Cited by 104Memory and Neural MechanismsStress Responses and CortisolNeurotransmitter Receptor Influence on Behavior

The DOI matches its Crossref record; 38 of the 38 references it cites were found in a registry or an index.

Safety Signals Mitigate the Consequences of Uncontrollable Stress Via a Circuit Involving the Sensory Insular Cortex and Bed Nucleus of the Stria Terminalis

Open access

Christianson, John P., Jennings, Joshua H., Ragole, Thomas, Flyer, Johana G.N., Benison, Alexander M., Barth, Daniel S., Watkins, Linda R., Maier, Steven F.·2011·Biological Psychiatry

DOI 10.1016/j.biopsych.2011.04.004PMC PMC3159417

Open this paper in CoChat — free account

Abstract

Background Safety signals exert a powerful buffering effect when provided during exposure to uncontrollable stressors. We evaluated the role of the sensory insular cortex (Si) and the extend amygdala in this "safety signal effect."Methods Rats were implanted with microinjection cannula, exposed to inescapable tailshocks either with or without a safety signal, and later tested for anxiety-like behavior or neuronal Fos expression.Results Exposure to the uncontrollable stressor reduced later social exploration but not when safety signals were present. Temporary inhibition of Si during stressor exposure but not during later behavioral testing blocked the safety signal effect on social exploration. The stressor induced Fos in all regions of the amygdala, but safety signals significantly reduced the number of Fos immunoreactive cells in the basolateral amygdala and ventrolateral region of the bed nucleus of the stria terminalis (BNSTlv). Inhibition of BNSTlv neuronal activity during uncontrollable stressor exposure prevented the later reduction in social exploration. Finally, safety signals reduced the time spent freezing during uncontrollable stress.Conclusions These data suggest that safety signals inhibit the neural fear or anxiety response that normally occurs during uncontrollable stressors and that inhibition of the BNSTlv is sufficient to prevent later anxiety. These data lend support to a growing body of evidence that chronic fear is mediated in the basolateral amygdala and BNSTlv and that environmental factors that modulate fear during stress will alter the long-term consequences of the stressor.

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 · 10.1016/j.biopsych.2011.04.004

Cites

38 of 38 references verified0 citation errors · 0 not checkable

Statistics

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
Phasic vs Sustained Fear in Rats and Humans: Role of the Extended Amygdala in Fear vs Anxiety
Davis, M., Walker, D. L., Miles, L., & Grillon, C. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.109 · Cited by 1,513
Conditional and unconditional components of post-shock freezing
Fanselow, M. S. (1980) · Pavlovian Journal of Biological Science · doi:10.1007/bf03001163 · Cited by 1,191
Dissociating pain from its anticipation in the human brain
Ploghaus, A., Tracey, I., Gati, J. S., Clare, S., Menon, R. S., Matthews, P. M., & Rawlins, J. N. P. (1999) · Science · doi:10.1126/science.284.5422.1979 · Cited by 1,151
Activation of the left amygdala to a cognitive representation of fear
Phelps, E. A., O'Connor, K. J., Gatenby, J. C., Gore, J. C., Grillon, C., & Davis, M. (2001) · Nature Neuroscience · doi:10.1038/86110 · Cited by 895
A review of 25 years of the social interaction test
File, S. E., & Seth, P. (2003) · European Journal of Pharmacology · doi:10.1016/s0014-2999(03)01273-1 · Cited by 763
Invited review c-Fos as a transcription factor: a stressful (re)view from a functional map
Kovács, K. J. (1998) · Neurochemistry International · doi:10.1016/s0197-0186(98)00023-0 · Cited by 740
Neural circuits and mechanisms involved in Pavlovian fear conditioning: A critical review
Kim, J. J., & Jung, M. W. (2006) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.06.005 · Cited by 636
Changing Fear: The Neurocircuitry of Emotion Regulation
Hartley, C. A., & Phelps, E. A. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2009.121 · Cited by 528

