reward processing and stress sensitivity
Bogdan, R., Nikolova, Y. S., & Pizzagalli, D. A. (2012) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.05.007 · Cited by 114
“Accumulating research suggests that genetic differences conferring relatively increased subcortical DA or reduced cortical DA signaling (via either receptor availability or synaptic clearance) are associated with enhanced reward-related neural activation and behavior.”
Inducing Negative Affect Increases the Reward Value of Appetizing Foods in Dieters
Wagner, D. D., Boswell, R. G., Kelley, W. M., & Heatherton, T. F. (2012) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00238 · Cited by 95
“This study investigated the hypothesis, derived from animal models of drug addiction, that emotional distress sensitizes the brainʼs reward system to appetitive stimuli (e.g., Sinha, 2001; Piazza & Le Moal, 1996, 1998 ) and their cues (e.g., Peciña et al., 2006).”
Prefrontal Norepinephrine Determines Attribution of “High” Motivational Salience
Ventura, R., Latagliata, E. C., Morrone, C., Mela, I. L., & Puglisi‐Allegra, S. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003044 · Cited by 94
Negative affect and neural response to palatable food intake in bulimia nervosa
Bohon, C., & Stice, E. M. (2012) · Appetite · doi:10.1016/j.appet.2012.02.051 · Cited by 92
Anhedonia, Hyperkatifeia, and Negative Reinforcement in Substance Use Disorders
Koob, G. F. (2022) · Current topics in behavioral neurosciences · doi:10.1007/7854_2021_288 · Cited by 92
PRECLINICAL STUDY: Corticotropin‐releasing factor‐1 receptor antagonists decrease heroin self‐administration in long‐ but not short‐access rats
Greenwell, T. N., Funk, C. K., Cottone, P., Richardson, H. N., Chen, S. A., Rice, K. C., Zorrilla, E. P., & Koob, G. F. (2009) · Addiction Biology · doi:10.1111/j.1369-1600.2008.00142.x · Cited by 87
Corticotropin-Releasing Factor Within the Central Nucleus of the Amygdala and the Nucleus Accumbens Shell Mediates the Negative Affective State of Nicotine Withdrawal in Rats
Marcinkiewcz, C. A., Prado, M., Isaac, S. K., Marshall, S. A., Rylkova, D., & Bruijnzeel, A. W. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2008.231 · Cited by 89
Stress increases cue-triggered “wanting” for sweet reward in humans.
Pool, E. R., Brosch, T., Delplanque, S., & Sander, D. (2014) · Journal of Experimental Psychology Animal Learning and Cognition · doi:10.1037/xan0000052 · Cited by 84
Is comfort food really comforting? Mechanisms underlying stress-induced eating
Pool, E. R., Delplanque, S., Coppin, G., & Sander, D. (2015) · Food Research International · doi:10.1016/j.foodres.2014.12.034 · Cited by 87
“Peciña et al. (2006) demonstrated that pharmacologically induced stress has consequences for rodent behavior that are similar to those of increased mesolimbic dopaminergic activity.”
An acute psychosocial stress enhances the neural response to smoking cues
Dagher, A., Tannenbaum, B., Hayashi, T., Pruessner, J. C., & McBride, D. (2009) · Brain Research · doi:10.1016/j.brainres.2009.07.048 · Cited by 80
Cortisol administration induces global down-regulation of the brain's reward circuitry
Montoya, E. R., Bos, P. A., Terburg, D., Rosenberger, L. A., & van Honk, J. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.04.022 · Cited by 80
Neural correlates of Pavlovian-to-instrumental transfer in the nucleus accumbens shell are selectively potentiated following cocaine self-administration
Saddoris, M. P., Stamatakis, A. M., & Carelli, R. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07683.x · Cited by 84
Stress-induced eating in women with binge-eating disorder and obesity
Klatzkin, R. R., Gaffney, S., Cyrus, K., Bigus, E., & Brownley, K. A. (2016) · Biological Psychology · doi:10.1016/j.biopsycho.2016.11.002 · Cited by 88
Corticotropin-releasing factor in the nucleus accumbens shell induces swim depression, anxiety, and anhedonia along with changes in local dopamine/acetylcholine balance
Chen, Y.-W., Rada, P. V., Bützler, B. P., LEIBOWITZ, S. F., & Hoebel, B. G. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2011.12.009 · Cited by 78
Food-associated cues alter forebrain functional connectivity as assessed with immediate early gene and proenkephalin expression
Schiltz, C. A., Bremer, Q. Z., Landry, C. F., & Kelley, A. E. (2007) · BMC Biology · doi:10.1186/1741-7007-5-16 · Cited by 77
Dopamine D2/3- and μ-opioid receptor antagonists reduce cue-induced responding and reward impulsivity in humans
Weber, S. C., Beck‐Schimmer, B., Kajdi, M.-E., Müller, D., Tobler, P. N., & Quednow, B. B. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.113 · Cited by 76
Under the influence: Effects of adolescent ethanol exposure and anxiety on motivation for uncertain gambling-like cues in male and female rats
Hellberg, S. N., Levit, J. D., & Robinson, M. J. F. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.09.036 · Cited by 70
The α1 adrenergic receptor antagonist prazosin reduces heroin self-administration in rats with extended access to heroin administration
Greenwell, T. N., Walker, B. M., Cottone, P., Zorrilla, E. P., & Koob, G. F. (2008) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2008.07.012 · Cited by 69
Cued for Risk: Evidence for an Incentive Sensitization Framework to Explain the Interplay between Stress and Anxiety, Substance Abuse, and Reward Uncertainty in Disordered Gambling Behavior
Hellberg, S. N., Russell, T. I., & Robinson, M. J. F. (2019) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/s13415-018-00662-3 · Cited by 65
“In turn, administration of CRF has been shown to elevate the value of Pavlovian-associated reward cues (Peciña et al., 2006).”
An evolutionary medicine perspective on pain and its disorders
Nesse, R. M., & Schulkin, J. A. (2019) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2019.0288 · Cited by 76
Self-citation
The impact of mineralocorticoid receptor ISO/VAL genotype (rs5522) and stress on reward learning
Bogdan, R., Perlis, R. H., Fagerness, J. A., & Pizzagalli, D. A. (2010) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2010.00600.x · Cited by 70
