Sensitive periods in affective development: nonlinear maturation of fear learning
Open accessAbstract
At specific maturational stages, neural circuits enter sensitive periods of heightened plasticity, during which the development of both brain and behavior are highly receptive to particular experiential information. A relatively advanced understanding of the regulatory mechanisms governing the initiation, closure, and reinstatement of sensitive period plasticity has emerged from extensive research examining the development of the visual system. In this article, we discuss a large body of work characterizing the pronounced nonlinear changes in fear learning and extinction that occur from childhood through adulthood, and their underlying neural substrates. We draw upon the model of sensitive period regulation within the visual system, and present burgeoning evidence suggesting that parallel mechanisms may regulate the qualitative changes in fear learning across development.
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
Cites
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?
There is still a consensus that the amygdala, hippocampus, vmPFC, and ACC are central to fear learning and, especially, fear extinction.
“there is still a consensus that the Am, Hip, vmPFC, and ACC are central to fear learning [review in Ref. (193, 194)] and, especially, fear extinction [reviews in Ref. (187, 188, 195)].”
From The Stress Acceleration Hypothesis of Nightmares (2017) · cites this paper as [187]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Kessler, R. C., Berglund, P., Demler, O., Jin, R., Merikangas, K. R., & Walters, E. E. (2005) · Archives of General Psychiatry · doi:10.1001/archpsyc.62.6.593 · Cited by 20,391 · see citing works
Effects of stress throughout the lifespan on the brain, behaviour and cognition
Lupien, S. J., McEwen, B. S., Gunnar, M. R., & Heim, C. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2639 · Cited by 6,256 · see citing works
Dynamic mapping of human cortical development during childhood through early adulthood
Gogtay, N., Giedd, J. N., Lusk, L., Hayashi, K. M., Greenstein, D., Vaituzis, A. C., Nugent, T. F., Herman, D. H., Clasen, L. S., Toga, A. W., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0402680101 · Cited by 5,604 · see citing works
The adolescent brain and age-related behavioral manifestations
Spear, L. P. (2000) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(00)00014-2 · Cited by 5,433 · see citing works
The reward circuit: linking primate anatomy and human imaging
Haber, S. N., & Knutson, B. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.129 · Cited by 3,718 · see citing works
Contributions of the Amygdala to Emotion Processing: From Animal Models to Human Behavior
Phelps, E. A., & LeDoux, J. E. (2005) · Neuron · doi:10.1016/j.neuron.2005.09.025 · Cited by 3,203 · see citing works
Modality-Specific Retrograde Amnesia of Fear
Kim, J. J., & Fanselow, M. S. (1992) · Science · doi:10.1126/science.1585183 · Cited by 2,483 · see citing works
Critical period plasticity in local cortical circuits
Hensch, T. K. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1787 · Cited by 2,323 · see citing works
Regional Development of the Brain in Early Life
(1968) · Archives of Disease in Childhood · doi:10.1136/adc.43.229.388 · Cited by 2,107 · see citing works
Brain development in children and adolescents: Insights from anatomical magnetic resonance imaging
Lenroot, R. K., & Giedd, J. N. (2006) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2006.06.001 · Cited by 1,863 · see citing works
Sensitive periods in the development of the brain and behavior
Knudsen, E. I. (2004) · Journal of Cognitive Neuroscience · doi:10.1162/0898929042304796 · Cited by 1,842 · see citing works
Neurons in medial prefrontal cortex signal memory for fear extinction
Milad, M. R., & Quirk, G. J. (2002) · Nature · doi:10.1038/nature01138 · Cited by 1,836 · cited 1× · see citing works
“Following extinction training, presentation of the CS evokes activity within IL neurons that is associated with reduced conditioned fear expression (Milad and Quirk, 2002).”
BackgroundContext and Behavioral Processes in Extinction: Table 1.
Bouton, M. E. (2004) · Learning & Memory · doi:10.1101/lm.78804 · Cited by 1,808 · see citing works
Phelps, E. A., Delgado, M. R., Nearing, K. I., & LeDoux, J. E. (2004) · Neuron · doi:10.1016/j.neuron.2004.08.042 · Cited by 1,753 · see citing works
Chambers, R. A., Taylor, J. R., & Potenza, M. N. (2003) · American Journal of Psychiatry · doi:10.1176/appi.ajp.160.6.1041 · Cited by 1,719 · see citing works
(1967) · Medical Entomology and Zoology · Cited by 1,713 · see citing works
Reactivation of Ocular Dominance Plasticity in the Adult Visual Cortex
Pizzorusso, T., Medini, P., Berardi, N., Chierzi, S., Fawcett, J. W., & Maffei, L. (2002) · Science · doi:10.1126/science.1072699 · Cited by 1,679 · see citing works
Neural Mechanisms of Extinction Learning and Retrieval
Quirk, G. J., & Mueller, D. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301555 · Cited by 1,645 · see citing works
The contextual brain: implications for fear conditioning, extinction and psychopathology
Maren, S., Phan, K. L., & Liberzon, I. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3492 · Cited by 1,547 · see citing works
Fear Extinction as a Model for Translational Neuroscience: Ten Years of Progress
Milad, M. R., & Quirk, G. J. (2012) · Annual Review of Psychology · doi:10.1146/annurev.psych.121208.131631 · Cited by 1,466 · see citing works
LaBar, K. S., Gatenby, J. C., Gore, J. C., LeDoux, J. E., & Phelps, E. A. (1998) · Neuron · doi:10.1016/s0896-6273(00)80475-4 · Cited by 1,402 · see citing works
Bechara, A., Tranel, D., Damasio, H., Adolphs, R., Rockland, C., & Damasio, A. R. (1995) · Science · doi:10.1126/science.7652558 · Cited by 1,400 · see citing works
Neurobiological Basis of Failure to Recall Extinction Memory in Posttraumatic Stress Disorder
Milad, M. R., Pitman, R. K., Ellis, C. B., Gold, A. L., Shin, L. M., Lasko, N. B., Zeidan, M. A., Handwerger, K., Orr, S. P., & Rauch, S. L. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.06.026 · Cited by 1,339 · see citing works
Hensch, T. K. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144327 · Cited by 1,300 · see citing works
Preventing the return of fear in humans using reconsolidation update mechanisms
Schiller, D., Monfils, M.-H., Raio, C. M., Johnson, D. C., LeDoux, J. E., & Phelps, E. A. (2010) · Nature · doi:10.1038/nature08637 · Cited by 1,248 · see citing works
Milad, M. R., Wright, C. I., Orr, S. P., Pitman, R. K., Quirk, G. J., & Rauch, S. L. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.10.011 · Cited by 1,197 · see citing works
Sierra-Mercado, D., Padilla-Coreano, N., & Quirk, G. J. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.184 · Cited by 1,190 · see citing works
Classical fear-conditioning in the anxiety disorders: a meta-analysis
Lissek, S., Powers, A. S., McClure, E. B., Phelps, E. A., Woldehawariat, G., Grillon, C., & Pine, D. S. (2005) · Behaviour Research and Therapy · doi:10.1016/j.brat.2004.10.007 · Cited by 1,034 · see citing works
Extinction-Reconsolidation Boundaries: Key to Persistent Attenuation of Fear Memories
Monfils, M.-H., Cowansage, K. K., Klann, E., & LeDoux, J. E. (2009) · Science · doi:10.1126/science.1167975 · Cited by 960 · see citing works
The role of ventromedial prefrontal cortex in the recovery of extinguished fear
Quirk, G. J., Russo, G. K., Barron, J. L., & Lebron, K. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-16-06225.2000 · Cited by 957 · see citing works
Brain systems mediating aversive conditioning: an event-related fMRI study