Show all 37 references

Sorted by citations

Resolving the neural circuits of anxiety
Calhoon, G. G., & Tye, K. M. (2015) · Nature Neuroscience · doi:10.1038/nn.4101 · Cited by 766
Distinct extended amygdala circuits for divergent motivational states
Jennings, J. H., Sparta, D. R., Stamatakis, A. M., Ung, R. L., Pleil, K. E., Kash, T. L., & Stuber, G. D. (2013) · Nature · doi:10.1038/nature12041 · Cited by 704
Self-citation
Aversive state processing in the posterior insular cortex
Gehrlach, D. A., Dolensek, N., Klein, A. S., Roy Chowdhury, R., Matthys, A., Junghänel, M., Gaitanos, T. N., Podgornik, A., Black, T. D., Reddy Vaka, N., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0469-1 · Cited by 303
Insular cortex mediates approach and avoidance responses to social affective stimuli
Rogers-Carter, M. M., Varela, J. A., Gribbons, K. B., Pierce, A. F., McGoey, M. T., Ritchey, M., & Christianson, J. P. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0071-y · Cited by 277
Self-citation
Inhibition of Fear by Learned Safety Signals: A Mini-Symposium Review
Christianson, J. P., Fernando, A. B. P., Kazama, A. M., Jovanović, T., Ostroff, L. E., & Sangha, S. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.3340-12.2012 · Cited by 178
Self-citation
Network Organization Unfolds over Time during Periods of Anxious Anticipation
McMenamin, B. W., Langeslag, S. J. E., Sirbu, M., Padmala, S., & Pessoa, L. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.1579-14.2014 · Cited by 140
The Insula: A “Hub of Activity” in Migraine
Borsook, D., Veggeberg, R., Erpelding, N., Borra, R., Linnman, C., Burstein, R., & Becerra, L. (2016) · The Neuroscientist · doi:10.1177/1073858415601369 · Cited by 146
Safety Encoding in the Basal Amygdala
Sangha, S., Chadick, J. Z., & Janak, P. H. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3302-12.2013 · Cited by 137
Role of the bed nucleus of the stria terminalis in aversive learning and memoryPreprint
Goode, T. D., & Maren, S. (2017) · Learning & Memory · doi:10.1101/lm.044206.116 · Cited by 149
An insular view of the social decision-making network
Rogers-Carter, M. M., & Christianson, J. P. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.06.005 · Cited by 121
Self-citation
Ventral hippocampus interacts with prelimbic cortex during inhibition of threat response via learned safety in both mice and humans
Meyer, H. C., Odriozola, P., Cohodes, E. M., Mandell, J. D., Li, A., Yang, R., Hall, B. S., Haberman, J. T., Zacharek, S. J., Liston, C. M., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1910481116 · Cited by 121
Bed nucleus of the stria terminalis regulates fear to unpredictable threat signals
Goode, T. D., Ressler, R. L., Acca, G. M., Miles, O. W., & Maren, S. (2019) · eLife · doi:10.7554/elife.46525 · Cited by 120
Learning not to Fear: Neural Correlates of Learned Safety
Kong, E., Monje, F. J., Hirsch, J., & Pollak, D. D. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2013.191 · Cited by 113
Depressive-Like Behavior in Adolescents after Maternal Separation: Sex Differences, Controllability, and GABA
Leussis, M. P., Freund, N., Brenhouse, H. C., Thompson, B. S., & Andersen, S. L. (2012) · Developmental Neuroscience · doi:10.1159/000339162 · Cited by 95
Negative childhood experiences alter a prefrontal‐insular‐motor cortical network in healthy adults: A preliminary multimodal rsfMRI‐fMRI‐MRS‐dMRI study
Duncan, N. W., Hayes, D. J., Wiebking, C., Tiret, B., Pietruska, K., Chen, D. Q., Rainville, P., Marjańska, M., Ayad, O., Doyon, J., et al. (2015) · Human Brain Mapping · doi:10.1002/hbm.22941 · Cited by 91
Insular cortex projections to nucleus accumbens core mediate social approach to stressed juvenile rats
Rogers-Carter, M. M., Djerdjaj, A., Gribbons, K. B., Varela, J. A., & Christianson, J. P. (2019) · The Journal of Neuroscience · doi:10.1523/jneurosci.0316-19.2019 · Cited by 79
Self-citation
Optogenetic strategies to investigate neural circuitry engaged by stress
Sparta, D. R., Jennings, J. H., Ung, R. L., & Stuber, G. D. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.05.007 · Cited by 72
