Placing prediction into the fear circuit

McNally, Gavan P.; Johansen, Joshua P.; Blair, Hugh T.

doi:10.1016/j.tins.2011.03.005

Cited by 298Memory and Neural MechanismsNeuroscience and Neuropharmacology ResearchNeurotransmitter Receptor Influence on Behavior

Placing prediction into the fear circuit

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McNally, Gavan P., Johansen, Joshua P., Blair, Hugh T.·2011·Trends in Neurosciences

DOI 10.1016/j.tins.2011.03.005PMC PMC4245078

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Abstract

Pavlovian fear conditioning depends on synaptic plasticity at amygdala neurons. Here, we review recent electrophysiological, molecular and behavioral evidence suggesting the existence of a distributed neural circuitry regulating amygdala synaptic plasticity during fear learning. This circuitry, which involves projections from the midbrain periaqueductal gray region, can be linked to prediction error and expectation modulation of fear learning, as described by associative and computational learning models. It controls whether, and how much, fear learning occurs by signaling aversive events when they are unexpected. Functional neuroimaging and clinical studies indicate that this prediction circuit is recruited in humans during fear learning and contributes to exposure-based treatments for clinical anxiety. This aversive prediction error circuit might represent a conserved mechanism for regulating fear learning in mammals.

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Dopamine is implicated in pavlovian extinction learning.
“dopamine has also been implicated in pavlovian extinction learning (for review see McNally et al., 2011).”
From Retrieval-Dependent Mechanisms Affecting Emotional Memory Persistence: Reconsolidation, Extinction, and the Space in Between (2020) · cites this paper as McNally et al., 2011
The Conclusions (page unavailable) implicate dopamine in Pavlovian fear conditioning, including associative blocking, but do not link it specifically to extinction learning. The section ‘Instruction of fear extinction by negative prediction errors’ (page unavailable) discusses opioids and other mechanisms of extinction instead. (LLM, conf=0.84)
Experimental — accuracy not yet measured
Expectancy effects in the periaqueductal gray appear mediated by inhibition of ascending nociceptive inputs through endogenous opioid release, which blocks nociceptive responses when pain is expected.
“These expectancy effects seem to be mediated by inhibition of ascending nociceptive inputs through the release of endogenous opioids in the PAG1, which blocks nociceptive responses when pain is expected.”
From Representation of aversive prediction errors in the human periaqueductal gray (2014) · cites this paper as [1]
Animal models of fear conditioning suggest that regions encoding avoidance value receive prediction error signals generated in the PAG.
“Based on existent animal models of fear conditioning1,18, we posited that these regions receive the PE signals generated in PAG.”
From Representation of aversive prediction errors in the human periaqueductal gray (2014) · cites this paper as [1]

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Emotion circuits in the brain
LeDoux, J. E. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.155 · Cited by 8,444 · see citing works
A theory of Pavlovian conditioning : Variations in the effectiveness of reinforcement and nonreinforcement
Rescorla, R. A. (1972) · Medical Entomology and Zoology · Cited by 7,268 · see citing works
Classical conditioning II: Current research and theory.
Black, A. H., & Prokasy, W. F. (1972) · Appleton-Century-Crofts eBooks · Cited by 4,449 · see citing works
The rat nervous system
Paxinos, G. (1985) · Cited by 3,715 · 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
A model for Pavlovian learning: Variations in the effectiveness of conditioned but not of unconditioned stimuli.
Pearce, J. M., & Hall, G. (1980) · Psychological Review · doi:10.1037/0033-295x.87.6.532 · Cited by 3,023 · see citing works
A theory of attention: Variations in the associability of stimuli with reinforcement
Mackintosh, N. J. (1975) · Psychological Review · doi:10.1037/h0076778 · Cited by 2,733 · see citing works
The role of the amygdala in fear and anxiety
Davis, M. (1992) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.15.030192.002033 · Cited by 2,357 · see citing works
Psychological and neural mechanisms of the affective dimension of pain
Price, D. D. (2000) · Science · doi:10.1126/science.288.5472.1769 · Cited by 2,092 · 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
Toward a modern theory of adaptive networks: Expectation and prediction.
Sutton, R. S., & Barto, A. G. (1981) · Psychological Review · doi:10.1037/0033-295x.88.2.135 · Cited by 1,450 · see citing works
Neuronal signalling of fear memory
Maren, S., & Quirk, G. J. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1535 · Cited by 1,428 · see citing works
Neuronal Coding of Prediction Errors
Schultz, W., & Dickinson, A. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.473 · Cited by 1,427 · see citing works
Two types of dopamine neuron distinctly convey positive and negative motivational signals
Matsumoto, M., & Hikosaka, O. (2009) · Nature · doi:10.1038/nature08028 · Cited by 1,378 · see citing works
Integrative activity of the brain
Konorski, J. (1967) · Cited by 1,372 · see citing works
Dopamine responses comply with basic assumptions of formal learning theory
Waelti, P., Dickinson, A., & Schultz, W. (2001) · Nature · doi:10.1038/35083500 · Cited by 1,018 · see citing works
Plastic Synaptic Networks of the Amygdala for the Acquisition, Expression, and Extinction of Conditioned Fear
Pape, H.-C., & Pare, D. (2010) · Physiological Reviews · doi:10.1152/physrev.00037.2009 · Cited by 994 · see citing works
When fear is near: threat imminence elicits prefrontal periaqueductal gray shifts in humans.
Mobbs, D., Petrovic, P., Marchant, J. L., Hassabis, D., Weiskopf, N., Seymour, B., Dolan, R. J., & Frith, C. D. (2007) · Science · doi:10.1126/science.1144298 · Cited by 951 · see citing works
Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus
Amat, J., Baratta, M. V., Paul, E., Bland, S. T., Watkins, L. R., & Maier, S. F. (2005) · Nature Neuroscience · doi:10.1038/nn1399 · Cited by 931 · see citing works
Encoding of conditioned fear in central amygdala inhibitory circuits
Ciocchi, S., Herry, C., Grenier, F., Wolff, S. B. E., Letzkus, J. J., Vlachos, I., Ehrlich, I., Sprengel, R., Deisseroth, K., Stadler, M. B., et al. (2010) · Nature · doi:10.1038/nature09559 · Cited by 924 · see citing works
Amygdala inhibitory circuits and the control of fear memory
Ehrlich, I., Humeau, Y., Grenier, F., Ciocchi, S., Herry, C., & Lüthi, A. (2009) · Neuron · doi:10.1016/j.neuron.2009.05.026 · Cited by 878 · see citing works
Genetic dissection of an amygdala microcircuit that gates conditioned fear
Haubensak, W., Kunwar, P. S., Cai, H., Ciocchi, S., Wall, N. R., Ponnusamy, R., Biag, J., Dong, H.-W., Deisseroth, K., Callaway, E. M., et al. (2010) · Nature · doi:10.1038/nature09553 · Cited by 840 · see citing works
A perceptual-defensive-recuperative model of fear and pain
Bolles, R. C., & Fanselow, M. S. (1980) · Behavioral and Brain Sciences · doi:10.1017/s0140525x0000491x · Cited by 827 · see citing works
Phasic excitation of dopamine neurons in ventral VTA by noxious stimuli
Brischoux, F., Chakraborty, S., Brierley, D. I., & Ungless, M. A. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0811507106 · Cited by 801 · see citing works
Miami Symposium on the prediction of behavior, 1967 : aversive stimulation
Jones, M. R. (1968) · University of Miami Press eBooks · Cited by 732 · see citing works
Differential contribution of dorsal and ventral medial prefrontal cortex to the acquisition and extinction of conditioned fear in rats.
Morgan, M. A., & LeDoux, J. E. (1995) · Behavioral Neuroscience · doi:10.1037/0735-7044.109.4.681 · Cited by 717 · see citing works
Differential contribution of dorsal and ventral medial prefrontal cortex to the acquisition and extinction of conditioned fear in rats.
Morgan, M. A., & LeDoux, J. E. (1995) · Behavioral Neuroscience · doi:10.1037//0735-7044.109.4.681 · Cited by 717 · see citing works
"Attention-like" processes in classical conditioning
Kamin, L. J. (1967) · NASA Technical Reports Server (NASA) · Cited by 716 · see citing works
The Neuroscience of Mammalian Associative Learning
Fanselow, M. S., & Poulos, A. M. (2005) · Annual Review of Psychology · doi:10.1146/annurev.psych.56.091103.070213 · Cited by 683 · see citing works
Circuit-breakers: optical technologies for probing neural signals and systems
Zhang, F., Aravanis, A. M., Adamantidis, A., de Lecea, L., & Deisseroth, K. A. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2192 · Cited by 623 · see citing works
Temporal difference models describe higher-order learning in humans
Seymour, B., O'Doherty, J. P., Dayan, P., Koltzenburg, M., Jones, A. K., Dolan, R. J., Friston, K. J., & Frackowiak, R. S. (2004) · Nature · doi:10.1038/nature02581 · Cited by 605 · see citing works
The specificity of the ‘nonspecific’ midline and intralaminar thalamic nuclei
Groenewegen, H. J., & Berendse, H. W. (1994) · Trends in Neurosciences · doi:10.1016/0166-2236(94)90074-4 · Cited by 596 · 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
Representation of negative motivational value in the primate lateral habenula
Matsumoto, M., & Hikosaka, O. (2009) · Nature Neuroscience · doi:10.1038/nn.2233 · Cited by 547 · see citing works
Parallel circuits mediating distinct emotional coping reactions to different types of stress
Keay, K. A., & Bandler, R. (2001) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(01)00049-5 · Cited by 512 · see citing works
The periaqueductal gray and defensive behavior: functional representation and neuronal organization.
Carrive, P. (1993) · Behavioural Brain Research · doi:10.1016/0166-4328(93)90088-8 · Cited by 500 · see citing works
Effects of D-Cycloserine on Extinction: Translation From Preclinical to Clinical Work
Davis, M., Ressler, K., Rothbaum, B. O., & Richardson, R. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.03.084 · Cited by 498 · see citing works
Restricted cortical termination fields of the midline and intralaminar thalamic nuclei in the rat
Berendse, H. W., & Groenewegen, H. J. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90151-d · Cited by 494 · see citing works
From threat to fear: the neural organization of defensive fear systems in humans.
Mobbs, D., Marchant, J. L., Hassabis, D., Seymour, B., Tan, G., Gray, M., Petrovic, P., Dolan, R. J., & Frith, C. D. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.2378-09.2009 · Cited by 476 · see citing works
Pain reduction by electrical brain stimulation in man
Richardson, D. E., & Akil, H. (1977) · Journal of neurosurgery · doi:10.3171/jns.1977.47.2.0184 · Cited by 443 · see citing works
Pain reduction by electrical brain stimulation in man
Richardson, D. E., & Akil, H. (1977) · Journal of neurosurgery · doi:10.3171/jns.1977.47.2.0178 · Cited by 440 · see citing works
Opponent appetitive-aversive neural processes underlie predictive learning of pain relief
Seymour, B., O'Doherty, J. P., Koltzenburg, M., Wiech, K., Frackowiak, R., Friston, K., & Dolan, R. (2005) · Nature Neuroscience · doi:10.1038/nn1527 · Cited by 439 · see citing works
Is there a cell-biological alphabet for simple forms of learning?
Hawkins, R. D., & Kandel, E. R. (1984) · Psychological Review · doi:10.1037/0033-295x.91.3.375 · Cited by 436 · see citing works
Naloxone and shock-elicited freezing in the rat.
Fanselow, M. S., & Bolles, R. C. (1979) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0077609 · Cited by 411 · see citing works
The Midbrain Periaqueductal Gray as a Coordinator of Action in Response to Fear and Anxiety
Fanselow, M. S. (1991) · Springer eBooks · doi:10.1007/978-1-4615-3302-3_10 · Cited by 405 · see citing works
Glutamatergic activation of anterior cingulate cortex produces an aversive teaching signal
Johansen, J. P., & Fields, H. L. (2004) · Nature Neuroscience · doi:10.1038/nn1207 · Cited by 365 · see citing works
Self-citation
The Role of Associative History in Models of Associative Learning: A Selective Review and a Hybrid Model
Le Pelley, M. E. (2004) · The Quarterly Journal of Experimental Psychology Section B · doi:10.1080/02724990344000141 · Cited by 360 · see citing works
Expectation modulates neural responses to pleasant and aversive stimuli in primate amygdala
Belova, M. A., Paton, J. J., Morrison, S. E., & Salzman, C. D. (2007) · Neuron · doi:10.1016/j.neuron.2007.08.004 · Cited by 349 · see citing works
Dopamine-mediated modulation of odour-evoked amygdala potentials during pavlovian conditioning
Rosenkranz, J. A., & Grace, A. A. (2002) · Nature · doi:10.1038/417282a · Cited by 348 · see citing works
Chapter 13 Integration of somatic and autonomic reactions within the midbrain periaqueductal grey: Viscerotopic, somatotopic and functional organization
Bandler, R., Carrive, P., & Zhang, S. P. (1991) · Progress in brain research · doi:10.1016/s0079-6123(08)63056-3 · Cited by 329 · see citing works
Long-term potentiation in the amygdala: A cellular mechanism of fear learning and memory
Sigurdsson, T., Doyère, V., Cain, C. K., & LeDoux, J. E. (2006) · Neuropharmacology · doi:10.1016/j.neuropharm.2006.06.022 · Cited by 325 · see citing works
Neural substrates for expectation-modulated fear learning in the amygdala and periaqueductal gray
Johansen, J. P., Tarpley, J. W., LeDoux, J. E., & Blair, H. T. (2010) · Nature Neuroscience · doi:10.1038/nn.2594 · Cited by 312 · see citing works
Self-citation
Optical activation of lateral amygdala pyramidal cells instructs associative fear learning
Johansen, J. P., Hamanaka, H., Monfils, M. H., Behnia, R., Deisseroth, K., Blair, H. T., & LeDoux, J. E. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1002418107 · Cited by 308 · see citing works
Self-citation
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
Mapping brain networks in awake mice using combined optical neural control and fMRI
Desai, M., Kahn, I., Knoblich, U., Bernstein, J., Atallah, H. E., Yang, A., Kopell, N., Buckner, R. L., Graybiel, A. M., Moore, C. I., et al. (2010) · Journal of Neurophysiology · doi:10.1152/jn.00828.2010 · Cited by 276 · see citing works
Thalamic midline cell populations projecting to the nucleus accumbens, amygdala, and hippocampus in the rat
Su, H., & Bentivoglio, M. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902970410 · Cited by 269 · see citing works
Parallels between cerebellum- and amygdala-dependent conditioning
Medina, J. F., Repa, J. C., Mauk, M. D., & LeDoux, J. E. (2002) · Nature reviews. Neuroscience · doi:10.1038/nrn728 · Cited by 265 · see citing works
The computing neuron
Durbin, R. M., Miall, C., & Mitchison, G. (1989) · Addison-Wesley Longman Publishing Co., Inc. eBooks · Cited by 264 · see citing works
Previous Experience with Behavioral Control over Stress Blocks the Behavioral and Dorsal Raphe Nucleus Activating Effects of Later Uncontrollable Stress: Role of the Ventral Medial Prefrontal Cortex
Amat, J., Paul, E., Zarza, C., Watkins, L. R., & Maier, S. F. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.3630-06.2006 · Cited by 249 · see citing works
Rostral agranular insular cortex and pain areas of the central nervous system: A tract‐tracing study in the rat
Jasmin, L., Granato, A., & Ohara, P. T. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10978 · Cited by 238 · see citing works
The Midbrain periaqueductal gray matter : functional, anatomical, and neurochemical organization
Depaulis, A., & Bandler, R. J. (1991) · Plenum Press eBooks · Cited by 216 · see citing works
Inhibitory Cerebello-Olivary Projections and Blocking Effect in Classical Conditioning
Kim, J. J., Krupa, D. J., & Thompson, R. F. (1998) · Science · doi:10.1126/science.279.5350.570 · Cited by 211 · see citing works
A Study of the Protective Function of Acute Morphine Administration on Subsequent Posttraumatic Stress Disorder
Bryant, R. A., Creamer, M. C., O'Donnell, M. L., Silove, D. M., & McFARLANE, A. C. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.10.032 · Cited by 210 · see citing works
Amygdaloid D1 dopamine receptor involvement in Pavlovian fear conditioning
Guarraci, F. A., Frohardt, R. J., & Kapp, B. S. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01291-3 · Cited by 207 · 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
Pavlovian Fear Memory Induced by Activation in the Anterior Cingulate Cortex
Tang, J., Ko, S. W., Ding, H.-K., Qiu, C.-S., Calejesan, A. A., & Zhuo, M. (2005) · Molecular Pain · doi:10.1186/1744-8069-1-6 · Cited by 202 · see citing works
Central Amygdala Activity during Fear Conditioning
Duvarci, S., Popa, D., & Paré, D. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.4985-10.2011 · Cited by 202 · see citing works
Inhibition of the mesoamygdala dopaminergic pathway impairs the retrieval of conditioned fear associations.
Nader, K., & LeDoux, J. E. (1999) · Behavioral Neuroscience · doi:10.1037//0735-7044.113.5.891 · Cited by 194 · see citing works
Contributions of the anterior cingulate cortex and amygdala to pain- and fear-conditioned place avoidance in rats
Gao, Y., Ren, W.-H., Zhang, Y., & Zhao, Z. (2004) · Pain · doi:10.1016/j.pain.2004.04.030 · Cited by 186 · see citing works
Differential role of the medial and lateral prefrontal cortices in fear and anxiety.
Lacroix, L. P., Spinelli, S., Heidbreder, C. A., & Feldon, J. (2000) · Behavioral Neuroscience · doi:10.1037//0735-7044.114.6.1119 · Cited by 185 · see citing works
Separate brain regions code for salience vs. valence during reward prediction in humans
Jensen, J., Smith, A. J., Willeit, M., Crawley, A. P., Mikulis, D. J., Vitcu, I., & Kapur, S. (2006) · Human Brain Mapping · doi:10.1002/hbm.20274 · Cited by 178 · see citing works
Inhibition of the mesoamygdala dopaminergic pathway impairs the retrieval of conditioned fear associations.
Nader, K., & LeDoux, J. E. (1999) · Behavioral Neuroscience · doi:10.1037/0735-7044.113.5.891 · Cited by 174 · see citing works
Differential role of the medial and lateral prefrontal cortices in fear and anxiety.
Lacroix, L. P., Spinelli, S., Heidbreder, C. A., et al. (2000) · Behavioral Neuroscience · doi:10.1037/0735-7044.114.6.1119 · Cited by 167 · see citing works
Pavlovian Conditioning, Negative Feedback, and Blocking: Mechanisms that Regulate Association Formation
Fanselow, M. S. (1998) · Neuron · doi:10.1016/s0896-6273(00)81002-8 · Cited by 159 · see citing works
Role of NMDA receptors and MAP kinase in the amygdala in extinction of fear: clinical implications for exposure therapy*
Davis, M. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02138.x · Cited by 154 · see citing works
The Rostral Anterior Cingulate Cortex Modulates the Efficiency of Amygdala-Dependent Fear Learning
Bissière, S., Plachta, N., Hoyer, D., McAllister, K. H., Olpe, H.-R., Grace, A. A., & Cryan, J. F. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.10.022 · Cited by 151 · see citing works
Neural Correlates of Variations in Event Processing during Learning in Basolateral Amygdala
Roesch, M. R., Calu, D. J., Esber, G. R., & Schoenbaum, G. M. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.5781-09.2010 · Cited by 150 · see citing works
Evidence for two classes of nociceptive modulating neurons in the periaqueductal gray
Heinricher, M. M., Cheng, Z., & Fields, H. L. (1987) · Journal of Neuroscience · doi:10.1523/jneurosci.07-01-00271.1987 · Cited by 123 · see citing works
Opioid Receptors in the Midbrain Periaqueductal Gray Regulate Extinction of Pavlovian Fear Conditioning
McNally, G. P., Pigg, M., & Weidemann, G. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.1828-04.2004 · Cited by 117 · see citing works
Self-citation
Neural correlates of unconditioned response diminution during Pavlovian conditioning
Dunsmoor, J. E., Bandettini, P. A., & Knight, D. C. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2007.11.042 · Cited by 116 · see citing works
Prefrontal infusion of PD098059 immediately after fear extinction training blocks extinction-associated prefrontal synaptic plasticity and decreases prefrontal ERK2 phosphorylation
Hugues, S., Chessel, A., Léna, I., Marsault, R., & Garcia, R. (2006) · Synapse · doi:10.1002/syn.20291 · Cited by 114 · see citing works
Lesions of the periaqueductal gray and rostral ventromedial medulla disrupt antinociceptive but not cardiovascular aversive conditional responses
Helmstetter, F. J., & Tershner, S. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-11-07099.1994 · Cited by 109 · see citing works
Unconditioned stimulus pathways to the amygdala: effects of posterior thalamic and cortical lesions on fear conditioning
Lanuza, E., Nader, K., & LeDoux, J. E. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2003.12.034 · Cited by 108 · see citing works
Peripheral and intraamygdalar administration of the dopamine D-sub-1 receptor antagonist SCH 23390 blocks fear-potentiated startle but not shock reactivity or the shock sensitization of acoustic startle.
Greba, Q., & Kokkinidis, L. (2000) · Behavioral Neuroscience · doi:10.1037//0735-7044.114.2.262 · Cited by 107 · see citing works
Fear conditioning to tone, but not to context, is attenuated by lesions of the insular cortex and posterior extension of the intralaminar complex in rats.
Brunzell, D. H., & Kim, J. J. (2001) · Behavioral Neuroscience · doi:10.1037/0735-7044.115.2.365 · Cited by 103 · see citing works
Blockade of Endogenous Opioid Neurotransmission Enhances Acquisition of Conditioned Fear in Humans
Eippert, F., Bingel, U., Schoell, E. D., Yacubian, J., & Büchel, C. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.5336-07.2008 · Cited by 100 · see citing works
Gated Visual Input to the Central Auditory System
Gutfreund, Y., Zheng, W., & Knudsen, E. I. (2002) · Science · doi:10.1126/science.1073712 · Cited by 99 · see citing works
Opioid receptors in the midbrain periaqueductal gray regulate prediction errors during Pavlovian fear conditioning.
McNally, G. P., & Cole, S. (2006) · Behavioral Neuroscience · doi:10.1037/0735-7044.120.2.313 · Cited by 94 · see citing works
Self-citation
Peripheral and intraamygdalar administration of the dopamine D₁ receptor antagonist SCH 23390 blocks fear-potentiated startle but not shock reactivity or the shock sensitization of acoustic startle.
Greba, Q., & Kokkinidis, L. (2000) · Behavioral Neuroscience · doi:10.1037/0735-7044.114.2.262 · Cited by 94 · see citing works
Associative regulation of Pavlovian fear conditioning: Unconditioned stimulus intensity, incentive shifts, and latent inhibition.
Young, S. L., & Fanselow, M. S. (1992) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037//0097-7403.18.4.400 · Cited by 93 · see citing works
Opioid Receptors Regulate the Extinction of Pavlovian Fear Conditioning.
McNally, G. P., & Westbrook, R. F. (2003) · Behavioral Neuroscience · doi:10.1037/0735-7044.117.6.1292 · Cited by 91 · see citing works
Self-citation
Antinociception produced by mu opioid receptor activation in the amygdala is partly dependent on activation of mu opioid and neurotensin receptors in the ventral periaqueductal gray
Tershner, S. A., & Helmstetter, F. J. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02179-x · Cited by 90 · see citing works
Evidence of Pavlovian conditioned fear following electrical stimulation of the periaqueductal grey in the rat
Scala, G. D., Mana, M. J., Jacobs, W. J., & Phillips, A. G. (1987) · Physiology & Behavior · doi:10.1016/0031-9384(87)90185-5 · Cited by 89 · see citing works
Ascending and Descending Pathways in the Spinal Cord
Tracey, D. J. (2004) · Elsevier eBooks · doi:10.1016/b978-012547638-6/50008-0 · Cited by 85 · see citing works
Topographic commissural and descending projections of the habenula in the rat
Kim, U. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.21951 · Cited by 85 · see citing works
An electrophysiological characterization of the projection from the central nucleus of the amygdala to the periaqueductal gray of the rat: the role of opioid receptors
Gomez, T. M. D. C., & Behbehani, M. M. (1995) · Brain Research · doi:10.1016/0006-8993(95)00525-u · Cited by 84 · see citing works
Blocking, Unblocking, and Overexpectation of Fear: A Role for Opioid Receptors in the Regulation of Pavlovian Association Formation.
McNally, G. P., Pigg, M., & Weidemann, G. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.1.111 · Cited by 79 · see citing works
Self-citation
The neural correlates of negative prediction error signaling in human fear conditioning
Spoormaker, V. I., Andrade, K. C., Schröter, M. S., Sturm, A., Goya‐Maldonado, R., Sämann, P. G., & Czisch, M. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.09.042 · Cited by 78 · see citing works
Neural Correlates of Variations in Event Processing during Learning in Central Nucleus of Amygdala
Calu, D. J., Roesch, M. R., Haney, R. Z., Holland, P. C., & Schoenbaum, G. M. (2010) · Neuron · doi:10.1016/j.neuron.2010.11.019 · Cited by 67 · see citing works
Prefrontal afferents to the dorsal raphe nucleus in the rat
Gonçalves, L., Nogueira, M. I., Shammah‐Lagnado, S. J., & Metzger, M. (2008) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2008.11.012 · Cited by 66 · see citing works
Lesions of the habenula produce stress- and dopamine-dependent alterations in prepulse inhibition and locomotion
Heldt, S. A., & Ressler, K. J. (2006) · Brain Research · doi:10.1016/j.brainres.2005.12.053 · Cited by 65 · see citing works
Opioid Receptors in the Nucleus Accumbens Regulate Attentional Learning in the Blocking Paradigm
Iordanova, M. D., McNally, G. P., & Westbrook, R. F. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4679-05.2006 · Cited by 63 · see citing works
Self-citation
The role of prefrontal cortex in predictive fear learning.
Furlong, T. M., Cole, S., Hamlin, A. S., & McNally, G. P. (2010) · Behavioral Neuroscience · doi:10.1037/a0020739 · Cited by 58 · see citing works
Self-citation
Associative regulation of Pavlovian fear conditioning: Unconditioned stimulus intensity, incentive shifts, and latent inhibition.
Young, S. L., & Fanselow, M. S. (1992) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.18.4.400 · Cited by 58 · see citing works
Opioid antagonist impedes exposure.
Merluzzi, T. V., Taylor, C. B., Boltwood, M. D., & Götestam, K. G. (1991) · Journal of Consulting and Clinical Psychology · doi:10.1037/0022-006x.59.3.425 · Cited by 51 · see citing works
The midbrain periaqueductal gray and fear extinction: Opioid receptor subtype and roles of cyclic AMP, protein kinase A, and mitogen-activated protein kinase.
McNally, G. P., Lee, B.-W., Chiem, J. Y., & Choi, E. A. (2005) · Behavioral Neuroscience · doi:10.1037/0735-7044.119.4.1023 · Cited by 50 · see citing works
Self-citation
Dopamine activity in the nucleus accumbens modulates blocking in fear conditioning
Iordanova, M. D., Westbrook, R. F., & Killcross, S. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05195.x · Cited by 49 · see citing works
Regulation of extinction-related plasticity by opioid receptors in the ventrolateral periaqueductal gray matter
Parsons, R. G. (2010) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2010.00044 · Cited by 46 · see citing works
Opioid receptors mediate direct predictive fear learning: Evidence from one-trial blockingPreprint
Cole, S., & McNally, G. P. (2007) · Learning & Memory · doi:10.1101/lm.489507 · Cited by 39 · see citing works
Self-citation
Endogenous opiate system and systematic desensitization.
Egan, K. J., Carr, J. E., Hunt, D. D., & Adamson, R. (1988) · Journal of Consulting and Clinical Psychology · doi:10.1037//0022-006x.56.2.287 · Cited by 36 · see citing works
Facilitation of fear extinction by midbrain periaqueductal gray infusions of rb101(s), an inhibitor of enkephalin-degrading enzymes.
McNally, G. P. (2005) · Behavioral Neuroscience · doi:10.1037/0735-7044.119.6.1672 · Cited by 36 · see citing works
Self-citation
Expression of the IgLON cell adhesion molecules kilon and OBCAM in hypothalamic magnocellular neurons
Miyata, S., Funatsu, N., Matsunaga, W., Kiyohara, T., Sokawa, Y., & Maékawa, S. (2000) · The Journal of Comparative Neurology · doi:10.1002/1096-9861(20000814)424:1 · Cited by 35 · see citing works
The effect of the μ-opioid receptor antagonist naloxone on extinction of conditioned fear in the developing ratPreprint
Kim, J. H., & Richardson, R. (2009) · Learning & Memory · doi:10.1101/lm.1282309 · Cited by 35 · see citing works
The Roles of Endogenous Opioids in Fear Learning
McNally, G. P. (2009) · International Journal of Comparative Psychology · doi:10.46867/ijcp.2009.22.03.02 · Cited by 29 · see citing works
Self-citation
Temporal-difference prediction errors and Pavlovian fear conditioning: Role of NMDA and opioid receptors.
Cole, S., & McNally, G. P. (2007) · Behavioral Neuroscience · doi:10.1037/0735-7044.121.5.1043 · Cited by 29 · see citing works
Self-citation
Endogenous opiate system and systematic desensitization.
Egan, K. J., Carr, J. E., Hunt, D. D., et al. (1988) · Journal of Consulting and Clinical Psychology · doi:10.1037/0022-006x.56.2.287 · Cited by 29 · see citing works
Naltrexone renders one-session exposure therapy less effective: A controlled pilot study
Kozak, A. T., Spates, C. R., McChargue, D. E., Bailey, K. C., Schneider, K. L., & Liepman, M. R. (2006) · Journal of Anxiety Disorders · doi:10.1016/j.janxdis.2006.03.011 · Cited by 26 · see citing works
Opioid regulation of Pavlovian overshadowing in fear conditioning.
Zelikowsky, M., & Fanselow, M. S. (2010) · Behavioral Neuroscience · doi:10.1037/a0020083 · Cited by 21 · see citing works
The computational unit as an assembly of neurones: an implementation of an error correcting learning algorithm
McLaren, I. P. L. (1989) · Addison-Wesley Longman Publishing Co., Inc. eBooks · Cited by 19 · see citing works
Unblocking in Pavlovian fear conditioning.
Bradfield, L. A., & McNally, G. P. (2008) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.34.2.256 · Cited by 18 · see citing works
Self-citation
VII. Integrative Activity of the CNS
Frolkis, V. V., & Bezrukov, V. V. (2015) · Interdisciplinary topics in gerontology and geriatrics · doi:10.1159/000402955 · Cited by 14 · see citing works
Dopamine transmission in the amygdala modulates surprise in an aversive blocking paradigm.
Iordanova, M. D. (2010) · Behavioral Neuroscience · doi:10.1037/a0021111 · Cited by 13 · see citing works

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Research works printed but not linked: 2

[33]Pearce JM Mackintosh NJ Mitchell CJ LePelley ME Two theories of attention: a review and possible integration. Attention and Associative Learning 2010 11 40 Oxford
[112]Holland PC Maddux J-M Mitchell CJ LePelley ME Brain systems for attention in associative learning. Attention and Associative Learning 2010 305 350 Oxford

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Retrieval-Dependent Mechanisms Affecting Emotional Memory Persistence: Reconsolidation, Extinction, and the Space in Between
Vaverková, Z., Milton, A. L., & Merlo, E. (2020) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2020.574358 · Cited by 27 · see citing works

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Walker, D. L., & Davis, M. E. (2008) · Learning & Memory · doi:10.1101/lm.798908 · Cited by 67 · see citing works
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Lee, H. J., & Kim, J. J. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-20-08444.1998 · Cited by 310 · see citing works
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Traina, G., & Tuszyński, J. A. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242216327 · Cited by 18 · 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
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Frankland, P. W., & Josselyn, S. A. (2009) · Springer eBooks · doi:10.1007/978-0-387-75269-3_21 · Cited by 1 · see citing works

Authors: McNally, G. P., Johansen, J. P., & Blair, H. T.
Affiliations: UNSW Sydney (AU)
New York University (US)
University of California, Los Angeles (US)
Corresponding author: McNally, Gavan P.
ORCID: McNally, Gavan P.
Johansen, Joshua P.
Blair, Hugh T.
Venue: Trends in Neurosciences
Publisher: Elsevier BV
Published: 2011-06
Volume: 34
Issue: 6
Pages: 283-292
ISSN: 0166-2236 (ISSN-L)
DOI: 10.1016/j.tins.2011.03.005
PMC: PMC4245078
OpenAlex: W2023596252
Cited by: 298
References: 122
Citations by year: 2026: 13 · 2025: 10 · 2024: 45 · 2023: 19 · 2022: 15 · 2021: 20 · 2020: 21 · 2019: 20 · 2018: 14 · 2017: 22 · 2016: 22 · 2015: 26 · 2014: 13 · 2013: 15 · 2012: 20
FWCI: 1.38
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Trends in Neurosciences (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health
Australian Research Council
National Health and Medical Research Council
National Medical Research Council
National Institute of Mental Health (R01MH073700)
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: fear conditioning, prediction error, periaqueductal gray, fear learning, exposure therapy, anxiety disorders, fear extinction
MeSH terms: Amygdala, Animals, Conditioning, Classical, Fear, Humans, Learning, Neuronal Plasticity

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Placing prediction into the fear circuit

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