Aversive Prediction Error Signals in the Amygdala
Open accessAbstract
Prediction error signals are fundamental to learning. Here, in mice, we show that aversive prediction signals are found in the hemodynamic responses and theta oscillations recorded from the basolateral amygdala. During fear conditioning, amygdala responses evoked by footshock progressively decreased, whereas responses evoked by the auditory cue that predicted footshock concomitantly increased. Unexpected footshock evoked larger amygdala responses than expected footshock. The magnitude of the amygdala response to the footshock predicted behavioral responses the following day. The omission of expected footshock led to a decrease below baseline in the amygdala response suggesting a negative aversive prediction error signal. Thus, in mice, amygdala activity conforms to temporal difference models of aversive learning.
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?
Experiencing large prediction errors leads to learning over time.
“Available evidence indicates that experiencing large PEs leads to learning over time15,16.”
From Boundary effects of expectation in human pain perception (2019) · cites this paper as [16]
The Abstract says prediction-error signals are fundamental to learning, and the section ‘Relationship between amygdala signals and freezing behavior’ reports that mice with larger footshock-evoked amygdala responses showed better discrimination the following day. This supports a link between response magnitude and later learning, but the study does not establish that experiencing larger prediction errors causes learning generally. (LLM, conf=0.85)
Experimental — accuracy not yet measuredExperiencing PEs could, over time, change participants' association between the cue and the pain outcome.
“Furthermore, experiencing PEs could, over time, change participant’s association between the cue and the pain outcome15,16,29.”
From Boundary effects of expectation in human pain perception (2019) · cites this paper as [16]
The Summary of results says prediction errors are necessary for learning, and the Behavioral responses section reports that mice learned which cue predicted footshock over three days. This supports the proposed change in a cue–outcome association, but the study tested mice and footshock, not human participants and pain outcomes. (LLM, conf=0.85)
Experimental — accuracy not yet measuredSensitivity to painful stimulation can vary over time.
“Our interest in how perception changes across the experimental session was motivated by the observation that sensitivity to painful stimulation can vary over time15,16,28,29.”
From Boundary effects of expectation in human pain perception (2019) · cites this paper as [16]
The ‘Aversive prediction errors in amygdala hemodynamic responses’ section reports that mice’s amygdala responses to footshock decreased over three days of training. But the ‘Aversive prediction error signals in theta oscillations’ section attributes that decrease to expectation rather than simple habituation; the paper does not measure whether sensitivity to painful stimulation changed over time. (LLM, conf=0.82)
Experimental — accuracy not yet measured
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
NIH Image to ImageJ: 25 years of image analysis
Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012) · Nature Methods · doi:10.1038/nmeth.2089 · Cited by 64,638 · see citing works
A neural substrate of prediction and reward
Schultz, W., Dayan, P., & Montague, P. R. (1997) · Science · doi:10.1126/science.275.5306.1593 · Cited by 9,388 · see citing works
Neurophysiological investigation of the basis of the fMRI signal
Logothetis, N. K., Pauls, J., Augath, M., Trinath, T., & Oeltermann, A. (2001) · Nature · doi:10.1038/35084005 · Cited by 6,542 · see citing works
Brain magnetic resonance imaging with contrast dependent on blood oxygenation.
Ogawa, S., Lee, T. M., Kay, A. R., & Tank, D. W. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.24.9868 · Cited by 6,483 · see citing works
Beaton, A. E., & Keppel, G. (1975) · American Educational Research Journal · doi:10.2307/1162588 · Cited by 5,857 · see citing works
Theta oscillations in the hippocampus
Buzsáki, G. (2002) · Neuron · doi:10.1016/s0896-6273(02)00586-x · Cited by 3,332 · see citing works
Pearce, J. M., & Hall, G. (1980) · Psychological Review · doi:10.1037/0033-295x.87.6.532 · Cited by 3,023 · see citing works
Competitive Hebbian learning through spike-timing-dependent synaptic plasticity
Song, S., Miller, K. D., & Abbott, L. F. (2000) · Nature Neuroscience · doi:10.1038/78829 · Cited by 2,738 · see citing works
Design and Analysis: A Researcher's Handbook
Morgan, J. (2005) · Technometrics · doi:10.1198/tech.2005.s329 · Cited by 2,365 · see citing works
Brain magnetic resonance imaging with contrast-dependent oxygenation
Ogawa, S. (1990) · Medical Entomology and Zoology · Cited by 1,367 · see citing works
Entrainment of Neocortical Neurons and Gamma Oscillations by the Hippocampal Theta Rhythm
Sirota, A., Montgomery, S., Fujisawa, S., Isomura, Y., Zugaro, M., & Buzsáki, G. (2008) · Neuron · doi:10.1016/j.neuron.2008.09.014 · Cited by 1,015 · see citing works
Opponent interactions between serotonin and dopamine
Daw, N. D., Kakade, S., & Dayan, P. (2002) · Neural Networks · doi:10.1016/s0893-6080(02)00052-7 · Cited by 844 · see citing works
Amygdalar and Hippocampal Theta Rhythm Synchronization During Fear Memory Retrieval
Seidenbecher, T., Laxmi, T. R., Stork, O., & Pape, H.-C. (2003) · Science · doi:10.1126/science.1085818 · Cited by 728 · 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
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
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
From Fear to Safety and Back: Reversal of Fear in the Human Brain
Schiller, D., Levy, I., Niv, Y., LeDoux, J. E., & Phelps, E. A. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.2265-08.2008 · Cited by 429 · see citing works
Measurement of Dissolved Oxygen
Hitchman, M. L. (1978) · CERN Document Server (European Organization for Nuclear Research) · Cited by 415 · see citing works
Differential roles of human striatum and amygdala in associative learning
Li, J., Schiller, D., Schoenbaum, G. M., Phelps, E. A., & Daw, N. D. (2011) · Nature Neuroscience · doi:10.1038/nn.2904 · Cited by 364 · see citing works
Single-Neuron Activity and Tissue Oxygenation in the Cerebral Cortex
Thompson, J. K., Peterson, M. R., & Freeman, R. D. (2003) · Science · doi:10.1126/science.1079220 · Cited by 358 · 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
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
Maren, S., Aharonov, G., & Fanselow, M. S. (1996) · Behavioral Neuroscience · doi:10.1037//0735-7044.110.4.718 · Cited by 308 · see citing works
Placing prediction into the fear circuit
McNally, G. P., Johansen, J. P., & Blair, H. T. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.03.005 · Cited by 298 · see citing works
Network Oscillations: Emerging Computational Principles
Sejnowski, T. J., & Paulsen, O. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.3737-05d.2006 · Cited by 284 · see citing works
Maren, S., Aharonov, G., & Fanselow, M. S. (1996) · Behavioral Neuroscience · doi:10.1037/0735-7044.110.4.718 · Cited by 267 · see citing works
Paré, D., & Collins, D. R. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-07-02701.2000 · Cited by 262 · see citing works
Two Dimensions of Value: Dopamine Neurons Represent Reward But Not Aversiveness
Fiorillo, C. D. (2013) · Science · doi:10.1126/science.1238699 · Cited by 203 · see citing works
Paré, D., Pape, H., & Dong, J. (1995) · Journal of Neurophysiology · doi:10.1152/jn.1995.74.3.1179 · Cited by 147 · see citing works
Menon, M., Jensen, J., Vitcu, I., Graff‐Guerrero, A., Crawley, A. P., Smith, M. A., & Kapur, S. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.10.020 · Cited by 145 · see citing works
Offenhauser, N., Thomsen, K., Caesar, K., & Lauritzen, M. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2005.082776 · Cited by 143 · see citing works
Dunsmoor, J. E., Bandettini, P. A., & Knight, D. C. (2007) · Behavioral Neuroscience · doi:10.1037/0735-7044.121.4.635 · Cited by 137 · see citing works
Optimized 3 T EPI of the amygdalae
Robinson, S., Windischberger, C., Rauscher, A., & Moser, E. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2003.12.048 · Cited by 133 · see citing works
Linear sweep voltammetry with carbon paste electrodes in the rat striatum
O'Neill, R. D., Grünewald, R. A., Fillenz, M., & Albery, W. J. (1982) · Neuroscience · doi:10.1016/0306-4522(82)90009-4 · Cited by 133 · see citing works
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
Two Types of Intrinsic Oscillations in Neurons of the Lateral and Basolateral Nuclei of the Amygdala
Pape, H., Paré, D., & Driesang, R. B. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.79.1.205 · Cited by 114 · see citing works
Cerebral Correlates of Salient Prediction Error for Different Rewards and Punishments
Metereau, E., & Dreher, J.-C. (2013) · Cerebral Cortex · doi:10.1093/cercor/bhs037 · Cited by 114 · see citing works
Narayanan, R. T., Seidenbecher, T., Kluge, C., Bergado, J. A., Stork, O., & Pape, H. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05437.x · Cited by 111 · see citing works
McNally, G. P., & Cole, S. (2006) · Behavioral Neuroscience · doi:10.1037/0735-7044.120.2.313 · Cited by 94 · see citing works
A computer controlled analysis of freezing behaviour
Richmond, M. A., Murphy, C. A., Pouzet, B., Schmid, P., Rawlins, J. N. P., & Feldon, J. (1998) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(98)00150-2 · Cited by 90 · 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
The ins and outs of fMRI signals
Logothetis, N. K. (2007) · Nature Neuroscience · doi:10.1038/nn1007-1230 · Cited by 82 · see citing works
Lowry, J. P., Boutelle, M. G., & Fillenz, M. (1997) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(96)00140-9 · Cited by 82 · see citing works
Self-citationMcHugh, S. B., Fillenz, M., Lowry, J. P., Rawlins, J. N. P., & Bannerman, D. M. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07497.x · Cited by 80 · see citing works
Self-citationMorawetz, C., Holz, P., Lange, C., Baudewig, J., Weniger, G., Irle, E., & Dechent, P. (2007) · Magnetic Resonance Imaging · doi:10.1016/j.mri.2007.04.014 · Cited by 74 · see citing works
Heldt, S. A., & Ressler, K. J. (2006) · Brain Research · doi:10.1016/j.brainres.2005.12.053 · Cited by 65 · see citing works
Bolger, F. B., McHugh, S. B., Bennett, R., Li, J., Ishiwari, K., François, J., Conway, M. W., Gilmour, G., Bannerman, D. M., Fillenz, M., et al. (2010) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2010.11.013 · Cited by 65 · see citing works
Self-citationNorbury, R., Selvaraj, S., Taylor, M. J., Harmer, C., & Cowen, P. J. (2010) · Psychological Medicine · doi:10.1017/s0033291709990596 · Cited by 62 · see citing works
Lowry, J. P., Griffin, K., McHugh, S. B., Lowe, A., Tricklebank, M. D., & Sibson, N. R. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.04.187 · Cited by 58 · see citing works
Self-citationNeural mechanisms underlying the conditioned diminution of the unconditioned fear response
Wood, K. H., Hoef, L. V., & Knight, D. C. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.12.048 · Cited by 47 · see citing works
Neurobiological Mechanisms Underlying the Blocking Effect in Aversive Learning
Eippert, F., Gamer, M., & Büchel, C. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.1210-12.2012 · Cited by 41 · see citing works
Barkus, C., Line, S. J., Huber, A., Capitão, L. P., Lima, J., Jennings, K. A., Lowry, J., Sharp, T., Bannerman, D. M., & McHugh, S. B. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.09.003 · Cited by 35 · see citing works
Self-citationLi, J., Bravo, D. S., Upton, A. L., Gilmour, G., Tricklebank, M. D., Fillenz, M., Martin, C. J., Lowry, J. P., Bannerman, D. M., & McHugh, S. B. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07927.x · Cited by 29 · see citing works
Self-citationOrganization of Neural Systems for Aversive Information Processing: Pain, Error, and Punishment
Kobayashi, S. (2012) · Frontiers in Neuroscience · doi:10.3389/fnins.2012.00136 · Cited by 27 · see citing works
McHugh, S. B., Marques–Smith, A., Li, J., Rawlins, J. N. P., Lowry, J., Conway, M. W., Gilmour, G., Tricklebank, M. D., & Bannerman, D. M. (2012) · European Journal of Neuroscience · doi:10.1111/ejn.12057 · Cited by 20 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
The neural bases of emotion regulation
Etkin, A., Büchel, C., & Gross, J. J. (2015) · Nature Reviews Neuroscience · doi:10.1038/nrn4044 · Cited by 1,244 · see citing works
Encoding of fear learning and memory in distributed neuronal circuits
Herry, C., & Johansen, J. P. (2014) · Nature Neuroscience · doi:10.1038/nn.3869 · Cited by 474 · see citing works
Common brain mechanisms of chronic pain and addiction
Elman, I., & Borsook, D. (2016) · Neuron · doi:10.1016/j.neuron.2015.11.027 · Cited by 303 · see citing works
Expectancies as core features of mental disorders
Rief, W., Glombiewski, J. A., Gollwitzer, M., Schubö, A., Schwarting, R. K. W., & Thorwart, A. (2015) · Current Opinion in Psychiatry · doi:10.1097/yco.0000000000000184 · Cited by 235 · see citing works
Functional dissociation of stimulus intensity encoding and predictive coding of pain in the insula
Geuter, S., Boll, S., Eippert, F., & Büchel, C. (2017) · eLife · doi:10.7554/elife.24770 · Cited by 184 · see citing works
A Discrete Dorsal Raphe to Basal Amygdala 5-HT Circuit Calibrates Aversive Memory
Sengupta, A., & Holmes, A. (2019) · Neuron · doi:10.1016/j.neuron.2019.05.029 · Cited by 112 · see citing works
Developing treatments for cognitive deficits in schizophrenia: The challenge of translation
Young, J. W., & Geyer, M. (2014) · Journal of Psychopharmacology · doi:10.1177/0269881114555252 · Cited by 110 · see citing works
The influence of subcortical shortcuts on disordered sensory and cognitive processing.
McFadyen, J., Dolan, R. J., & Garrido, M. I. (2020) · Nature Reviews Neuroscience · doi:10.1038/s41583-020-0287-1 · Cited by 91 · see citing works
Approach-Avoidance Decisions Under Threat: The Role of Autonomic Psychophysiological States
Livermore, J. J. A., Klaassen, F. H., Bramson, B., Hulsman, A. M., Meijer, S. W., Held, L. K., Klumpers, F., de Voogd, L. D., & Karin Roelofs, A. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.621517 · Cited by 100 · see citing works
Concepts, goals and the control of survival-related behaviors
Feldman Barrett, L., & Finlay, B. L. (2018) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2018.10.001 · Cited by 89 · see citing works
Levy, I., & Schiller, D. (2021) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2020.11.007 · Cited by 95 · see citing works
Dissociable Learning Processes Underlie Human Pain Conditioning
Zhang, S., Mano, H., Ganesh, G., Robbins, T. W., & Seymour, B. (2015) · Current Biology · doi:10.1016/j.cub.2015.10.066 · Cited by 84 · see citing works
Human Pavlovian fear conditioning conforms to probabilistic learning
Tzovara, A., Korn, C. W., & Bach, D. R. (2018) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1006243 · Cited by 75 · see citing works
Κube, T., Glombiewski, J. A., Gall, J., Touissant, L., Gärtner, T., & Rief, W. (2019) · Journal of Affective Disorders · doi:10.1016/j.jad.2019.03.027 · Cited by 67 · see citing works
Boundary effects of expectation in human pain perception
Hird, E. J., Charalambous, C., El-Deredy, W., Jones, A. K. P., & Talmi, D. (2019) · Scientific Reports · doi:10.1038/s41598-019-45811-x · Cited by 68 · see citing works
Delusions and prediction error: clarifying the roles of behavioural and brain responses
Corlett, P. R., & Fletcher, P. C. (2015) · Cognitive Neuropsychiatry · doi:10.1080/13546805.2014.990625 · Cited by 63 · see citing works
A Central Amygdala-Substantia Innominata Neural Circuitry Encodes Aversive Reinforcement Signals.
Cui, Y., Lv, G., Jin, S., Peng, J., Yuan, J., He, X.-B., Gong, H., Xu, F.-Q., Xu, T.-H., & Li, H. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.10.062 · Cited by 59 · see citing works
Neural substrates of appetitive and aversive prediction error
Iordanova, M. D., Yau, J. O.-Y., McDannald, M. A., & Corbit, L. H. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.10.029 · Cited by 60 · see citing works
Jarcho, J. M., Davis, M. M., Shechner, T., Degnan, K. A., Henderson, H. A., Stoddard, J., Fox, N. A., Leibenluft, E., Pine, D. S., & Nelson, E. E. (2016) · Psychological Science · doi:10.1177/0956797616638319 · Cited by 57 · see citing works
Dopamine-associated cached values are not sufficient as the basis for action selection
Hollon, N. G., Arnold, M. M., Gan, J. O., Walton, M. E., & Phillips, P. E. M. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1419770111 · Cited by 52 · see citing works
Modelling posttraumatic stress disorders in animals
Török, B., Sipos, E., Pivac, N., & Zelena, D. (2018) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2018.11.013 · Cited by 52 · see citing works
Distinct Processing of Aversive Experience in Amygdala Subregions
Michely, J., Rigoli, F., Rutledge, R. B., Hauser, T. U., & Dolan, R. J. (2019) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2019.07.008 · Cited by 46 · see citing works
The Rescorla-Wagner model, prediction error, and fear learning
Yau, J. O.-Y., & McNally, G. P. (2023) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2023.107799 · Cited by 45 · see citing works
Adaptive contextualization: a new role for the default mode network in affective learning
Marstaller, L., Burianová, H., & Reutens, D. C. (2017) · Human Brain Mapping · doi:10.1002/hbm.23442 · Cited by 37 · 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
Brain Mechanisms Controlling Pavlovian Fear Conditioning
Yau, J., & McNally, G. (2018) · Journal of Experimental Psychology: Animal Learning and Cognition · doi:10.1037/xan0000181 · Cited by 23 · see citing works
The Roles of Basolateral Amygdala Parvalbumin Neurons in Fear Learning
Yau, J. O.-Y., Chaichim, C., Power, J., & McNally, G. P. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.2461-20.2021 · Cited by 34 · see citing works
Pain, from perception to action: A computational perspective
Chen, Z. S., & Wang, J. (2022) · iScience · doi:10.1016/j.isci.2022.105707 · Cited by 35 · see citing works
Serotonergic neuromodulation of synaptic plasticity
Higa, G. S. V., Viana, F. J. C., Francis-Oliveira, J., Cruvinel, E., Franchin, T. S., Marcourakis, T., Ulrich, H., & De Pasquale, R. (2024) · Neuropharmacology · doi:10.1016/j.neuropharm.2024.110036 · Cited by 29 · see citing works
Dopamine induces fear extinction by activating the reward-responding amygdala neurons
Zhang, X., Flick, K., Rizzo, M., Pignatelli, M., & Tonegawa, S. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2501331122 · Cited by 26 · see citing works
Ho, S.-H. S., Muzik, M., Rosenblum, K. L., Morelen, D. M., Nakamura, Y., & Swain, J. E. (2020) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2020.568824 · Cited by 28 · see citing works
Insensitivity to loss predicts apathy in huntington's disease
Mclauchlan, D., Lancaster, T., Craufurd, D., Linden, D. E. J., & Rosser, A. (2019) · Movement Disorders · doi:10.1002/mds.27787 · Cited by 21 · see citing works
McHugh, S. B., Barkus, C., Lima, J., Glover, L. R., Sharp, T., & Bannerman, D. M. (2015) · Genes Brain & Behavior · doi:10.1111/gbb.12215 · Cited by 24 · see citing works
Self-citationEarly 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
Disrupted reinforcement learning during post-error slowing in ADHD
Chevrier, A., Bhaijiwala, M., Lipszyc, J., Cheyne, D., Graham, S., & Schachar, R. (2019) · PLOS ONE · doi:10.1371/journal.pone.0206780 · Cited by 21 · see citing works
Enhanced discriminative aversive learning and amygdala responsivity in 5-HT transporter mutant mice
Lima, J., Sharp, T., Bannerman, D. M., & McHugh, S. B. (2019) · Translational Psychiatry · doi:10.1038/s41398-019-0476-8 · Cited by 20 · see citing works
Self-citationDirect serotonin release in humans shapes aversive learning and inhibition
Colwell, M., Tagomori, H., Shang, F., Cheng, H. I., Wigg, C., Browning, M. D., Cowen, P. J., Murphy, S. E., & Harmer, C. J. (2024) · Nature Communications · doi:10.1038/s41467-024-50394-x · Cited by 18 · see citing works
Learning rules for aversive associative memory formation
Ozawa, T., & Johansen, J. P. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.02.010 · Cited by 22 · see citing works
Retrorubral field is a hub for diverse threat and aversive outcome signals
Moaddab, M., & McDannald, M. A. (2021) · Current Biology · doi:10.1016/j.cub.2021.02.055 · Cited by 15 · see citing works
He, Z., Jiang, Y., Gu, S., Wu, D., Qin, D., Feng, G., Ma, X., Huang, J. H., & Wang, F. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.713762 · Cited by 17 · see citing works
Cortico-Brainstem Mechanisms of Biased Perceptual Decision-Making in the Context of Pain
Wiech, K., Eippert, F., Vandekerckhove, J., Zaman, J., Placek, K., Tuerlinckx, F., Vlaeyen, J. W. S., & Tracey, I. (2021) · Journal of Pain · doi:10.1016/j.jpain.2021.11.006 · Cited by 14 · see citing works
Egorova, N., Benedetti, F., Gollub, R. L., & Kong, J. (2019) · European Journal of Pain · doi:10.1002/ejp.1510 · Cited by 14 · see citing works
Modulation of aversive value coding in the vertebrate and invertebrate brain
Perisse, E., Miranda, M., & Trouche, S. G. (2023) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2023.102696 · Cited by 13 · see citing works
Decision-Making in Anxiety and Its Disorders
Grupe, D. W. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-805308-9.00026-9 · Cited by 13 · see citing works
Marstaller, L., Burianová, H., & Reutens, D. C. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2016.04.008 · Cited by 11 · see citing works
Czekalla, N., Schröder, A., Mayer, A. V., Stierand, J., Stolz, D. S., Κube, T., Korn, C. W., Wilhelm, I., Klein, J. P., Paulus, F. M., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.05.09.593087 · Cited by 10 · see citing works
Kalbe, F., & Schwabe, L. (2021) · Cerebral Cortex · doi:10.1093/cercor/bhab402 · Cited by 10 · see citing works
Klaassen, F. H., de Voogd, L. D., Hulsman, A. M., O’Reilly, J. X., Klumpers, F., Figner, B., & Karin Roelofs, A. (2024) · Communications Biology · doi:10.1038/s42003-024-06267-6 · Cited by 9 · see citing works
Irrelevant Threats Linger and Affect Behavior in High Anxiety
Aberg, K. C., Toren, I., & Paz, R. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.1186-22.2022 · Cited by 8 · see citing works
Li, J., Schwarz, A. J., & Gilmour, G. (2015) · Current topics in behavioral neurosciences · doi:10.1007/7854_2016_1 · Cited by 7 · see citing works
Evidence for predictions established by phantom sound
Qi, Y., Guo, Z.-H., Guo, X., Guan, R., Luo, B., Sun, J., Wang, M., Li, H., & Chen, L. (2022) · NeuroImage · doi:10.1016/j.neuroimage.2022.119766 · Cited by 5 · see citing works
Monitoring deep brain stimulation by measuring regional brain oxygen responses in freely moving mice
Bazzu, G., Serra, P. A., Hamelink, R., Feenstra, M. G. P., Willuhn, I., & Denys, D. A. J. P. (2019) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2019.01.012 · Cited by 5 · see citing works
Valmiki, M., Fawzy, P., Valmiki, S., Aid, M., Chaitou, A. R., Zahid, M., & Khan, S. (2021) · Cureus · doi:10.7759/cureus.13718 · Cited by 5 · see citing works
Dopamine and Its Actions in the Basal Ganglia System
Bullock, D. H. (2016) · Innovations in cognitive neuroscience · doi:10.1007/978-3-319-42743-0_5 · Cited by 3 · see citing works
Real-time changes in hippocampal energy demands during a spatial working memory task
Kealy, J., Bennett, R., Woods, B., & Lowry, J. P. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.02.034 · Cited by 3 · see citing works
Self-citationHailwood, J. M., Gilmour, G., Robbins, T. W., Saksida, L. M., Bussey, T. J., Marston, H. M., & Gastambide, F. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.14150 · Cited by 3 · see citing works
Duggins, P., & Eliasmith, C. (2024) · European Journal of Neuroscience · doi:10.1111/ejn.16338 · Cited by 2 · see citing works
Asymmetric representation of aversive prediction errors in Pavlovian threat conditioningPreprint
Ojala, K. E., Tzovara, A., Poser, B. A., Lutti, A., & Bach, D. R. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.07.10.197665 · Cited by 2 · see citing works
The Rescorla-Wagner model, prediction error, and fear learningPreprint
McNally, G. P., & Yau, J. O.-Y. (2023) · doi:10.31234/osf.io/csj56 · Cited by 2 · see citing works
Cheon, M., Kim, W., & Chung, C. (2025) · The FASEB Journal · doi:10.1096/fj.202403158r · Cited by 1 · see citing works
School Social Relationships and Brain Functioning
Asscheman, J. S., & Deater-Deckard, K. D. (2022) · Springer eBooks · doi:10.1007/978-3-031-07109-6_8 · Cited by 1 · see citing works
Basolateral amygdala parvalbumin neurons report aversive prediction error to constrain fear learningPreprint
Yau, J. O.-Y., Chaichim, C., Power, J., & McNally, G. P. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.09.22.307561 · Cited by 1 · see citing works
Lima, J., Sharp, T., Taylor, A. M., Bannerman, D. M., & McHugh, S. B. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/154690
Self-citationShortcuts for fear in hierarchical visual systems
McFadyen, J. (2019) · The University of Queensland · doi:10.14264/uql.2019.269
Sato, S., Kato, T., & Toyoizumi, T. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.01.28.702194
Young, W., Kal, E. C., Ellmers, T. J., Maslivec, A., Wilson, M., Russo, Y., Evans, K., & Norris, M. (2026) · Research Square · doi:10.21203/rs.3.rs-9897696/v1
- Authors
- McHugh, S. B., Barkus, C., Huber, A., Capitao, L., Lima, J., Lowry, J. P., & Bannerman, D. M.
- Affiliations
- University of Oxford (GB)
- National University of Ireland, Maynooth (IE)
- Venue
- Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2014-07-02
- Volume
- 34
- Issue
- 27
- Pages
- 9024-9033
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC4078079
- OpenAlex
- W2099499810
- Cited by
- 68
- References
- 55
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 5 · 2023: 4 · 2022: 4 · 2021: 9 · 2020: 6 · 2019: 10 · 2018: 6 · 2017: 4 · 2016: 6 · 2015: 7 · 2014: 3
- FWCI
- 3.72
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by
- Locations
- Journal of Neuroscience (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Wellcome Trust (087736, 074385)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- basolateral amygdala, fear conditioning, temporal difference learning, footshock, auditory cues, hemodynamic response, theta oscillations, aversive learning, mice
- MeSH terms
- Acoustic Stimulation, Amygdala, Animals, Avoidance Learning, Conditioning, Classical, Discrimination Learning, Electroshock, Fear, Hemodynamics, Locomotion, Male, Mice, Inbred CBA, Mice, Inbred C57BL, Theta Rhythm, Freezing Reaction, Cataleptic, Mice, Anticipation, Psychological
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