Self-citation
What can We Know from Pituitary–Adrenal Hormones About the Nature and Consequences of Exposure to Emotional Stressors?
Armario, A., Daviu, N., Muñoz-Abellán, C., Rabasa, C., Fuentes, S., Belda, X., Gagliano, H., & Nadal, R. A. (2012) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-012-9814-6 · Cited by 76
Learning About Safety: Conditioned Inhibition as a Novel Approach to Fear Reduction Targeting the Developing Brain
Odriozola, P., & Gee, D. G. (2021) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2020.20020232 · Cited by 62
Maternally responsive neurons in the bed nucleus of the stria terminalis and medial preoptic area: Putative circuits for regulating anxiety and reward
McHenry, J. A., Rubinow, D. R., & Stuber, G. D. (2015) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2015.04.001 · Cited by 57
Affective touch and regulation of stress responses
Kidd, T., Devine, S. L., & Walker, S. C. (2022) · Health Psychology Review · doi:10.1080/17437199.2022.2143854 · Cited by 65
Adaptation of the hypothalamus–pituitary–adrenal axis to daily repeated stress does not follow the rules of habituation: A new perspective
Rabasa, C., Gagliano, H., Pastor‐Ciurana, J., Fuentes, S., Belda, X., Nadal, R. A., & Armario, A. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.06.013 · Cited by 59
Controllability over stressor decreases responses in key threat-related brain areas
Limbachia, C., Morrow, K., Khibovska, A., Meyer, C., Padmala, S., & Pessoa, L. (2021) · Communications Biology · doi:10.1038/s42003-020-01537-5 · Cited by 65
A role for the interoceptive insular cortex in the consolidation of learned fear
Casanova, J. P., Madrid, C., Contreras, M., Rodríguez, M., Vasquez, M., & Torrealba, F. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.08.032 · Cited by 55
Short- and long-term consequences of stressor controllability in adolescent rats
Kubala, K. H., Christianson, J. P., Kaufman, R. D., Watkins, L. R., & Maier, S. F. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.06.027 · Cited by 54
Self-citation
Posterior insular cortex is necessary for conditioned inhibition of fear
Foilb, A. R., Flyer-Adams, J. G., Maier, S. F., & Christianson, J. P. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.08.004 · Cited by 53
Self-citation
Safety learning and the Pavlovian conditioned inhibition of fear in humans: Current state and future directions
Laing, P. A. F., & Harrison, B. J. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.05.014 · Cited by 68
Effects of neonatal amygdala lesions on fear learning, conditioned inhibition, and extinction in adult macaques.
Kazama, A. M., Heuer, E., Davis, M. E., & Bachevalier, J. (2012) · Behavioral Neuroscience · doi:10.1037/a0028241 · Cited by 51
Neurochemical Signaling of Reward and Aversion to Ventral Tegmental Area Glutamate Neurons
McGovern, D. J., Polter, A. M., & Root, D. H. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.1419-20.2021 · Cited by 42
Stress-protective neural circuits: not all roads lead through the prefrontal cortex
Christianson, J. P., & Greenwood, B. N. (2013) · Stress · doi:10.3109/10253890.2013.794450 · Cited by 44
Self-citation
Differential distribution of serotonin receptor subtypes in BNSTALG neurons: Modulation by unpredictable shock stress
Hazra, R., Guo, J. D., Dabrowska, J., & Rainnie, D. G. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.08.014 · Cited by 42
Sex differences in fear discrimination do not manifest as differences in conditioned inhibitionPreprint
Foilb, A. R., Bals, J., Sarlitto, M. C., & Christianson, J. P. (2017) · Learning & Memory · doi:10.1101/lm.045500.117 · Cited by 42
Self-citation
Deep rest: An integrative model of how contemplative practices combat stress and enhance the body’s restorative capacity.
Crosswell, A. D., Mayer, S. E., Whitehurst, L. N., Picard, M. A., Zebarjadian, S., & Epel, E. S. (2023) · Psychological Review · doi:10.1037/rev0000453 · Cited by 50
Dopamine Rebound-Excitation Theory: Putting Brakes on PTSD