Büchel, C., Morris, J., Dolan, R. J., & Friston, K. J. (1998) · Neuron · doi:10.1016/s0896-6273(00)80476-6 · Cited by 951 · see citing works
Switching on and off fear by distinct neuronal circuits
Herry, C., Ciocchi, S., Senn, V., Demmou, L., Müller, C., & Lüthi, A. (2008) · Nature · doi:10.1038/nature07166 · Cited by 950 · see citing works
Local GABA Circuit Control of Experience-Dependent Plasticity in Developing Visual Cortex
Hensch, T. K., Fagiolini, M., Mataga, N., Stryker, M. P., Baekkeskov, S., & Kash, S. F. (1998) · Science · doi:10.1126/science.282.5393.1504 · Cited by 910 · see citing works
Extinction of emotional learning: contribution of medial prefrontal cortex
Morgan, M. A., Romanski, L. M., & LeDoux, J. E. (1993) · Neuroscience Letters · doi:10.1016/0304-3940(93)90241-c · Cited by 897 · see citing works
The antidepressant fluoxetine restores plasticity in the adult visual cortex
Vetencourt, J. F. M., Sale, A., Viegi, A., Baroncelli, L., De Pasquale, R., F. O'Leary, O., Castrén, E., & Maffei, L. (2008) · Science · doi:10.1126/science.1150516 · Cited by 890 · see citing works
Early developmental emergence of human amygdala–prefrontal connectivity after maternal deprivation
Gee, D. G., Gabard-Durnam, L. J., Flannery, J., Goff, B., Humphreys, K. L., Telzer, E. H., Hare, T. A., Bookheimer, S. Y., & Tottenham, N. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1307893110 · Cited by 871 · see citing works
Quirk, G. J., Repa, J. C., & LeDoux, J. E. (1995) · Neuron · doi:10.1016/0896-6273(95)90092-6 · Cited by 808 · see citing works
Hippocampal Neurogenesis Regulates Forgetting During Adulthood and Infancy
Akers, K. G., Martinez-Canabal, A., Restivo, L., Yiu, A. P., De Cristofaro, A., Hsiang, H.-L. (., Wheeler, A. L., Guskjolen, A., Niibori, Y., Shoji, H., et al. (2014) · Science · doi:10.1126/science.1248903 · Cited by 761 · see citing works
Perineuronal Nets Protect Fear Memories from Erasure
Gogolla, N., Caroni, P., Lüthi, A., & Herry, C. (2009) · Science · doi:10.1126/science.1174146 · Cited by 760 · see citing works
Wagner, F. (2002) · Neuropsychopharmacology · doi:10.1016/s0893-133x(01)00367-0 · Cited by 739 · see citing works
A Developmental Shift from Positive to Negative Connectivity in Human Amygdala–Prefrontal Circuitry
Gee, D. G., Humphreys, K. L., Flannery, J., Goff, B., Telzer, E. H., Shapiro, M., Hare, T. A., Bookheimer, S. Y., & Tottenham, N. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.3446-12.2013 · Cited by 731 · see citing works
Contextual fear, gestalt memories, and the hippocampus
Fanselow, M. S. (2000) · Behavioural Brain Research · doi:10.1016/s0166-4328(99)00186-2 · Cited by 728 · see citing works
Morgan, M. A., & LeDoux, J. E. (1995) · Behavioral Neuroscience · doi:10.1037/0735-7044.109.4.681 · Cited by 717 · see citing works
Inhibitory threshold for critical-period activation in primary visual cortex
Fagiolini, M., & Hensch, T. K. (2000) · Nature · doi:10.1038/35004582 · Cited by 716 · see citing works
McDonald, A. J., Mascagni, F., & Guo, L. (1996) · Neuroscience · doi:10.1016/0306-4522(95)00417-3 · Cited by 689 · see citing works
Experience-driven plasticity of visual cortex limited by myelin and nogo receptor
McGee, A. W., Yang, Y., Fischer, Q. S., Daw, N. W., & Strittmatter, S. M. (2005) · Science · doi:10.1126/science.1114362 · Cited by 643 · see citing works
Developmental neurobiology of cognitive control and motivational systems.
Somerville, L. H., & Casey, B. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.01.006 · Cited by 634 · see citing works
Impaired fear conditioning following unilateral temporal lobectomy in humans
LaBar, K., LeDoux, J., Spencer, D., & Phelps, E. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-10-06846.1995 · Cited by 631 · see citing works
Prefrontal control of fear: more than just extinction
Sotres-Bayon, F., & Quirk, G. J. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.02.005 · Cited by 625 · cited 1× · see citing works
“Collectively, these neuroplastic changes in the cortex during adolescence coincide with a transitional phase spanning the juvenile stage in which fear learning and extinction are independent of the cortex and the mature adult stage in which these processes are dynamically regulated by vmPFC-subcortical circuitry (Bake…”
BackgroundThe GABA Excitatory/Inhibitory Shift in Brain Maturation and Neurological Disorders
Ben‐Ari, Y., Khalilov, I., Kahle, K. T., & Cherubini, E. (2012) · The Neuroscientist · doi:10.1177/1073858412438697 · Cited by 622 · see citing works
Removing brakes on adult brain plasticity: From molecular to behavioral interventions
Bavelier, D., Levi, D. M., Li, R. W., Dan, Y., & Hensch, T. K. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4812-10.2010 · Cited by 589 · see citing works
Activity in Prelimbic Cortex Is Necessary for the Expression of Learned, But Not Innate, Fears
Corcoran, K., & Quirk, G. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.5327-06.2007 · Cited by 580 · see citing works
Galtrey, C. M., & Fawcett, J. W. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2006.09.006 · Cited by 575 · see citing works
Quirk, G. J., Armony, J. L., & LeDoux, J. E. (1997) · Neuron · doi:10.1016/s0896-6273(00)80375-x · Cited by 563 · see citing works
Burgos-Robles, A., Vidal-Gonzalez, I., & Quirk, G. J. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0378-09.2009 · Cited by 530 · see citing works
Burgos-Robles, A., Vidal-Gonzalez, I., Santini, E., & Quirk, G. J. (2007) · Neuron · doi:10.1016/j.neuron.2007.02.021 · Cited by 516 · see citing works
Presence and acquired origin of reduced recall for fear extinction in PTSD: Results of a twin study
Milad, M. R., Orr, S. P., Lasko, N. B., Chang, Y., Rauch, S. L., & Pitman, R. K. (2008) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2008.01.017 · Cited by 512 · see citing works
Synaptic plasticity in the basolateral amygdala induced by hippocampal formation stimulation in vivo
Maren, S., & Fanselow (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-11-07548.1995 · Cited by 499 · see citing works
Calcium-Permeable AMPA Receptor Dynamics Mediate Fear Memory Erasure
Clem, R. L., & Huganir, R. L. (2010) · Science · doi:10.1126/science.1195298 · Cited by 496 · see citing works
Afferent connections of the medial frontal cortex of the rat. II. Cortical and subcortical afferents
Condé, F., Maire-Lepoivre, E., Audinat, É., & Crépel, F. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903520407 · Cited by 494 · see citing works
Kalisch, R., Korenfeld, E., Stephan, K. E., Weiskopf, N., Seymour, B., & Dolan, R. J. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.2021-06.2006 · Cited by 493 · see citing works
Sugiyama, S., Di Nardo, A. A., Aizawa, S., Matsuo, I., Volovitch, M., Prochiantz, A., & Hensch, T. K. (2008) · Cell · doi:10.1016/j.cell.2008.05.054 · Cited by 491 · see citing works
A Role for the Human Dorsal Anterior Cingulate Cortex in Fear Expression
Milad, M. R., Quirk, G. J., Pitman, R. K., Orr, S. P., Fischl, B., & Rauch, S. L. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.04.032 · Cited by 485 · see citing works
Amygdala intercalated neurons are required for expression of fear extinction
Likhtik, E., Popa, D., Apergis-Schoute, J., Fidacaro, G. A., & Paré, D. (2008) · Nature · doi:10.1038/nature07167 · Cited by 474 · see citing works
Organization of amygdaloid projections to the prefrontal cortex and associated striatum in the rat
McDonald, A. J. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90247-l · Cited by 463 · see citing works
Gating of Fear in Prelimbic Cortex by Hippocampal and Amygdala Inputs
Sotres-Bayón, F., Sierra‐Mercado, D., Pardilla‐Delgado, E., & Quirk, G. J. (2012) · Neuron · doi:10.1016/j.neuron.2012.09.028 · Cited by 451 · see citing works
Comparative aspects of amygdala connectivity
PRICE, J. L. (2003) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2003.tb07070.x · Cited by 442 · see citing works
Two different lateral amygdala cell populations contribute to the initiation and storage of memory
Repa, J. C., Muller, J., Apergis, J., Desrochers, T. M., Zhou, Y., & LeDoux, J. E. (2001) · Nature Neuroscience · doi:10.1038/89512 · Cited by 440 · see citing works
GABAergic Interneurons Shape the Functional Maturation of the Cortex
Le Magueresse, C., & Monyer, H. (2013) · Neuron · doi:10.1016/j.neuron.2013.01.011 · Cited by 425 · see citing works
Thickness of ventromedial prefrontal cortex in humans is correlated with extinction memory
Milad, M. R., Quinn, B. T., Pitman, R. K., Orr, S. P., Fischl, B., & Rauch, S. L. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0502441102 · Cited by 412 · see citing works
Altered fear learning across development in both mouse and human
Pattwell, S. S., Duhoux, S., Hartley, C. A., Johnson, D. C., Jing, D., Elliott, M. D., Ruberry, E. J., Powers, A., Mehta, N., Yang, R. R., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1206834109 · Cited by 404 · see citing works
Self-citationMaternal presence serves as a switch between learning fear and attraction in infancy
Moriceau, S., & Sullivan, R. M. (2006) · Nature Neuroscience · doi:10.1038/nn1733 · Cited by 386 · see citing works
The role of the amygdala in conditioned and unconditioned fear and anxiety
Davis, M. (2000) · The Amygdala · doi:10.1093/oso/9780198505013.003.0006 · Cited by 384 · see citing works
Fear erasure in mice requires synergy between antidepressant drugs and extinction training
Karpova, N. N., Pickenhagen, A., Lindholm, J., Tiraboschi, E., Kulesskaya, N., Ágústsdóttir, A., Antila, H., Popova, D., Akamine, Y., Sullivan, R., et al. (2011) · Science · doi:10.1126/science.1214592 · Cited by 382 · see citing works
Hong, E. J., McCord, A. E., & Greenberg, M. E. (2008) · Neuron · doi:10.1016/j.neuron.2008.09.024 · Cited by 366 · see citing works
Lynx1, a Cholinergic Brake, Limits Plasticity in Adult Visual Cortex
Morishita, H., Miwa, J. M., Heintz, N., & Hensch, T. K. (2010) · Science · doi:10.1126/science.1195320 · Cited by 365 · see citing works
Epigenetic Priming of Memory Updating during Reconsolidation to Attenuate Remote Fear Memories
Gräff, J., Joseph, N. F., Horn, M. E., Samiei, A., Meng, J., Seo, J., Rei, D., Bero, A. W., Phan, T. X., Wagner, F., et al. (2014) · Cell · doi:10.1016/j.cell.2013.12.020 · Cited by 357 · see citing works
Zeidan, M. A., Igoe, S. A., Linnman, C., Vitalo, A., Levine, J. B., Klibanski, A., Goldstein, J. M., & Milad, M. R. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.05.016 · Cited by 354 · see citing works
Contextual fear conditioning in humans: cortical–hippocampal and amygdala contributions
Alvarez, R. P., Biggs, A., Chen, G., Pine, D. S., & Grillon, C. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1246-08.2008 · Cited by 325 · see citing works
Reducing Intracortical Inhibition in the Adult Visual Cortex Promotes Ocular Dominance Plasticity
Harauzov, A., Spolidoro, M., DiCristo, G., De Pasquale, R., Cancedda, L., Pizzorusso, T., Viegi, A., Berardi, N., & Maffei, L. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.2233-09.2010 · Cited by 319 · see citing works
Good memories of bad events in infancy
Sullivan, R. M., Landers, M., Yeaman, B., & Wilson, D. A. (2000) · Nature · doi:10.1038/35024156 · Cited by 315 · see citing works
Longitudinal four-dimensional mapping of subcortical anatomy in human development
Raznahan, A., Shaw, P. W., Lerch, J. P., Clasen, L. S., Greenstein, D., Berman, R., Pipitone, J., Chakravarty, M. M., & Giedd, J. N. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1316911111 · Cited by 312 · see citing works
Katoh‐Semba, R., TAKEUCHI, I. K., Semba, R., & Kato, K. (1997) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1997.69010034.x · Cited by 308 · see citing works
Adolescence: what do transmission, transition and translation have to do with it?
Casey, B. J., Duhoux, S., & Cohen, M. M. (2010) · Neuron · doi:10.1016/j.neuron.2010.08.033 · Cited by 297 · see citing works
Sotres-Bayon, F., Bush, D. E. A., & LeDoux, J. E. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301316 · Cited by 293 · see citing works
Mauney, S. A., Athanas, K. M., Pantazopoulos, H., Shaskan, N., Passeri, E., Berretta, S., & Woo, T.-U. W. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.05.007 · Cited by 291 · see citing works
Marschner, A., Kalisch, R., Vervliet, B., Vansteenwegen, D., & Büchel, C. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.1651-08.2008 · Cited by 235 · see citing works
Contextual conditioning and auditory cue conditioning dissociate during development.