Prefrontal/accumbal catecholamine system processes high motivational salience
Puglisi‐Allegra, S., & Ventura, R. (2012) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2012.00031 · Cited by 71
Activating Corticotropin-Releasing Factor Systems in the Nucleus Accumbens, Amygdala, and Bed Nucleus of Stria Terminalis: Incentive Motivation or Aversive Motivation?
Baumgartner, H. M., Schulkin, J. A., & Berridge, K. C. (2021) · Biological Psychiatry · doi:10.1016/j.biopsych.2021.01.007 · Cited by 63
Self-citation
Stress-induced plasticity of a CRH/GABA projection disrupts reward behaviors in mice
Birnie, M. T., Short, A. K., de Carvalho, G., Taniguchi, L., Gunn, B. G., Pham, A. L., Itoga, C. A., Xu, X., Chen, L. Y., Mahler, S. V., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-36780-x · Cited by 70
The evolving neurobiology of early-life stress
Birnie, M. T., & Baram, T. Z. (2025) · Neuron · doi:10.1016/j.neuron.2025.02.016 · Cited by 76
Social defeat stress and escalation of cocaine and alcohol consumption: Focus on CRF
Newman, E. L., Leonard, M. Z., Arena, D. T., de Almeida, R. M. M., & Miczek, K. A. (2018) · Neurobiology of Stress · doi:10.1016/j.ynstr.2018.09.007 · Cited by 70
Evidence for a compulsive-like behavior in rats exposed to alternate access to highly preferred palatable food
Rossetti, C., Spena, G., Halfon, O., & Boutrel, B. (2013) · Addiction Biology · doi:10.1111/adb.12065 · Cited by 62
Self-regulation and its failure: The seven deadly threats to self-regulation.
Wagner, D. D., & Heatherton, T. F. (2014) · American Psychological Association eBooks · doi:10.1037/14341-026 · Cited by 66
Neurodevelopmental origins of substance use disorders: Evidence from animal models of early‐life adversity and addiction
Levis, S. C., Baram, T. Z., & Mahler, S. V. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15223 · Cited by 63
New viral‐genetic mapping uncovers an enrichment of corticotropin‐releasing hormone‐expressing neuronal inputs to the nucleus accumbens from stress‐related brain regions
Itoga, C. A., Chen, Y., Fateri, C., Echeverry, P. A., Lai, J. M., Delgado, J., Badhon, S., Short, A. K., Baram, T. Z., & Xu, X. (2019) · The Journal of Comparative Neurology · doi:10.1002/cne.24676 · Cited by 61
Dopaminergic signaling of uncertainty and the aetiology of gambling addiction
Zack, M. H., George, R. S., & Clark, L. (2019) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2019.109853 · Cited by 62
Striatal Cholinergic Interneurons Are a Novel Target of Corticotropin Releasing Factor
Lemos, J. C., Shin, J. H., & Alvarez, V. A. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.0479-19.2019 · Cited by 59
Effects of acute stress on acquisition of nicotine conditioned place preference in adolescent rats: a role for corticotropin-releasing factor 1 receptors
Brielmaier, J., McDonald, C. G., & Smith, R. F. (2012) · Psychopharmacology · doi:10.1007/s00213-011-2378-1 · Cited by 54
The psychological science of addiction
Gifford, E. V., & Humphreys, K. N. (2007) · Addiction · doi:10.1111/j.1360-0443.2006.01706.x · Cited by 64
Evolutionary conservation of glucocorticoids and corticotropin releasing hormone: Behavioral and physiological adaptations
Schulkin, J. A. (2011) · Brain Research · doi:10.1016/j.brainres.2011.03.055 · Cited by 54
Self-citation
Food seeking in spite of harmful consequences is under prefrontal cortical noradrenergic control
Latagliata, E. C., Patrono, E., Puglisi‐Allegra, S., & Ventura, R. (2010) · BMC Neuroscience · doi:10.1186/1471-2202-11-15 · Cited by 48
Opposite effects of stress on effortful motivation in high and low anxiety are mediated by CRHR1 in the VTA
Zalachoras, I., Astori, S., Meijer, M., Grosse, J., Zanoletti, O., de Suduiraut, I. G., Deussing, J. M., & Sandi, C. (2022) · Science Advances · doi:10.1126/sciadv.abj9019 · Cited by 51
“In addition, previous work implicated CRHR1 actions in the NAc in appetitive behaviors ( 30 , 56 – 58 ), while CRHR1 actions in the VTA in deleterious motivational effects of acute stress ( 9 , 11 ).”
Knockdown of CRF1 Receptors in the Ventral Tegmental Area Attenuates Cue- and Acute Food Deprivation Stress-Induced Cocaine Seeking in Mice
Chen, N. A., Jupp, B., Sztainberg, Y., Lebow, M., Brown, R. M., Kim, J. H., Chen, A., & Lawrence, A. J. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.4763-12.2014 · Cited by 45
Metabotropic glutamate receptor blockade in nucleus accumbens shell shifts affective valence towards fear and disgust
Richard, J. M., & Berridge, K. C. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07553.x · Cited by 51
Self-citation
Differential representation of Pavlovian–instrumental transfer by prefrontal cortex subregions and striatum
Homayoun, H., & Moghaddam, B. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06679.x · Cited by 45
Investigating dopamine and glucocorticoid systems as underlying mechanisms of anhedonia
Lamontagne, S. J., Melendez, S. I., & Olmstead, M. C. (2018) · Psychopharmacology · doi:10.1007/s00213-018-5007-4 · Cited by 43
Angst and the amygdala
Schulkin, J. A. (2006) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2006.8.4/jschulkin · Cited by 39
Self-citation
Brain regulation of hunger and motivation: The case for integrating homeostatic and hedonic concepts and its implications for obesity and addiction
Morales, I. (2022) · Appetite · doi:10.1016/j.appet.2022.106146 · Cited by 39
Effects of electroconvulsive seizures on depression-related behavior, memory and neurochemical changes in Wistar and Wistar–Kyoto rats
Kyeremanteng, C., MacKay, J. C., James, J. S., Kent, P., Cayer, C., Anisman, H., & Merali, Z. (2014) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2014.05.012 · Cited by 37
A neuronal coping mechanism linking stress-induced anxiety to motivation for reward
Klenowski, P. M., Zhao-Shea, R., Freels, T. G., Molas, S., Zinter, M., M'angale, P. G., Xiao, C., Martínez‐Núñez, L., Thomson, T., & Tapper, A. R. (2023) · Science Advances · doi:10.1126/sciadv.adh9620 · Cited by 38
Separating desire from prediction of outcome value
Berridge, K. C. (2023) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2023.07.007 · Cited by 37
Self-citation