Lee, J. C., Wang, L. P., & Tsien, J. Z. (2016) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2016.00163 · Cited by 42
Inactivation of the Ventrolateral Orbitofrontal Cortex Impairs Flexible Use of Safety Signals
Sarlitto, M. C., Foilb, A. R., & Christianson, J. P. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.03.037 · Cited by 37
Self-citation
Central neural substrates involved in temperature discrimination, thermal pain, thermal comfort, and thermoregulatory behavior
Craig, A. D. B. (2018) · Handbook of clinical neurology · doi:10.1016/b978-0-444-63912-7.00019-9 · Cited by 37
Role of bed nucleus of the stria terminalis and amygdala AMPA receptors in the development and expression of context conditioning and sensitization of startle by prior shock
Davis, M., & Walker, D. L. (2014) · Brain Structure and Function · doi:10.1007/s00429-013-0616-5 · Cited by 35
From safety to frustration: The neural substrates of inhibitory learning in aversive and appetitive conditioning procedures
Cassaday, H. J., Muir, C., Stevenson, C. W., Bonardi, C., Hock, R. M., & Waite, L. J. (2023) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2023.107757 · Cited by 36
A prefrontal-bed nucleus of the stria terminalis circuit limits fear to uncertain threat
Glover, L. R., McFadden, K. M., Bjorni, M., Smith, S. R., Rovero, N. G., Oreizi-Esfahani, S., Yoshida, T., Postle, A. F., Nonaka, M., Halladay, L. R., et al. (2020) · eLife · doi:10.7554/elife.60812 · Cited by 35
Individual differences in behavioral and cardiovascular reactivity to emotive stimuli and their relationship to cognitive flexibility in a primate model of trait anxiety
Shiba, Y., Santangelo, A. M., Braesicke, K., Agustín‐Pavón, C., Cockcroft, G. J., Haggard, M. P., & Roberts, A. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00137 · Cited by 31
Brain c-fos expression patterns induced by emotional stressors differing in nature and intensity
Úbeda-Contreras, J., Marin‐Blasco, I., Nadal, R. A., & Armario, A. (2018) · Brain Structure and Function · doi:10.1007/s00429-018-1624-2 · Cited by 31
Maternal Stress Combined with Terbutaline Leads to Comorbid Autistic-Like Behavior and Epilepsy in a Rat Model
Bercum, F. M., Rodgers, K. M., Benison, A. M., Smith, Z. Z., Taylor, J. A., Brunsgaard, E. K., Grabenstatter, H. L., Dudek, F. E., & Barth, D. S. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.2803-15.2015 · Cited by 33
Self-citation
PET Mapping of Neurofunctional Changes in a Posttraumatic Stress Disorder Model
Zhu, Y., Du, R., Zhu, Y., Shen, Y., Zhang, K., Chen, Y., Song, F., Wu, S., Zhang, H., & Tian, M. (2016) · Journal of Nuclear Medicine · doi:10.2967/jnumed.116.173443 · Cited by 31
Widespread Pressure Delivered by a Weighted Blanket Reduces Chronic Pain: A Randomized Controlled Trial
Baumgartner, J. N., Quintana, D., Leija, L., Schuster, N. M., Bruno, K. A., Castellanos, J. P., & Case, L. K. (2021) · Journal of Pain · doi:10.1016/j.jpain.2021.07.009 · Cited by 33
Evolution of stress responses refine mechanisms of social rank
Korzan, W. J., & Summers, C. H. (2021) · Neurobiology of Stress · doi:10.1016/j.ynstr.2021.100328 · Cited by 30
Noradrenergic alpha-2 receptor modulators in the ventral bed nucleus of the stria terminalis: Effects on anxiety behavior in postpartum and virgin female rats.
Smith, C. D., Piasecki, C. C., Weera, M. M., Olszewicz, J., & Lonstein, J. S. (2013) · Behavioral Neuroscience · doi:10.1037/a0032776 · Cited by 27
Active behavioral coping alters the behavioral but not the endocrine response to stress
Helmreich, D. L., Tylee, D., Christianson, J. P., Kubala, K. H., Govindarajan, S. T., O’Neill, W. E., Becoats, K., Watkins, L., & Maier, S. F. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.04.005 · Cited by 27
Self-citation
Toward a systems-oriented approach to the role of the extended amygdala in adaptive responding
Waraczynski, M. A. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.05.015 · Cited by 28
Neural correlates of appetitive–aversive interactions in Pavlovian fear conditioningPreprint
Nasser, H. M., & McNally, G. P. (2013) · Learning & Memory · doi:10.1101/lm.029744.112 · Cited by 28
Anticipation and violated expectation of pain are influenced by trait rumination: An fMRI study
Kökönyei, G., Galambos, A., Édes, A. E., Kocsel, N., Szabó, E., Pap, D., Kozák, L. R., Bagdy, G., & Juhász, G. (2018) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-018-0644-y · Cited by 24
Deciphering Memory Function with Optogenetics
Beyeler, A., Eckhardt, C. A., & Tye, K. M. (2014) · Progress in molecular biology and translational science · doi:10.1016/b978-0-12-420170-5.00012-x · Cited by 24
Early adversity disrupts the adult use of aversive prediction errors to reduce fear in uncertainty
Wright, K. M., DiLeo, A., & McDannald, M. A. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00227 · Cited by 23
Inactivation of ventral hippocampus interfered with cued-fear acquisition but did not influence later recall or discrimination
Chen, V. M., Foilb, A. R., & Christianson, J. P. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.09.008 · Cited by 27
Self-citation
Synaptic Plasticity in the Bed Nucleus of the Stria Terminalis: Underlying Mechanisms and Potential Ramifications for Reinstatement of Drug- and Alcohol-Seeking Behaviors
Harris, N. A., & Winder, D. G. (2018) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.8b00169 · Cited by 22
A role for miR-132 in learned safety
Ronovsky, M., Zambon, A., Cicvaric, A., Boehm, V., Hoesel, B., Moser, B. A., Yang, J., Schmid, J. A., Haubensak, W. E., Monje, F. J., et al. (2019) · Scientific Reports · doi:10.1038/s41598-018-37054-z · Cited by 22
Environmental certainty influences the neural systems regulating responses to threat and stress
Meyer, H. C., Sangha, S., Radley, J. J., LaLumiere, R. T., & Baratta, M. V. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.10.014 · Cited by 20
Different neural circuitry is involved in physiological and psychological stress-induced PTSD-like “nightmares” in rats
Yu, B., Cui, S., Zhang, X., Cui, X., Li, S., Sheng, Z., Cao, Q., Huang, Y., Xu, Y.-P., Lin, Z.-X., et al. (2015) · Scientific Reports · doi:10.1038/srep15976 · Cited by 21
An unexpected increase in restraint duration alters the expression of stress response habituation
Kearns, R., & Spencer, R. L. (2013) · Physiology & Behavior · doi:10.1016/j.physbeh.2013.03.029 · Cited by 23
Distributed and Multifaceted Effects of Threat and Safety
Morrow, K., Murty, D. V. P. S., Kim, J., Song, S., Hu, K., & Pessoa, L. (2021) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_01807 · Cited by 18
Serotonin 2C receptor antagonist improves fear discrimination and subsequent safety signal recall
Foilb, A. R., & Christianson, J. P. (2015) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2015.08.017 · Cited by 19
Self-citation
Evaluation of the posterior insular cortex involvement in anxiogenic response to emotional stress in male rats: Functional topography along the rostrocaudal axis
Vitorio, A. S., Reis‐Silva, L. L., Barretto‐de‐Souza, L., Gomes‐de‐Souza, L., & Crestani, C. C. (2022) · Physiology & Behavior · doi:10.1016/j.physbeh.2022.114006 · Cited by 17
Insular muscarinic signaling regulates anxiety-like behaviors in rats on the elevated plus-maze
Li, H., Chen, L., Li, P., Wang, X., & Zhai, H. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.05.017 · Cited by 17
Potential of microRNAs as novel targets in the alleviation of pathological fear
Murphy, C. P., & Singewald, N. (2017) · Genes Brain & Behavior · doi:10.1111/gbb.12427 · Cited by 18
Functional networks activated by controllable and uncontrollable stress in male and female rats
Worley, N. B., Everett, S., Foilb, A. R., & Christianson, J. P. (2020) · Neurobiology of Stress · doi:10.1016/j.ynstr.2020.100233 · Cited by 17
Self-citation
The effects of predator odor (TMT) exposure and mGlu 3 NAM pretreatment on lasting behavioral and molecular adaptations in the insular cortex and BNST
Tyler, R. E., Bluitt, M. N., Engers, J. L., Lindsley, C. W., & Besheer, J. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2022.108943 · Cited by 17
Cortico-Striatal Activity Characterizes Human Safety Learning via Pavlovian Conditioned Inhibition
Laing, P. A. F., Steward, T., Davey, C. G., Felmingham, K. L., Fullana, M. A., Vervliet, B., Greaves, M. D., Moffat, B. A., Glarin, R. K., & Harrison, B. J. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.2181-21.2022 · Cited by 17
Neural correlates of safety learning
Foilb, A. R., Sansaricq, G., Zona, E. E., Fernando, K., & Christianson, J. P. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.112884 · Cited by 16
Self-citation
Elevated fear responses to threatening cues in rats with early life stress is associated with greater excitability and loss of gamma oscillations in ventral-medial prefrontal cortex
Bercum, F. M., Gomez, M. J. N., & Saddoris, M. P. (2021) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2021.107541 · Cited by 15
Neonatal lesions of orbital frontal areas 11/13 in monkeys alter goal-directed behavior but spare fear conditioning and safety signal learning
Kazama, A. M., Davis, M. E., & Bachevalier, J. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00037 · Cited by 15
Adolescent Alcohol Drinking Renders Adult Drinking BLA-Dependent: BLA Hyper-Activity as Contributor to Comorbid Alcohol Use Disorder and Anxiety Disorders
Moaddab, M., Mangone, E., Ray, M. H., & McDannald, M. A. (2017) · Brain Sciences · doi:10.3390/brainsci7110151 · Cited by 14
ITI-Signals and Prelimbic Cortex Facilitate Avoidance Acquisition and Reduce Avoidance Latencies, Respectively, in Male WKY Rats
Beck, K. D., Jiao, X., Smith, I. M., Myers, C. E., Pang, K. C. H., & Servatius, R. J. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00403 · Cited by 14
Emotion regulation during threat: Parsing the time course and consequences of safety signal processing
Hefner, K. R., Verona, E., & Curtin, J. J. (2016) · Psychophysiology · doi:10.1111/psyp.12660 · Cited by 14
Work-Related Anxieties and Work-Place Phobia: A Topical Phenomenon at the Interface of Clinical and Organizational Research and Practice
Muschalla, B. (2016) · Springer eBooks · doi:10.1007/978-3-319-32331-2_5 · Cited by 14
Research progress on the neural circuits mechanisms of anxiety
Gong, W. (2025) · Frontiers in Neural Circuits · doi:10.3389/fncir.2025.1609145 · Cited by 18
Basolateral amygdala inactivation eliminates fear-induced underestimation of time in a temporal bisection task
Kamada, T., & Hata, T. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.07.027 · Cited by 9
The Role of the Medial Prefrontal Cortex in Spatial Margin of Safety Calculations
Qi, S., Cross, L., Wise, T., Sui, X., O’Doherty, J. P., & Mobbs, D. (2024) · Journal of Neuroscience · doi:10.1523/jneurosci.1162-22.2024 · Cited by 9
Social Transfer of Fear in Rodents
Kondrakiewicz, K., Rokosz, K., Nikolaev, T., Górkiewicz, T., Danielewski, K., Gruszczyńska, A., Meyza, K. Z., & Knapska, E. (2019) · Current Protocols in Neuroscience · doi:10.1002/cpns.85 · Cited by 9
Plasticity in the Interoceptive System
Torrealba, F., Madrid, C., Contreras, M., & Gómez, K. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-62817-2_4 · Cited by 8
Work Ability Impairment and Facets of Workplace Perception Are Predictive of Sick Leave Duration in Persons With Work Anxiety
Muschalla, B. (2018) · Zeitschrift für Arbeits- und Organisationspsychologie A&O · doi:10.1026/0932-4089/a000271 · Cited by 7
Absence Makes the Mind Grow Fonder: Reconceptualizing Studies of Safety Learning in Translational Research on Anxiety
Cho, H., Likhtik, E., & Dennis‐Tiwary, T. A. (2021) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-020-00855-9 · Cited by 7
Brain Mechanisms for Learning and Using Safety Signals
Foilb, A. R., & Christianson, J. P. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-813693-5.00011-3 · Cited by 7
Self-citation
Bed nucleus of the stria terminalis regulates fear to unpredictable threat signalsPreprint
Goode, T. D., Ressler, R. L., Acca, G. M., Miles, O. W., & Maren, S. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/376228 · Cited by 8
The Role of the Medial Prefrontal Cortex in Spatial Margin of Safety CalculationsPreprint
Qi, S., Cross, L., Wise, T., Sui, X., O’Doherty, J. P., & Mobbs, D. (2021) · Research Square · doi:10.21203/rs.3.rs-132967/v1 · Cited by 7
Emerging Roles of GluN3B NMDA Receptor Subunit in the Central Nervous System
Huang, Y., Xie, J., Chen, J., Guo, S., Li, Y., & Liu, F. (2025) · Neuroscience Bulletin · doi:10.1007/s12264-025-01523-z · Cited by 3
Arbeitsbezogene Ängste in Forschung und Praxis
Muschalla, B. (2014) · Zeitschrift für Arbeits- und Organisationspsychologie A&O · doi:10.1026/0932-4089/a000166 · Cited by 3
Adaptive Homeostatic Strategies of Resilient Intrinsic Self-Regulation in Extremes (RISE): A Randomized Controlled Trial of a Novel Behavioral Treatment for Chronic Pain
Kent, M., Mardian, A. S., Hustead, M. L.-R., Gress‐Smith, J. L., Ciciolla, L. M., Kim, J. L., & Scott, B. A. (2021) · Frontiers in Psychology · doi:10.3389/fpsyg.2021.613341 · Cited by 5
The Role of the Medial Prefrontal Cortex in Spatial Margin of Safety CalculationsPreprint
Qi, S., Cross, L., Wise, T., Sui, X., O’Doherty, J. P., & Mobbs, D. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.06.05.137075 · Cited by 3
Imaging of Functional Brain Circuits during Acquisition and Memory Retrieval in an Aversive Feedback Learning Task: Single Photon Emission Computed Tomography of Regional Cerebral Blood Flow in Freely Behaving Rats
Braun, K., Mannewitz, A., Bock, J., Kreitz, S., Heß, A., Scheich, H., & Goldschmidt, J. (2021) · Brain Sciences · doi:10.3390/brainsci11050659 · Cited by 1
The neurobehavioral impact of stress and the therapeutic role of valproic acid in a PTSD animal model
Hajghani, M. S., Sabzalizadeh, M., Shamsara, A., Taherh, H., Haghani, M., Arabpour, A. A., Farhadi, M., & Afarinesh, M. R. (2025) · Brain Research · doi:10.1016/j.brainres.2025.149922 · Cited by 1
Integrating anxiety and motivation: Prefrontal mechanisms arbitrating the approach-avoidance conflict
Benson, A. A., & Gao, W. (2026) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2026.106762 · Cited by 2
Corticotropin-releasing factor neurotransmission in the insular cortex regulates anxiogenic-like behavior to acute restraint stress: A site-specific study in rats
Reis‐Silva, L. L., Tomeo, R. A., Barretto‐de‐Souza, L., Gomes‐de‐Souza, L., Vitorio, A. S., Santos, A., Nunes‐de‐Souza, R. L., & Crestani, C. C. (2026) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2026.107986 · Cited by 1
Comparative insights into insula structure and function
Charbonneau, J. A., Carp, S. B., Bennett, J. L., Maw, S. M., Moadab, G., Christianson, J. P., Baxter, M. G., & Bliss‐Moreau, E. (2026) · Nature Neuroscience · doi:10.1038/s41593-026-02380-3 · Cited by 1
Self-citation
Intermittent swim stress effects on anxiety behavior
Warner, T. A. (2013) · University of New Hampshire Scholars Repository (University of New Hampshire at Manchester) · Cited by 1
Avanços na compreensão das bases neurais da regulação emocional – Revisão narrativa
Silva, W. D. S. (2024) · Research Society and Development · doi:10.33448/rsd-v13i8.46553 · Cited by 1
Arbeitsbezogene Ängste in Forschung und Praxis: ein aktuelles Schnittstellenphänomen
Muschalla, B. (2014) · Digitale Bibliothek Braunschweig (Verbundzentrale Göttingen (VZG)) · doi:10.24355/dbbs.084-201907181316-0 · Cited by 1
Effect of unexpected stressor duration on the expression of stress response habituation
Ramsey, R. E. (2011) · CU Scholar (University of Colorado Boulder)
Levels of Perineuronal Nets in the Basolateral Amygdala Are Correlated with Sex Differences in Fear Learning
Bals, J. (2017)
Kainate receptor auxiliary subunits NETO1 and NETO2 in anxiety and fear-related behaviors
Mennesson, M. (2019) · Työväentutkimus Vuosikirja
Faculty Opinions recommendation of Safety encoding in the basal amygdala.
Seymour, B., & Mano, H. (2013) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.717988886.793472789
Preprint: Emotion regulation during threat: Parsing the time course and consequences of safety signal processingPreprint
Hefner, K. R., Verona, E., & Curtin, J. J. (2018) · PsyArXiv (OSF Preprints) · doi:10.31234/osf.io/62sbm

Authors: Christianson, J. P., Jennings, J. H., Ragole, T., Flyer, J. G. N., Benison, A. M., Barth, D. S., Watkins, L. R., & Maier, S. F.
Affiliations: University of Colorado Boulder (US)
ORCID: Christianson, John P.
Barth, Daniel S.
Watkins, Linda R.
Maier, Steven F.
Venue: Biological Psychiatry
Publisher: Elsevier BV
Published: 2011-09
Volume: 70
Issue: 5
Pages: 458-464
ISSN: 0006-3223 (ISSN-L)
DOI: 10.1016/j.biopsych.2011.04.004
PMC: PMC3159417
OpenAlex: W2049738669
Cited by: 104
References: 37
Citations by year: 2026: 4 · 2025: 3 · 2024: 3 · 2023: 3 · 2022: 4 · 2021: 13 · 2020: 5 · 2019: 8 · 2018: 11 · 2017: 6 · 2016: 6 · 2015: 11 · 2014: 8 · 2013: 11 · 2012: 7
FWCI: 4.38
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Biological Psychiatry (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Mental Health (MH050479, MH082453)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords: safety signals, uncontrollable stress, bed nucleus of the stria terminalis, basolateral amygdala, Fos expression, anxiety-like behavior, social exploration, freezing behavior, fear response, stress buffering
MeSH terms: Amygdala, Animals, Brain Mapping, Cerebral Cortex, Cues, Electric Stimulation, Fear, Male, Microinjections, Muscimol, Neural Pathways, Septal Nuclei, Social Behavior, Stress, Psychological, Tetrodotoxin, Rats, Sprague-Dawley, Immobility Response, Tonic, 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

Safety Signals Mitigate the Consequences of Uncontrollable Stress Via a Circuit Involving the Sensory Insular Cortex and Bed Nucleus of the Stria Terminalis

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks