Safety Signals Mitigate the Consequences of Uncontrollable Stress Via a Circuit Involving the Sensory Insular Cortex and Bed Nucleus of the Stria Terminalis
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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.
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BLA inputs to the ventrolateral BNST promote freezing during uncontrollable stress and subsequent reduction in social interaction, both of which responses are reduced by inhibition of ventrolateral BNST.
“BLA inputs to the ventrolateral BNST promote freezing during uncontrollable stress and subsequent reduction in social interaction, both of which responses are reduced by inhibition of ventrolateral BNST86.”
From Resolving the neural circuits of anxiety (2015) · cites this paper as [86]
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Cites
The rat brain in stereotaxic coordinates
Palkovits, M. (1983) · Neuropeptides · doi:10.1016/0143-4179(83)90049-5 · Cited by 28,959 · see citing works
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
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 1,488 · see citing works
Conditional and unconditional components of post-shock freezing
Fanselow, M. S. (1980) · Pavlovian Journal of Biological Science · doi:10.1007/bf03001163 · Cited by 1,153 · see citing works
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 · see citing works
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 · see citing works
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 744 · see citing works
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 · see citing works
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 · see citing works
Changing Fear: The Neurocircuitry of Emotion Regulation
Hartley, C. A., & Phelps, E. A. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2009.121 · Cited by 492 · see citing works
Romanski, L. M., & LeDoux, J. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-11-04501.1992 · Cited by 461 · see citing works
Stress-induced enhancement of fear learning: An animal model of posttraumatic stress disorder
Rau, V., DeCola, J. P., & Fanselow, M. S. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.04.010 · Cited by 428 · see citing works
Synaptic correlates of fear extinction in the amygdala
Amano, T., Ünal, Ç. T., & Paré, D. (2010) · Nature Neuroscience · doi:10.1038/nn.2499 · Cited by 369 · see citing works
Sonnenberg, J. L., Mitchelmore, C., Macgregor-Leon, P. F., Hempstead, J. L., Morgan, J. I., & Curran, T. (1989) · Journal of Neuroscience Research · doi:10.1002/jnr.490240111 · Cited by 331 · see citing works
Jovanovic, T., Norrholm, S. D., Fennell, J. E., Keyes, M., Fiallos, A. M., Myers, K. M., Davis, M., & Duncan, E. J. (2009) · Psychiatry Research · doi:10.1016/j.psychres.2007.12.014 · Cited by 315 · see citing works
Cortical afferents to the extended amygdala
McDONALD, A. J., SHAMMAH‐LAGNADO, S. J., SHI, C., & DAVIS, M. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb09275.x · Cited by 306 · see citing works
Rogan, M. T., & LeDoux, J. E. (1995) · Neuron · doi:10.1016/0896-6273(95)90070-5 · Cited by 292 · see citing works
Pain Pathways Involved in Fear Conditioning Measured with Fear-Potentiated Startle: Lesion Studies
Shi, C., & Davis, M. E. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-01-00420.1999 · Cited by 282 · see citing works
Effects of coping behavior with and without a feedback signal on stress pathology in rats.
Weiss, J. M. (1971) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0031581 · Cited by 234 · see citing works
Distinct Neural Signatures for Safety and Danger in the Amygdala and Striatum of the Mouse
Rogan, M. T., Leon, K. S., Perez, D. L., & Kandel, E. R. (2005) · Neuron · doi:10.1016/j.neuron.2005.02.017 · Cited by 226 · see citing works
Christianson, J. P., Ragole, T., Amat, J., Greenwood, B. N., Strong, P. V., Paul, E. D., Fleshner, M., Watkins, L. R., & Maier, S. F. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.09.011 · Cited by 204 · see citing works
Self-citationMaier, S. F., Grahn, R. E., Kalman, B. A., Sutton, L. C., Wiertelak, E. P., & Watkins, L. R. (1993) · Behavioral Neuroscience · doi:10.1037//0735-7044.107.2.377 · Cited by 177 · see citing works
Self-citationAuditory, Somatosensory, and Multisensory Insular Cortex in the Rat
Rodgers, K. M., Benison, A. M., Klein, A., & Barth, D. S. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn054 · Cited by 163 · see citing works
Self-citationBaratta, M. V., Christianson, J. P., Gomez, D. M., Zarza, C. M., Amat, J., Masini, C. V., Watkins, L. R., & Maier, S. F. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.03.042 · Cited by 156 · see citing works
Self-citationOstroff, L. E., Cain, C. K., Bedont, J. L., Monfils, M., & LeDoux, J. E. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0913384107 · Cited by 154 · see citing works
Blanchard, R. J. (2008) · Handbook of behavioral neuroscience · doi:10.1016/s1569-7339(07)x0001-8 · Cited by 142 · see citing works
Maier, S. F., Grahn, R. E., Kalman, B. A., et al. (1993) · Behavioral Neuroscience · doi:10.1037/0735-7044.107.2.377 · Cited by 134 · see citing works
Self-citationHammack, S. E., Richey, K. J., Watkins, L. R., & Maier, S. F. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.2.443 · Cited by 130 · see citing works
Self-citationFear conditioned with escapable and inescapable shock: Effects of a feedback stimulus.
Mineka, S., Cook, M. C., & Miller, S. (1984) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.10.3.307 · Cited by 129 · see citing works
Christianson, J. P., Paul, E. D., Irani, M., Thompson, B. M., Kubala, K. H., Yirmiya, R., Watkins, L. R., & Maier, S. F. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.04.024 · Cited by 107 · see citing works
Self-citationChristianson, 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-citationChristianson, J. P., Thompson, B. M., Watkins, L. R., & Maier, S. F. (2008) · Stress · doi:10.1080/10253890802510302 · Cited by 87 · see citing works
Self-citationReznikov, L. R., Reagan, L. P., & Fadel, J. R. (2008) · The Journal of Comparative Neurology · doi:10.1002/cne.21687 · Cited by 65 · see citing works
Conditioned inhibition and the UCS-CS interval
Maier, S. F., Rapaport, P. M., & Wheatley, K. L. (1976) · Animal Learning & Behavior · doi:10.3758/bf03214039 · Cited by 54 · see citing works
Self-citationMinor, T. R., Trauner, M. A., Lee, C.-Y., & Dess, N. K. (1990) · Journal of Experimental Psychology: Animal Behavior Processes · doi:10.1037/0097-7403.16.2.123 · Cited by 37 · see citing works
Shock signals and the development of stress-induced analgesia.
Maier, S. F., & Keith, J. R. (1987) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.13.3.226 · Cited by 37 · see citing works
Self-citationGreenwood, B. N., Strong, P. V., & Fleshner, M. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.03.012 · Cited by 24 · see citing works
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Resolving the neural circuits of anxiety
Calhoon, G. G., & Tye, K. M. (2015) · Nature Neuroscience · doi:10.1038/nn.4101 · Cited by 766 · see citing works
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 · see citing works
Self-citationAversive 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 · see citing works
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 · see citing works
Self-citationInhibition of Fear by Learned Safety Signals: minisymposium review
Christianson, J. P., Fernando, A., Kazama, A. M., Jovanović, T., Ostroff, L. E., & Sangha, S. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.3340-12.2012 · Cited by 158 · see citing works
Self-citationNetwork 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 · see citing works
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 · see citing works
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 131 · see citing works
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 138 · see citing works
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 · see citing works
Self-citationMeyer, 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 118 · see citing works
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 113 · see citing works
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 · see citing works
Leussis, M. P., Freund, N., Brenhouse, H. C., Thompson, B. S., & Andersen, S. L. (2012) · Developmental Neuroscience · doi:10.1159/000339162 · Cited by 95 · see citing works
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 87 · see citing works
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 · see citing works
Self-citationOptogenetic 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 71 · see citing works
Self-citationArmario, 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 71 · see citing works
Odriozola, P., & Gee, D. G. (2021) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2020.20020232 · Cited by 62 · see citing works
McHenry, J. A., Rubinow, D. R., & Stuber, G. D. (2015) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2015.04.001 · Cited by 56 · see citing works
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 60 · see citing works
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 · see citing works
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 57 · see citing works
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 53 · see citing works
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 52 · see citing works
Self-citationPosterior insular cortex is necessary for conditioned inhibition of fear
Foilb, A. R., Flyer-Adams, J. G., Maier, S., & Christianson, J. P. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.08.004 · Cited by 49 · see citing works
Self-citationLaing, P., & Harrison, B. (2021) · Neuroscience and Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.05.014 · Cited by 37 · see citing works
Kazama, A. M., Heuer, E., Davis, M., & Bachevalier, J. (2012) · Behavioral Neuroscience · doi:10.1037/a0028241 · Cited by 42 · see citing works
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 43 · see citing works
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 42 · see citing works
Self-citationHazra, R., Guo, J. D., Dabrowska, J., & Rainnie, D. G. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.08.014 · Cited by 42 · see citing works
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 · see citing works
Self-citationCrosswell, 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 41 · see citing works
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 39 · see citing works
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 36 · see citing works
Self-citationCraig, A. D. B. (2018) · Handbook of clinical neurology · doi:10.1016/b978-0-444-63912-7.00019-9 · Cited by 37 · see citing works
Davis, M., & Walker, D. L. (2014) · Brain Structure and Function · doi:10.1007/s00429-013-0616-5 · Cited by 35 · see citing works
Cassaday, H., Muir, C., Stevenson, C., Bonardi, C., Hock, R., & Waite, L. (2023) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2023.107757 · Cited by 12 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 31 · see citing works
Self-citationPET 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 30 · see citing works
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 29 · see citing works
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 · see citing works
Smith, C. D., Piasecki, C. C., Weera, M. M., Olszewicz, J., & Lonstein, J. S. (2013) · Behavioral Neuroscience · doi:10.1037/a0032776 · Cited by 27 · see citing works
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 · see citing works
Self-citationToward 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 26 · see citing works
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 26 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Chen, V. M., Foilb, A. R., & Christianson, J. P. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.09.008 · Cited by 23 · see citing works
Self-citationHarris, N. A., & Winder, D. G. (2018) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.8b00169 · Cited by 22 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 21 · see citing works
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 · see citing works
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 · see citing works
Self-citationVitorio, 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 · see citing works
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 · see citing works
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 · see citing works
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 16 · see citing works
Self-citationTyler, 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 · see citing works
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 16 · see citing works
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 · see citing works
Self-citationBercum, 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 · see citing works
Kazama, A. M., Davis, M. E., & Bachevalier, J. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00037 · Cited by 15 · see citing works
Moaddab, M., Mangone, E., Ray, M. H., & McDannald, M. A. (2017) · Brain Sciences · doi:10.3390/brainsci7110151 · Cited by 14 · see citing works
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 · see citing works
Hefner, K. R., Verona, E., & Curtin, J. J. (2016) · Psychophysiology · doi:10.1111/psyp.12660 · Cited by 14 · see citing works
Muschalla, B. (2016) · Springer eBooks · doi:10.1007/978-3-319-32331-2_5 · Cited by 14 · see citing works
Research progress on the neural circuits mechanisms of anxiety
Gong, W. (2025) · Frontiers in Neural Circuits · doi:10.3389/fncir.2025.1609145 · Cited by 13 · see citing works
Kamada, T., & Hata, T. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.07.027 · Cited by 9 · see citing works
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 · see citing works
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 8 · see citing works
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 7 · see citing works
Muschalla, B. (2018) · Zeitschrift für Arbeits- und Organisationspsychologie A&O · doi:10.1026/0932-4089/a000271 · Cited by 7 · see citing works
Cho, H., Likhtik, E., & Dennis‐Tiwary, T. A. (2021) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-020-00855-9 · Cited by 7 · see citing works
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 · see citing works
Self-citationBed 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 6 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 4 · see citing works
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 · see citing works
Braun, K., Mannewitz, A., Bock, J., Kreitz, S., Heß, A., Scheich, H., & Goldschmidt, J. (2021) · Brain Sciences · doi:10.3390/brainsci11050659 · Cited by 1 · see citing works
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 · see citing works
Benson, A. A., & Gao, W. (2026) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2026.106762 · Cited by 1 · see citing works
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 · see citing works
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 · see citing works
Self-citationIntermittent 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 · see citing works
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 · see citing works
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 · see citing works
Effect of unexpected stressor duration on the expression of stress response habituation
Ramsey, R. E. (2011) · CU Scholar (University of Colorado Boulder)
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
Hefner, K. R., Verona, E., & Curtin, J. J. (2018) · 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)
- Venue
- Biological Psychiatry
- Publisher
- Elsevier BV
- Published
- 2011-09
- Volume
- 70
- Issue
- 5
- Pages
- 458-464
- ISSN
- 0006-3223 (ISSN-L)
- 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
- 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
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