Authors: Peciña, S., Schulkin, J., & Berridge, K. C.
Affiliations: University of Michigan (US)
Georgetown University (US)
Corresponding author: Peciña, Susana
ORCID: Schulkin, Jay
Berridge, Kent C
Venue: BMC Biology
Publisher: Springer Science and Business Media LLC
Published: 2006-04-13
Volume: 4
Issue: 1
Pages: 8-8
ISSN: 1741-7007 (ISSN-L)
DOI: 10.1186/1741-7007-4-8
PMC: PMC1459217
OpenAlex: W1789705209
Cited by: 194
References: 64
Citations by year: 2026: 4 · 2025: 8 · 2024: 8 · 2023: 5 · 2022: 13 · 2021: 8 · 2020: 5 · 2019: 12 · 2018: 14 · 2017: 6 · 2016: 7 · 2015: 8 · 2014: 14 · 2013: 9 · 2012: 17
FWCI: 4.18
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
Locations: BMC Biology (publishedVersion, cc-by)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Deep Blue (University of Michigan) (submittedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders: National Institutes of Health
National Institute of Mental Health (MH-63649, R01MH063649)
National Institute on Drug Abuse (DA015188, R01DA015188)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
Keywords: corticotropin-releasing factor, nucleus accumbens shell, incentive salience, Pavlovian-to-instrumental transfer, sucrose reward, incentive motivation, stress, binge eating, amphetamine, reward cues
MeSH terms: Animals, Corticotropin-Releasing Hormone, Cues, Male, Microinjections, Motivation, Nucleus Accumbens, Reinforcement, Psychology, Reward, Stress, Physiological, Sucrose, Rats, Sprague-Dawley, Rats

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

Nucleus accumbens corticotropin-releasing factor increases cue-triggered motivation for sucrose reward: paradoxical positive incentive effects in stress?

Abstract

Overview

Integrity signals

Figures

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks