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Conscious and unconscious emotional learning in the human amygdala

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Morris, J. S., Öhman, A., Dolan, R. J.·1998·Nature

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Abstract

If subjects are shown an angry face as a target visual stimulus for less than forty milliseconds and are then immediately shown an expressionless mask, these subjects report seeing the mask but not the target. However, an aversively conditioned masked target can elicit an emotional response from subjects without being consciously perceived. Here we study the mechanism of this unconsciously mediated emotional learning. We measured neural activity in volunteer subjects who were presented with two angry faces, one of which, through previous classical conditioning, was associated with a burst of white noise. In half of the trials, the subjects' awareness of the angry faces was prevented by backward masking with a neutral face. A significant neural response was elicited in the right, but not left, amygdala to masked presentations of the conditioned angry face. Unmasked presentations of the same face produced enhanced neural activity in the left, but not right, amygdala. Our results indicate that, first, the human amygdala can discriminate between stimuli solely on the basis of their acquired behavioural significance, and second, this response is lateralized according to the subjects' level of awareness of the stimuli.

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BackgroundResultInfluential
A brain-computer interface for potential non-verbal facial communication based on EEG signals related to specific emotions
Kashihara, K. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00244 · Cited by 55
“During the experiments, a loudspeaker was placed behind a participant and a 100-dB white noise burst was used as the auditory stimulus (Morris et al., 1998).”
BackgroundMethod
New insights in the limbic modulation of visual inputs: The role of the inferior longitudinal fasciculus and the Li-Am bundle
Latini, F. (2014) · Neurosurgical Review · doi:10.1007/s10143-014-0583-1 · Cited by 53
Task-irrelevant angry faces capture attention in visual search while modulated by resources.
Huang, S.-L., Chang, Y.-C., & Chen, Y.-J. (2011) · Emotion · doi:10.1037/a0022763 · Cited by 53
Elevated responses to constant facial emotions in different faces in the human amygdala: an fMRI study of facial identity and expression
Gläscher, J. P., Tüscher, O., Weiller, C., & Büchel, C. (2004) · BMC Neuroscience · doi:10.1186/1471-2202-5-45 · Cited by 54
“Furthermore, we expected that constant fearful expressions (shown in different identities) would elicit the strongest amygdala activation given the evidence from lesion and imaging studies that this expression is a particularly potent activator of the amygdala [11,12,17,30,31].”
Background
Gender differences in brain activity generated by unpleasant word stimuli concerning body image: an fMRI study
Shirao, N., Okamoto, Y., Mantani, T., Okamoto, Y., & Yamawaki, S. (2005) · The British Journal of Psychiatry · doi:10.1192/bjp.186.1.48 · Cited by 54
“Human lesion and imaging studies consistently indicate that the amygdala is concerned in fear conditioning (Morris et al, 1998), in the recognition of fearful facial expressions (Adolphs, 1999) and in the evocation of fearful emotional responses from direct stimulation (Halgren et al, 1978).”
Background
The importance of low spatial frequency information for recognising fearful facial expressions
Mermillod, M., Vuilleumier, P. O., Peyrin, C., Alleysson, D., & Marendaz, C. (2008) · Connection Science · doi:10.1080/09540090802213974 · Cited by 52
“Furthermore, both neuroimaging (Morris, Ohman and Dolan 1998 ) and behavioural results (Esteves and Ohman 1993 ) indicate that amygdala responses to fearful faces may persist when the faces are masked and not consciously processed.”
Very early modulation of brain responses to neutral faces by a single prior association with an emotional context: Evidence from MEG
Morel‐Kohlmeyer, S., Beaucousin, V., Perrin, M., & George, N. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.04.016 · Cited by 57
“…the left amygdala would rather be involved in the explicit evaluation of emotional – mainly negative – events (e.g. Cornwell et al., 2008; Glascher and Adolphs, 2003; Hardee et al., 2008; Hung et al., 2010; Luo et al., 2009; Morris et al., 1998; Pegna et al., 2005; see Gainotti, 2012 for a review).”
Depersonalization Disorder: A Functional Neuroanatomical Perspective
Phillips, M. L., & Sierra, M. (2003) · Stress · doi:10.1080/1025389031000138538 · Cited by 62
“…et al., 2000; Dolan et al., 2000), in the enhanced perception of emotionallysalient information (Anderson and Phelps, 2001), and in the response to presentations of fearful and angry facial expressions of which the observer had no conscious awareness (Morris et al., 1998b; Whalen et al., 1998).”
Background
Amygdala function in emotion, cognition, and behavior
Domínguez‐Borràs, J., & Vuilleumier, P. O. (2022) · Handbook of clinical neurology · doi:10.1016/b978-0-12-823493-8.00015-8 · Cited by 56
Relationships between temperament dimensions in personality and unconscious emotional responses.
Yoshino, A., Kimura, Y., Yoshida, T., Takahashi, Y., & Nomura, S. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.09.027 · Cited by 49
Subconscious facial expression mimicry is preserved in older adulthood.
Bailey, P. E., & Henry, J. D. (2009) · Psychology and Aging · doi:10.1037/a0015789 · Cited by 54
A parametric study of fear generalization to faces and non-face objects: relationship to discrimination thresholds
Holt, D. J., Boeke, E. A., Wolthusen, R. P. F., Nasr, S., Milad, M. R., & Tootell, R. B. H. (2014) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2014.00624 · Cited by 51
“Alternatively, autonomic responses might be more sensitive than perception in some cases, based on prior demonstrations of sub-threshold summation (Kulikowski and King-Smith, 1973; To et al., 2011) and “unconscious” fear responses (Morris et al., 1998; Whalen et al., 1998).”
A Role for the Human Amygdala in Higher Cognition
Schaefer, A., & Gray, J. R. (2007) · Reviews in the Neurosciences · doi:10.1515/revneuro.2007.18.5.355 · Cited by 57
Association of Amygdala Development With Different Forms of Anxiety in Autism Spectrum Disorder
Andrews, D. S., Aksman, L., Kerns, C. M., Lee, J. K., Winder‐Patel, B., Harvey, D. J., Waizbard‐Bartov, E., Heath, B. E., Solomon, M., Rogers, S. J., et al. (2022) · Biological Psychiatry · doi:10.1016/j.biopsych.2022.01.016 · Cited by 51
“Indeed, emotional processing functional imaging studies suggest the right amygdala to be more engaged in rapid processing of potentially threatening stimuli and the left in prolonged stimulus evaluation (67,69,70).”
Background
Necker’s smile: Immediate affective consequences of early perceptual processes
Topolinski, S., Erle, T. M., & Reber, R. (2015) · Cognition · doi:10.1016/j.cognition.2015.03.004 · Cited by 50
Perception of emotion in abstract artworks
Melcher, D., & Bacci, F. (2013) · Progress in brain research · doi:10.1016/b978-0-444-63287-6.00010-5 · Cited by 54
Amygdala responses to masked and low spatial frequency fearful faces: a preliminary fMRI study in panic disorder
Ottaviani, C., Cevolani, D., Nucifora, V., Borlimi, R., Agati, R., Leonardi, M., Plato, G. D., & Brighetti, G. (2012) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2011.12.010 · Cited by 51
“Consistent with an evolutionary argument, previous functional magnetic resonance imaging (fMRI) studies demonstrated that the amygdala is activated in response to fearful faces even when conscious recognition is prevented by backward masking (Morris et al., 1998; Whalen et al., 1998; Adolphs, 2008).”
Transcranial magnetic stimulation of medial prefrontal cortex modulates face expressions processing in a priming task
Mattavelli, G. C., Cattaneo, Z., & Papagno, C. (2011) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2011.01.038 · Cited by 53
The link between optimism bias and attention bias: A neurocognitive perspective
Kress, L., & Aue, T. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.07.016 · Cited by 56
“Critical brain structures underlying emotional memories usually consist of the amygdala (Morris et al., 1998), the insula (Hamann, 2001), and the septo-hippocampal system”
Background
Visual Attention and Emotional Perception
Pessoa, L., & Ungerleider, L. G. (2005) · Neurobiology of Attention · doi:10.1016/b978-012375731-9/50032-x · Cited by 49
“How does one reconcile this view with the finding that amygdala responses are evoked by masked faces of which subjects are presumably unaware (Morris et al., 1998; Whalen et al., 1998)? In such instances, it is possible that attentional resources to the masked stimuli were not sufficiently reduced by a competing task.”
Background
Impaired identity recognition of faces with emotional expressions in body dysmorphic disorder
Feusner, J. D., Bystritsky, A., Hellemann, G., & Bookheimer, S. Y. (2010) · Psychiatry Research · doi:10.1016/j.psychres.2009.01.016 · Cited by 49
“processing of threat-related information is highly prioritized and may occur automatically, even when the threat is not explicitly attended (Morris et al. 1998;Whalen et al. 1998;Vuilleumier and Schwartz 2001).”
Background
Functional Mapping of Dynamic Happy and Fearful Facial Expression Processing in Adolescents
Rahko, J. S., Paakki, J., Starck, T., Nikkinen, J., Remes, J. J., Hurtig, T. M., Kuusikko‐Gauffin, S., Mattila, M., Jussila, K. K., Jansson-Verkasalo, E. M., et al. (2010) · Brain Imaging and Behavior · doi:10.1007/s11682-010-9096-x · Cited by 50
Not What You Expect: Experience but not Expectancy Predicts Conditioned Responses in Human Visual and Supplementary Cortex
Moratti, S., & Keil, A. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp052 · Cited by 49
“…autonomic responses such as skin conductance (Hamm and Vaitl 1996; Hamm et al. 2003; Knight et al. 2003) and conditioned amygdala activations (Morris et al. 1998, 1999, 2001; Whalen et al. 1998; Williams et al. 2004) have been shown to be independent from conscious awareness of the CS--US…”
Background
Pavlovian aversive and appetitive odor conditioning in humans: subjective, peripheral, and electrocortical changes
Hermann, C., Ziegler, S., Birbaumer, N., & Flor, H. (2000) · Experimental Brain Research · doi:10.1007/s002210000343 · Cited by 51
In the Face of Emotions: Event-Related Potentials in Supraliminal and Subliminal Facial Expression Recognition
Balconi, M., & Lucchiari, C. (2005) · Genetic Social and General Psychology Monographs · doi:10.3200/mono.131.1.41-69 · Cited by 48
In Harm’s Way: On Preferential Response to Threatening Stimuli
March, D. S., Gaertner, L., & Olson, M. A. (2017) · Personality and Social Psychology Bulletin · doi:10.1177/0146167217722558 · Cited by 48
Effects of amygdala lesions on sleep in rhesus monkeys
Benca, R. M., Obermeyer, W. H., Shelton, S. E., Droster, J., & Kalin, N. H. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02761-x · Cited by 51
Distinct functional connectivities predict clinical response with emotion regulation therapy
Fresco, D. M., Roy, A. K., Adelsberg, S., Seeley, S., García-Lesy, E., Liston, C., & Mennin, D. S. (2017) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2017.00086 · Cited by 43
“…targets of treatment for GAD with and without co-occurring MDD. Keywords: generalized anxiety disorder, major depressive disorder, worry, somatic anxiety, decentering, resting state functional connectivity Frontiers in Human Neuroscience | www.frontiersin.org 1 March 2017 | Volume 11 | Article 86”
Background
Rapid, high-frequency, and theta-coupled gamma oscillations in the inferior occipital gyrus during face processing
Sato, W., Kochiyama, T., Uono, S., Matsuda, K., Usui, K., Inoue, Y., & Toichi, M. (2014) · Cortex · doi:10.1016/j.cortex.2014.02.024 · Cited by 52
“Neuroimaging studies have suggested that such rapid emotional expression processing is related to amygdala activity (e.g., Morris et al., 1998).”
Background
Automatic Neural Processing of Disorder-Related Stimuli in Social Anxiety Disorder: Faces and More
Schulz, C., Mothes‐Lasch, M., & Straube, T. (2013) · Frontiers in Psychology · doi:10.3389/fpsyg.2013.00282 · Cited by 49
“We hope that especially this section stimulates future research on the neurobiology of SAD and automatic threat processing in SAD in particular.”
Background
The two sides of beauty: Laterality and the duality of facial attractiveness
Franklin, R. G., & Adams, R. B. (2009) · Brain and Cognition · doi:10.1016/j.bandc.2009.10.002 · Cited by 47
Attentional capture by emotional faces is contingent on attentional control settings
Barratt, D., & Bundesen, C. (2012) · Cognition & Emotion · doi:10.1080/02699931.2011.645279 · Cited by 53
A comparison of selective attention and facial processing biases in typically developing children who are high and low in self-reported trait anxiety
Richards, A., French, C. C., Nash, G., Hadwin, J. A., & Donnelly, N. (2007) · Development and Psychopathology · doi:10.1017/s095457940707023x · Cited by 47

Authors: Morris, J. S., Öhman, A., & Dolan, R. J.
Affiliations: National Hospital for Neurology and Neurosurgery (GB)
Karolinska University Hospital (SE)
The Royal Free Hospital (GB)
ORCID: Dolan, R. J.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 1998-06
Volume: 393
Issue: 6684
Pages: 467-470
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/30976
OpenAlex: W1883268346
Cited by: 1,665
References: 30
Citations by year: 2026: 14 · 2025: 18 · 2024: 27 · 2023: 21 · 2022: 36 · 2021: 36 · 2020: 54 · 2019: 38 · 2018: 54 · 2017: 59 · 2016: 58 · 2015: 56 · 2014: 69 · 2013: 69 · 2012: 85
FWCI: 31.64
Type: journal article
Language: en
Open access: green
hdl.handle.net
Licence: other-oa
www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
RePEc: Research Papers in Economics (submittedVersion)
UCL Discovery (University College London) (submittedVersion)
Max Planck Digital Library (submittedVersion)
MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
Funders: Wellcome Trust
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Face Recognition and Perception
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Keywords: amygdala, emotional learning, backward masking, masked stimuli, conscious perception, hemispheric lateralization, aversive conditioning, angry faces, classical conditioning
MeSH terms: Adult, Amygdala, Anger, Conditioning, Classical, Consciousness, Emotions, Facial Expression, Humans, Functional Laterality, Learning, Male, Tomography, Emission-Computed

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Conscious and unconscious emotional learning in the human amygdala

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