Rudy, J. W. (1993) · Behavioral Neuroscience · doi:10.1037//0735-7044.107.5.887 · Cited by 220 · see citing works
Extinction of auditory fear conditioning requires MAPK/ERK activation in the basolateral amygdala
Herry, C., Trifilieff, P., Micheau, J., Lüthi, A., & Mons, N. E. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04893.x · Cited by 203 · see citing works
Di Cristo, G., Chattopadhyaya, B., Kuhlman, S. J., Fu, Y., Bélanger, M.-C., Wu, C. Z., Rutishauser, U., Maffei, L., & Huang, Z. J. (2007) · Nature Neuroscience · doi:10.1038/nn2008 · Cited by 201 · see citing works
Sakata, K., Woo, N. H., Martinowich, K., Greene, J. S., Schloesser, R. J., Shen, L., & Lu, B. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0811431106 · Cited by 200 · see citing works
Impaired Extinction Retention in Adolescent Rats: Effects of D-Cycloserine
McCallum, J., Kim, J. H., & Richardson, R. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.92 · Cited by 198 · see citing works
Distinct neural signatures of threat learning in adolescents and adults
Lau, J. Y., Britton, J. C., Nelson, E. E., Angold, A., Ernst, M., Goldwin, M., Grillon, C., Leibenluft, E., Lissek, S., Norcross, M., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1005494108 · Cited by 197 · see citing works
Development of the GABAergic System from Birth to Adolescence
Kilb, W. (2012) · The Neuroscientist · doi:10.1177/1073858411422114 · Cited by 190 · see citing works
Kim, J. H., & Richardson, R. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.09.003 · Cited by 189 · see citing works
Reinstatement of Conditioned Fear in Humans Is Context Dependent and Impaired in Amnesia.
LaBar, K. S., & Phelps, E. A. (2005) · Behavioral Neuroscience · doi:10.1037/0735-7044.119.3.677 · Cited by 184 · cited 1× · see citing works
“the hippocampus (Kalisch et al, 2006; Milad et al, 2007b), and hippocampal lesions impair context-dependent fear reinstatement (LaBar and Phelps, 2005), a finding that parallels observations in rodents (Wilson et al, 1995).”
ResultThe Development and Neurobiology of Infant Attachment and Fear
Landers, M. S., & Sullivan, R. M. (2012) · Developmental Neuroscience · doi:10.1159/000336732 · Cited by 180 · see citing works
Electrolytic lesions of the dorsal hippocampus disrupt renewal of conditional fear after extinction.Preprint
Ji, J.-Z., & Maren, S. (2005) · Learning & memory (Cold Spring Harbor, N.Y.) · doi:10.1101/lm.91705 · Cited by 174 · see citing works
Contextual conditioning and auditory cue conditioning dissociate during development.
Rudy, J. W. (1993) · Behavioral Neuroscience · doi:10.1037/0735-7044.107.5.887 · Cited by 173 · see citing works
Callaghan, B. L., & Richardson, R. (2011) · Behavioral Neuroscience · doi:10.1037/a0022008 · Cited by 169 · see citing works
Prefrontal cortical inputs to the basal amygdala undergo pruning during late adolescence in the rat
Cressman, V. L., Balaban, J., Steinfeld, S., Shemyakin, A., Graham, P., Parisot, N., & Moore, H. (2010) · Journal of Comparative Neurology · doi:10.1002/cne.22359 · Cited by 161 · see citing works
Selective early-acquired fear memories undergo temporary suppression during adolescence
Pattwell, S. S., Bath, K. G., Casey, B. J., Ninan, I., & Lee, F. S. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1012975108 · Cited by 161 · see citing works
Self-citationAmygdalohippocampal and Amygdalocortical Projections in the Primate Brain
Amaral, D. G. (1986) · Advances in experimental medicine and biology · doi:10.1007/978-1-4684-7971-3_1 · Cited by 158 · see citing works
Kim, J. H., Hamlin, A. S., & Richardson, R. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.0596-09.2009 · Cited by 154 · see citing works
Immunohistochemical Analyses of Long-Term Extinction of Conditioned Fear in Adolescent Rats
Kim, J. H., Li, S., & Richardson, R. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq116 · Cited by 149 · see citing works
Camp, L. L., & Rudy, J. W. (1988) · Developmental Psychobiology · doi:10.1002/dev.420210103 · Cited by 147 · see citing works
Myelin associated inhibitors: A link between injury-induced and experience-dependent plasticity
Akbik, F. V., Cafferty, W. B. J., & Strittmatter, S. M. (2011) · Experimental Neurology · doi:10.1016/j.expneurol.2011.06.006 · Cited by 147 · see citing works
The development of fear learning and generalization in 8-13 year-olds
Glenn, C. R., Klein, D. N., Lissek, S., Britton, J. C., Pine, D. S., & Hajcak, G. (2012) · Developmental Psychobiology · doi:10.1002/dev.20616 · Cited by 144 · see citing works
Hartley, C. A., Fischl, B., & Phelps, E. A. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq253 · Cited by 143 · see citing works
Self-citationThe role of the rat hippocampal system in several effects of context in extinction.
Wilson, A., Brooks, D. C., & Bouton, M. E. (1995) · Behavioral Neuroscience · doi:10.1037//0735-7044.109.5.828 · Cited by 140 · see citing works
Fear conditioning and extinction across development: Evidence from human studies and animal models
Shechner, T., Hong, M., Britton, J. C., Pine, D., & Fox, N. (2014) · Biological Psychology · doi:10.1016/j.biopsycho.2014.04.001 · Cited by 139 · see citing works
Converting juvenile into adult plasticity: a role for the brain's extracellular matrix
Gundelfinger, E. D., Frischknecht, R., Choquet, D., & Heine, M. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07253.x · Cited by 136 · see citing works
The Importance of Early Experiences for Neuro-Affective Development
Tottenham, N. (2013) · Current topics in behavioral neurosciences · doi:10.1007/7854_2013_254 · Cited by 133 · see citing works
Human amygdala activity during the expression of fear responses.
Cheng, D. T., Knight, D. C., Smith, C. N., & Helmstetter, F. J. (2006) · Behavioral Neuroscience · doi:10.1037/0735-7044.120.5.1187 · Cited by 131 · see citing works
The Importance of Early Experiences for Neuro-Affective Development
Tottenham, N. (2013) · Current topics in behavioral neurosciences · doi:10.1007/978-3-662-45758-0_254 · Cited by 128 · see citing works
A developmental dissociation in reinstatement of an extinguished fear response in rats.
Kim, J., & Richardson, R. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.03.004 · Cited by 116 · see citing works
The role of the rat hippocampal system in several effects of context in extinction.
Wilson, A., Brooks, D. C., & Bouton, M. E. (1995) · Behavioral Neuroscience · doi:10.1037/0735-7044.109.5.828 · Cited by 115 · see citing works
Kim, J. H., & Richardson, R. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.4736-07.2008 · Cited by 114 · see citing works
Wu, X., Fu, Y., Knott, G. W., Lu, J., Cristo, G. D., & Huang, Z. J. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.3189-11.2012 · Cited by 111 · see citing works
Developmental emergence of fear learning corresponds with changes in amygdala synaptic plasticity
Thompson, J. V., Sullivan, R. M., & Wilson, D. A. (2008) · Brain Research · doi:10.1016/j.brainres.2008.01.057 · Cited by 109 · see citing works
Functional emergence of the hippocampus in context fear learning in infant rats
Raineki, C., Holman, P. J., Dębiec, J., Bugg, M., Beasley, A., & Sullivan, R. M. (2009) · Hippocampus · doi:10.1002/hipo.20702 · Cited by 103 · see citing works
Callaghan, B. L., & Richardson, R. (2012) · Translational Psychiatry · doi:10.1038/tp.2012.65 · Cited by 97 · see citing works
Nabel, E. M., & Morishita, H. (2013) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2013.00146 · Cited by 85 · see citing works
Postnatal maturation of GABAergic transmission in the rat basolateral amygdala.
Ehrlich, D. E., Ryan, S., Hazra, R., Guo, J.-D., & Rainnie, D. (2013) · Journal of Neurophysiology · doi:10.1152/jn.01105.2012 · Cited by 84 · see citing works
Extinction in the developing rat: an examination of renewal effects.
Yap, C., & Richardson, R. (2007) · Developmental Psychobiology · doi:10.1002/dev.20244 · Cited by 84 · see citing works
Blockade of amygdala metabotropic glutamate receptor subtype 1 impairs fear extinction
Kim, J., Lee, S., Park, H., Song, B., Hong, I., Geum, D., Shin, K., & Choi, S. (2007) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2007.01.125 · Cited by 78 · see citing works
A window of vulnerability: Impaired fear extinction in adolescence
Baker, K., Den, M. L., Graham, B. M., & Richardson, R. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.10.009 · Cited by 68 · see citing works
The development of skin conductance fear conditioning in children from ages 3 to 8 years
Gao, Y., Raine, A., Venables, P. H., Dawson, M. E., & Mednick, S. A. (2009) · Developmental Science · doi:10.1111/j.1467-7687.2009.00874.x · Cited by 62 · see citing works
Recovery of fear memories in rats: Role of gamma-amino butyric acid (GABA) in infantile amnesia.
Kim, J. H., McNally, G. P., & Richardson, R. (2006) · Behavioral Neuroscience · doi:10.1037/0735-7044.120.1.40 · Cited by 57 · see citing works
Cortico-amygdala circuits: Role in the conditioned stress response
Berretta, S. (2005) · Stress · doi:10.1080/10253890500489395 · Cited by 47 · see citing works
Treating the Developing Brain: Implications from Human Imaging and Mouse Genetics
Casey, B. J., Pattwell, S. S., Glatt, C. E., & Lee, F. S. (2012) · Annual Review of Medicine · doi:10.1146/annurev-med-052611-130408 · Cited by 29 · see citing works
Self-citationMohapatra, S., Agarwal, V., & Sitholey, P. (2013) · Asian Journal of Psychiatry · doi:10.1016/j.ajp.2013.06.017 · Cited by 18 · see citing works
Kim, J., Lee, S., Park, H., Song, B., Hong, I., Geum, D., Shin, K., & Choi, S. (2007) · Cited by 7 · see citing works
Fear Models in Animals and Humans
Hartley, C. A., & Phelps, E. A. (2013) · Springer eBooks · doi:10.1007/978-1-4614-6599-7_1 · Cited by 6 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Cowan, C. S. M., Dinan, T. G., & Cryan, J. F. (2020) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.13156 · Cited by 176 · see citing works
Gee, D. G. (2021) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2021.21090944 · Cited by 148 · see citing works
Neural contributors to trauma resilience: a review of longitudinal neuroimaging studies
Roeckner, A. R., Oliver, K. I., Lebois, L. A. M., van Rooij, S. J. H., & Stevens, J. S. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01633-y · Cited by 103 · see citing works
Opendak, M., Gould, E., & Sullivan, R. (2017) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2017.02.002 · Cited by 94 · see citing works
Hostinar, C. E., Nusslock, R., & Miller, G. E. (2018) · Journal of Clinical Child & Adolescent Psychology · doi:10.1080/15374416.2016.1266647 · Cited by 90 · see citing works
The Stress Acceleration Hypothesis of Nightmares
Nielsen, T. (2017) · Frontiers in Neurology · doi:10.3389/fneur.2017.00201 · Cited by 63 · see citing works
An Adolescent Sensitive Period for Threat Responding: Impacts of Stress and Sex
Gerhard, D. M., Meyer, H. C., & Lee, F. S. (2021) · Biological Psychiatry · doi:10.1016/j.biopsych.2020.10.003 · Cited by 54 · see citing works
Self-citation
- Authors
- Hartley, C. A., & Lee, F. S.
- Affiliations
- Cornell University (US)
- Corresponding author
- Hartley, Catherine A
- Venue
- Neuropsychopharmacology
- Published
- 2014-07-18
- Volume
- 40
- Issue
- 1
- Pages
- 50-60
- ISSN
- 0893-133X (ISSN-L)
- 1740-634X
- PMC
- PMC4262897
- OpenAlex
- W2024045888
- Cited by
- 80
- References
- 134
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 4 · 2023: 5 · 2022: 8 · 2021: 8 · 2020: 13 · 2019: 9 · 2018: 7 · 2017: 11 · 2016: 4 · 2015: 4 · 2014: 1
- FWCI
- 0.64
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Neuropsychopharmacology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- sensitive period, fear learning, fear extinction, emotional development, neuroplasticity, visual system development, childhood to adulthood development
- MeSH terms
- Animals, Brain, Critical Period, Psychological, Extinction, Psychological, Fear, Humans, Learning, Nerve Net, Neuronal Plasticity
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