Cited by 713Neural and Behavioral Psychology StudiesPsychosomatic Disorders and Their TreatmentsNeurotransmitter Receptor Influence on Behavior

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Neuroanatomical correlates of externally and internally generated human emotion

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Eric M. Reiman, Richard David Lane, Geoffrey L. Ahern, GARY E.R. SCHWARTZ, Richard J. Davidson, Karl John Friston, Lang Sheng Yun, Kewei Chen·1997·American Journal of Psychiatry

DOI 10.1176/ajp.154.7.918

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Abstract

OBJECTIVE: Positron emission tomography was used to investigate the neural substrates of normal human emotional and their dependence on the types of emotional stimulus. METHOD: Twelve healthy female subjects underwent 12 measurements of regional brain activity following the intravenous bolus administration of [15O]H2O as they alternated between emotion-generating and control film and recall tasks. Automated image analysis techniques were used to characterize and compare the increases in regional brain activity associated with the emotional response to complex visual (film) and cognitive (recall) stimuli. RESULTS: Film- and recall-generated emotion were each associated with significantly increased activity in the vicinity of the medial prefrontal cortex and thalamus, suggesting that these regions participate in aspects of emotion that do not depend on the nature of the emotional stimulus. Film-generated emotion was associated with significantly greater increases in activity bilaterally in the occipitotemporparietal cortex, lateral cerebellum, hypothalamus, and a region that includes the anterior temporal cortex, amygdala, and hippocampal formation, suggesting that these regions participate in the emotional response to certain exteroceptive sensory stimuli. Recall-generated sadness was associated with significantly greater increases in activity in the vicinity of the anterior insular cortex, suggesting that this region participates in the emotional response to potentially distressing cognitive or interoceptive sensory stimuli. CONCLUSIONS: While this study should be considered preliminary, it identified brain regions that participate in externally and internally generated human emotion.

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“…current external events and recall of past events) led to the involvement of the MPFC (Frey, Kostopoulos, & Petrides, 2000; Geday et al., 2003; Hariri, Mattay, Tessitore, Fera, & Weinberger, 2003; Hariri, Tessitore, Mattay, Fera, & Weinberger, 2002; Lane et al., 1997; Reiman et al., 1997).”
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The Amygdala in Post-Traumatic Stress Disorder
Shin, L. M. (2009) · Humana Press eBooks · doi:10.1007/978-1-60327-329-9_15 · Cited by 11
Chapter 7 Anterograde amnesia
Markowitsch, H. J. (2008) · Handbook of clinical neurology · doi:10.1016/s0072-9752(07)88007-9 · Cited by 15
“…to the changes in affective behavior are firstly that the mediodorsal thalamus constitutes a cornerstone in the basolateral limbic circuit and secondly that functional imaging studies found thalamic activation towards emotional stimuli (Fink et al., 1996; Lane et al., 1997; Reiman et al., 1997).”
Background
Distinct Effects of D9-tetrahydrocannabinol and Cannabidiol on Neural Activation During Emotional Processing
Fusar‐Poli, P. (2009) · European Psychiatry · doi:10.1016/s0924-9338(09)70439-0 · Cited by 11
Neurofunctional changes related to methamphetamine and sexual cues in methamphetamine dependence from short‐ to long‐term abstinence
Yan, C. P., Yang, W., Luo, J., Tang, F., & Liu, J. (2024) · Addiction Biology · doi:10.1111/adb.13405 · Cited by 10
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The Neuroscience of Maternal Love
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“Thus, this region is vital to the process of monitoring one’s own emotional state in making personally relevant decisions [39] .”
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A continuous emotional task activates the left amygdala in healthy volunteers: 18FDG PET study
Fernández-Egea, E., Parellada, E., Lomeña, F., Falcón, C., Pavı́a, J., Mané, A., Sugranyes, G., Valdes, M., & Bernardo, M. (2009) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2008.01.003 · Cited by 10
“003 emotional perception circuit (Reiman et al., 1997; Zald and Pardo, 1997; Buchanan et al., 2000; Zalla et al., 2000), and helped to define the brain structures that play a role in the neurobiology of emotion.”
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Correction: Affect and the Brain's Functional Organization: A Resting-State Connectivity Approach
Rohr, C. S., Okon‐Singer, H., Craddock, R. C., Villringer, A., & Margulies, D. S. (2013) · PLoS ONE · doi:10.1371/annotation/a4f9f707-5e23-42f8-9d02-ccdade49750a · Cited by 11
Normal Patterns and Variants in PET Brain Imaging
Newberg, A. B., & Alavi, A. A. (2010) · PET Clinics · doi:10.1016/j.cpet.2009.12.006 · Cited by 10
Treatment with Selective Serotonin Reuptake Inhibitors and Mirtapazine Results in Differential Brain Activation by Visual Erotic Stimuli in Patients with Major Depressive Disorder
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Stress and Anxiety Disorders
Chen, C. V., George, S. A., & Liberzon, I. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803592-4.00079-1 · Cited by 10
Traumatic imagery following glucocorticoid administration in earthquake-related post-traumatic stress disorder: A preliminary functional magnetic resonance imaging study
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Generalized and specific emotion impairments as potential markers of severity in Obsessive-Compulsive Disorder: a preliminary study using Facial Action Coding System (FACS).
Valeriani, G., Bersani, F. S., Liberati, D., Polli, E., Girolami, M. T., Zullo, D., Imperatori, C., Melcore, C., Tomassini, L., Albano, G., et al. (2015) · PubMed · Cited by 9
Regression analysis utilizing subjective evaluation of emotional experience in PET studies on emotions
Aalto, S., Wallius, E., Näätänen, P., Hiltunen, J., Metsähonkala, L., Sipilä, H. T., & Karlsson, H. (2005) · Brain Research Protocols · doi:10.1016/j.brainresprot.2005.06.003 · Cited by 9
Patterns of brain activity in patients with epilepsy and depression
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Huang, F., Li, S., Li, D., Yang, M., Ding, H., Di, Y., & Zhu, T. (2022) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph19159200 · Cited by 8
“Since people’s reactions to negative emotions tend to be consistent across cultures and populations [24,25] and the impacts of negative emotion on suicidal ideation are more direct [26], the pandemic-related negative emotions may directly induce an increase in suicidal ideation across regions.”
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Study on predicting sentiment from images using categorical and sentimental keyword-based image retrieval
Seo, S., & Kang, D. (2015) · The Journal of Supercomputing · doi:10.1007/s11227-015-1510-0 · Cited by 8
“Humans feel diverse sentiments through the effect of various stimuli, such as visual, acoustic, tactile, and olfactory [23].”
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Fuzzy-GIST for 4-emotion recognition in natural scene images
Zhang, Q., & Lee, M.-H. (2010) · International Joint Conference on Neural Networks (IJCNN) · doi:10.1109/ijcnn.2010.5596978 · Cited by 9
“In term of the subject's response analysis, a large body of literature describes neural correlates of human emotion that different emotions are associated with the activation of circumscribed neural network [11]–[14].”
Neural Correlates of Winning and Losing While Watching Soccer Matches
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Mindfulness-based interventions in secure settings: challenges and opportunities
Witharana, D., & Adshead, G. M. J. (2013) · Advances in Psychiatric Treatment · doi:10.1192/apt.bp.111.009167 · Cited by 8
Addressing Evidence Linking Secondary Alexithymia to Aberrant Humor Processing
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Effects of a mental stress challenge on brain function in coronary artery disease patients with and without depression.
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“A p value of 0.005 has been shown to represent the best trade-off between Type I and Type II errors (Reiman et al., 1997).”
BackgroundInfluential
On the origins and diagnosis of asperger syndrome : a clinical, neuroimaging and genetic study
Wendt, T. N. (2004) · Cited by 8
Cerebral Correlates of Varying Ages of Emotional Memories
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“Coordinates sensorimotor responses to unpredictable threatening content (Szily & Kéri, 2008) and cognitive tasks (Reiman et al., 1997).”
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The Role of the Temporal Lobe in Human Social Cognition
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Regional and Temporal Differences in Brain Activity With Morally Good or Bad Judgments in Men: A Magnetoencephalography Study
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The contribution of brain imaging to the study of panic disorder
Volpe, U., Merlotti, E., Mucci, A., & Galderisi, S. (2004) · Epidemiology and Psychiatric Sciences · doi:10.1017/s1121189x00001755 · Cited by 7
“Reiman et al. (1997), analizzando la notevole mole di dati prodotti dagli studi condotti con la PET, argomenta che le regioni talamiche e prefrontali sono coinvolte nelle risposte emozionali normali, indipendentemente dal tipo o dalla valenza dello stimolo; che le aree associative…”
Background
Asymmetry in the emotional content of lateralised multimodal hallucinations following right thalamic stroke
Mollet, G. A., Harrison, D. W., Walters, R. P., & Foster, P. S. (2007) · Cognitive Neuropsychiatry · doi:10.1080/13546800701319094 · Cited by 7
“Many studies have demonstrated that emotional arousal generates increased thalamic activity (George et al., 1995; Goldin et al., 2005; Lane, Reiman, Ahern, Schwartz, & Davidson, 1997; Lane, Reiman, Bradley, et al., 1997; Reiman et al., 1997).”
Background
Influence of aversive visual stimulation on attention, working memory, and anxiety in university students.
Giron, P. R., & de Almeida, R. M. M. (2010) · Psychology & Neuroscience · doi:10.3922/j.psns.2010.1.014 · Cited by 7
“Reiman et al. (1997) and Lane, Chua and Dolan (1997) also mentioned the difficulty of establishing analyses and mapping of emotions in the brain in regions such as the hypothalamus, prefrontal cortex, thalamus, and median cerebral cortex, which are activated in very similar ways by both adverse and…”
Background
Psychiatric syndromes in cerebellar degeneration
Leroi, I., O’Hearn, E., & Margolis, R. L. (2001) · International Review of Psychiatry · doi:10.1080/09540260120082173 · Cited by 7
Distinction in the function and microstructure of white matter between major depressive disorder and generalized anxiety disorder
Yu, Y., Zhang, T., Li, Q., Song, M., Qi, L., Sun, J., Ji, G., Tian, Y., & Wang, K. (2025) · Journal of Affective Disorders · doi:10.1016/j.jad.2025.01.018 · Cited by 6
Olfaction, Emotion & the Amygdala: arousal-dependent modulation of long-term autobiographical memory and its association with olfaction: beginning to unravel the Proust phenomenon?
Hughes, M. (2004) · DOAJ (DOAJ: Directory of Open Access Journals) · Cited by 6
Parameters of the spectral analysis of the heart rate variability in treating depression
Andruskevicius, S. (2009) · Medicina · doi:10.3390/medicina45030028 · Cited by 6
Real-Time Elicitation of Moral Emotions Using a Prejudice Paradigm
Fourie, M. M., Kilchenmann, N., Malcolm‐Smith, S., & Thomas, K. G. F. (2012) · Frontiers in Psychology · doi:10.3389/fpsyg.2012.00275 · Cited by 6
Monte-Carlo based neuroimaging set-level multiple-comparison correction
Chen, K., Reiman, E. M., Bandy, D. J., & Alexander, G. E. (2003) · IFAC Proceedings Volumes · doi:10.1016/s1474-6670(17)33464-x · Cited by 6
Self-citation
Ventrolateral Prefrontal Cortex Updates Chosen Value According to Choice Set Size
Fujiwara, J., Usui, N., Eifuku, S., Iijima, T., Taira, M., Tsutsui, K., & Tobler, P. N. (2017) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_01207 · Cited by 6
“In line with this interpretation, many studies have found the insula to be involved in processing aversive emotional states, conflict, pain, and distress ( Jensen et al., 2016; Shenhav et al., 2014; Corradi-Dell’Acqua, Hofstetter, & Vuilleumier, 2011; Fujiwara et al., 2009b; Wicker et al., 2003; Calder, Lawrence, & Yo…”
BackgroundResult

Authors: Reiman, E. M., Lane, R. D., Ahern, G. L., SCHWARTZ, G. E. R., Davidson, R. J., Friston, K. J., Yun, L. S., & Chen, K.
Affiliations: University of Arizona (US)
ORCID: Eric M. Reiman
Richard David Lane
GARY E.R. SCHWARTZ
Richard J. Davidson
Karl John Friston
Kewei Chen
Venue: American Journal of Psychiatry
Publisher: American Psychiatric Association Publishing
Published: 1997-07-01
Volume: 154
Issue: 7
Pages: 918-925
ISSN: 0002-953X (ISSN-L)
1535-7228
DOI: 10.1176/ajp.154.7.918
OpenAlex: W1525298240
Semantic Scholar: f12897c2e3c50642666b917f8c8ad7542bb93594
Cited by: 711
References: 38
Citations by year: 2026: 1 · 2025: 7 · 2024: 8 · 2023: 8 · 2022: 6 · 2021: 10 · 2020: 9 · 2019: 15 · 2018: 12 · 2017: 12 · 2016: 15 · 2015: 23 · 2014: 19 · 2013: 27 · 2012: 16
FWCI: 18.78
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: American Journal of Psychiatry (publishedVersion)
PubMed (publishedVersion)
UCL Discovery (University College London) (submittedVersion)
Funders: Wellcome Trust
National Institutes of Health (5k20mh000972-05)
National Institute of Mental Health (MH00972, MH00875)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Health Sciences › Medicine › Psychiatry and Mental health › Psychosomatic Disorders and Their Treatments
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords: emotions, neural substrates of emotion, sadness, medial prefrontal cortex, thalamus, amygdala, hippocampal formation, anterior insula, interoception, exteroception, regional brain activity
MeSH terms: Adult, Affective Symptoms, Arousal, Brain, Brain Mapping, Cognition, Emotions, Female, Humans, Middle Aged, Motion Pictures, Oxygen Radioisotopes, Mental Recall, Research Design, Sensation, Tomography, Emission-Computed, Visual Perception, Water

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Neuroanatomical correlates of externally and internally generated human emotion

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