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Neuroanatomical correlates of externally and internally generated human emotion
Open accessAbstract
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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“Reiman et al. (1997) used either film clips or personal recall to generate emotional response and found that internal and external generation of emotion depended on subtly different brain regions.”
From Affective Cognition and its Disruption in Mood Disorders (2011) · cites this paper as Reiman et al. (1997)
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“Finally, induction of sadness has resulted in increased activation within the bilateral insular (George et al., 1995; Partiot, Grafman, Sadato, Wachs, & Hallett, 1995; Reiman et al., 1997) as well as the bilateral anterior, middle, and posterior temporal cortices (Lane et al., 1997).”
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“fluency, speech articulation, recall of internally generated emotions, particularly sadness, selective attention and attaching emotional valence to pleasant stimuli (Paulesu et al., 1993; Guenther, 2001; Reiman et al., 1997; Corbetta et al., 1991; CrespoFacorro et al., 2001).”
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“The insula, particularly the anterior insula, is preferentially involved in the evaluative, experiential or expressive aspects of internally generated emotions (Reiman et al. 1997; Craig 2003) and anterior/middle insular activation has been observed during the ingestion of chocolate in ‘chocolate lovers’ (Small et al.”
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“Fittingly, the dMPFC has been shown to be more responsive to internally driven emotional states (Reiman et al., 1997), and it has been implicated in self-relatedness, as evidenced by increased dMPFC activation during self-referential judgments of words (Fossati et al.”
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“…rather than the physical aspects of faces (Rotshtein et al., 2005; Fox et al., 2009b) and that the mPFC is activated when a subject perceives or attempts to regulate the effects of an emotionally evocative stimulus (Lane et al., 1997; Reiman et al., 1997; Ochsner et al., 2002; Phan et al., 2002).”
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“…interactions in processing of emotional experience and memory Functional imaging studies in humans show that several subcortical and cortical structures are engaged in encoding, expression, and recall of emotions (Rauch et al., 1996; Zald and Pardo, 1997; Reiman et al., 1997; Taylor et al., 1998).”
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Heinzel, A., Minnerop, M., Schäfer, R. B., Müller, H., Franz, M., & Hautzel, H. (2011) · Journal of Affective Disorders · doi:10.1016/j.jad.2011.06.012 · Cited by 30
“This hypothesis fits in with functional imaging studies that support the crucial role of the ACC in emotional processing in healthy subjects and subjects with emotional disorders (Grimm et al., 2009; Lane et al., 1998; Larisch et al., 1997; Northoff et al., 2007; Reiman et al., 1997).”
ResultEmotion in voice matters: Neural correlates of emotional prosody perception
Iredale, J. M., Rushby, J. A., McDonald, S., Marco, A. D.-D., & Swift, J. (2013) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2013.06.025 · Cited by 30
Shen, Z., Jiang, L., Yang, S., Ye, J., Dai, N., Liu, X., Li, N., Lü, J., Liu, F., Lü, Y., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0184712 · Cited by 31
van Eijndhoven, P., van Wingen, G. A., Fernández, G., Rijpkema, M., Verkes, R. J., Buitelaar, J. K., & Tendolkar, I. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.08.040 · Cited by 33
“The insula has been implicated before in memory formation (Kirwan et al., 2008), but is more generally known for its role in mood regulation (Reiman et al., 1997).”
Engagement of multifocal neural circuits during recall of autobiographical happy events
Cerqueira, C. T., Almeida, J., Gorenstein, C., Gentil, V., Leite, C. C., Sato, J. R., Amaro, E., & Busatto, G. F. (2008) · Brazilian Journal of Medical and Biological Research · doi:10.1590/s0100-879x2008001200006 · Cited by 30
“The insula is seen as relevant to the cortical mapping of information pertaining to bodily features that accompany emotional reactions, having a specific role in the central representation of emotion-related internal visceral responses (8,29,35).”
BackgroundTseng, A., Wang, Z., Huo, Y., Goh, S., Russell, J. A., & Peterson, B. S. (2015) · Human Brain Mapping · doi:10.1002/hbm.23041 · Cited by 30
“Thus, we posit that TD participants enlisted more attentional resources when viewing low-arousal faces because they were attempting to assess and classify lowarousal, ambiguous stimuli [Petersen and Posner, 2012; Posner and Petersen, 1990; Reiman et al., 1997].”
Thermenos, H. W., Makris, N., Whitfield, S., Brown, A., Giuliano, A. J., Lee, E. H., Faraone, S. V., Tsuang, M. T., & Seidman, L. J. (2011) · Bipolar Disorders · doi:10.1111/j.1399-5618.2011.00920.x · Cited by 29
Clouard, C., Jouhanneau, M., Meunier-Salaün, M.-C., Malbert, C., & Val‐Laillet, D. (2012) · PLoS ONE · doi:10.1371/journal.pone.0037968 · Cited by 29
“[68] found that the ACC was involved in the experience of unpleasant emotions, while the PHC was rather activated by pleasant taste [39].”
BackgroundLingford-Hughes, A. R., Daglish, M. R. C., Stevenson, B. J., Feeney, A., Pandit, S. A., Wilson, S. J., Myles, J. S., Grasby, P. M., & Nutt, D. (2006) · Addiction Biology · doi:10.1111/j.1369-1600.2006.00001.x · Cited by 28
“The medial prefrontal area plays a role in processing positive or negative emotions (Lane et al. 1997; Reiman et al. 1997) and is also a brain region whose metabolism is altered by drugs of abuse, e.”
BackgroundMancini-Marı̈e, A., Potvin, S., Fahim, C., Beauregard, M., Mensour, B., & Stip, É. (2006) · The Journal of Clinical Psychiatry · doi:10.4088/jcp.v67n0302 · Cited by 28
Cerebral moderation of cardiovascular functioning: A functional cerebral systems perspective
Foster, P. S., Drago, V., Ferguson, B. J., & Harrison, D. W. (2008) · Clinical Neurophysiology · doi:10.1016/j.clinph.2008.08.021 · Cited by 28
“…following recollection of emotional memories, which is known to produce changes in both cerebral (Foster and Harrison, 2002a; Lane et al., 1997; Markowitsch et al., 2003; Reiman et al., 1997) and cardiovascular functioning (Foster and Webster, 2001; Labouvie-Vief et al., 2003; Marci et al., 2007).”
Bremner, J. D., Vythilingam, M., Vermetten, E. H. G. J. M., & Charney, D. S. (2006) · Journal of Affective Disorders · doi:10.1016/j.jad.2006.10.028 · Cited by 29
“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).”
BackgroundInfluentialNK1 receptor antagonism and the neural processing of emotional information in healthy volunteers
McCabe, C., Cowen, P. J., & Harmer, C. J. (2009) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145709990150 · Cited by 27
“The medial prefrontal cortex is intimately associated with this amygdala circuitry and is also often activated in tasks involving the processing of affective information (Bush et al. 2000 ; Lane et al. 1997; Reiman et al. 1997 ; Yoshimura et al. 2009), particularly those 0.”
BackgroundChaposhloo, M., Nicholson, A. A., Becker, S., McKinnon, M. C., Lanius, R. A., Shaw, S. B., & Initiative, A. D. N. (2023) · NeuroImage Clinical · doi:10.1016/j.nicl.2023.103417 · Cited by 27
“, 1997) or watching emotional movies (Lane et al., 1997; Reiman et al., 1997).”
BackgroundNeural mechanism for judging the appropriateness of facial affect
Kim, J.-W., Kim, J., Jeong, B., Ki, S. W., Im, D.-M., Lee, S. J., & Lee, H. S. (2005) · Cognitive Brain Research · doi:10.1016/j.cogbrainres.2005.08.018 · Cited by 27
Foster, P. S., & Webster, D. G. (2001) · International Journal of Psychophysiology · doi:10.1016/s0167-8760(00)00163-x · Cited by 27
“…inŽduction Schwartz et al., 1981; Roberts and Weerts, 1982; Ekman et al., 1983; Cook et al., 1988; Stemmler, 1989; Rime et al., 1990; Sidorova et al., 1992; de Jong-Meyer et al., 1993; George et al., 1995; Partiot et al., 1995; Foster et al., 1997, .1999; Lane et al., 1997; Reiman et al., 1997 .”
Fusar‐Poli, P., Bhattacharyya, S., Allen, P., Crippa, J. A., Borgwardt, S., Martín‐Santos, R., Seal, M. L., O’Carroll, C., Atakan, Z., Zuardi, A. W., et al. (2010) · Journal of Clinical Neuroscience · doi:10.1016/j.jocn.2009.06.027 · Cited by 26
Investigation of an emotion perception test using functional magnetic resonance imaging
Bae, S., Kang, K. D., Kim, S. W., Shin, Y., Nam, J. J., & Han, D. H. (2019) · Computer Methods and Programs in Biomedicine · doi:10.1016/j.cmpb.2019.104994 · Cited by 26
Aberrant White Matter Microstructure in Depressed Patients with Suicidality
Zhang, H., Li, H., Yin, L., Chen, Z., Wu, B., Huang, X., Jia, Z., & Gong, Q. (2021) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.27927 · Cited by 25
“The thalamus plays an important mediator role between the limbic system and the cerebral cortex, and thereby participates in the neural processing of emotional regulation and executive function.(26) Despite the mixed findings reported for the involvement of structural alterations in the thalamus in relation to suicide…”
ResultGray matter correlates of dispositional optimism: A voxel-based morphometry study
Yang, J., Wei, D., Wang, K., & Qiu, J. (2013) · Neuroscience Letters · doi:10.1016/j.neulet.2013.08.032 · Cited by 28
“Researchers have observed that the thalamus plays an important role in emotion regulation; for instance, it is activated when a person views films or recalls personal experiences that evoke happiness or sadness [26,36], and shows greater activity when a person imitates emotional expressions [8].”
BackgroundUecker, A., Reiman, E. M., Schacter, D. L., Polster, M. R., Cooper, L. A., Yun, L. S., & Chen, K. (1997) · Learning & Memory · doi:10.1101/lm.4.4.337 · Cited by 27
Self-citationBotellero, V. L., Skranes, J. S., Bjuland, K. J., Løhaugen, G. C. C., Haberg, A. K., Lydersen, S., Brubakk, A., Indredavik, M. S., & Martinussen, M. (2016) · Child and Adolescent Psychiatry and Mental Health · doi:10.1186/s13034-016-0093-8 · Cited by 25
“Different fMRI studies have also shown activation of the cerebellum in different emotional tasks, such us viewing pictures of deceased loved ones [81] and viewing pictures and movies evoking both negative and positive feelings [82, 83].”
BackgroundSun, J., Chen, L., He, J., Wang, Z., Guo, C., Ma, Y., Luo, Y., Gao, D.-Q., Yang, H., Fang, J., et al. (2022) · Frontiers in Psychology · doi:10.3389/fpsyg.2022.849847 · Cited by 25
Wu, X., Wang, L., Jiang, H., Fu, Y., Wang, T., Ma, Z., Wu, X., Wang, Y., Fan, F., Song, Y., et al. (2023) · NeuroImage Clinical · doi:10.1016/j.nicl.2023.103445 · Cited by 24
Sarinopoulos, I. C., Hesson, A., Gordon, C., Lee, S. A., Wang, L., Dwamena, F. C., & Smith, R. C. (2012) · Patient Education and Counseling · doi:10.1016/j.pec.2012.10.021 · Cited by 25
“This result is consistent with the neuroimaging literature showing the anterior portion of the insular cortex to be active during emotional challenges, emotional recall, and self-generated emotions, suggesting its key role in the conscious, evaluative, experiential, and expressive aspects of internally generated emoti…”
Resultde Borst, A. W., & de Gelder, B. (2016) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsw039 · Cited by 24
“The whole of the insular cortex, including posterior insula, has been suggested as a site where internally generated emotions and emotional context are evaluated and the expression of responses is initiated (Reiman et al., 1997).”
BackgroundThe brain structure and spontaneous activity baseline of the behavioral bias in trait anxiety
Yin, P., Zhang, M., Hou, X., Tan, Y., Fu, Y., & Qiu, J. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.06.036 · Cited by 25
Sebastiani, L., Simoni, A., Gemignani, A., Ghelarducci, B., & Santarcangelo, E. L. (2003) · Neuroscience Letters · doi:10.1016/s0304-3940(02)01358-7 · Cited by 25
“The regional modifications observed in EEG [1,12,13] and neuroimaging studies [15] during emotions, in fact, could have been overwhelmed, in our experiment, by the modalities of the stimulus presentation, which are likely to have forced cognitive processes into a holistic strategy and buffered actual differences among…”
Chen, Y.-T., Huang, M.-W., Hung, I.-C., Lane, H.-Y., & Hou, C.-J. (2014) · Behavioral and Brain Functions · doi:10.1186/1744-9081-10-36 · Cited by 24
“Neuroimaging studies in healthy participants have described a large increase in amygdala activity while individuals view photos of faces with fearful expressions [7,8] and other emotionally valenced stimuli [9-12].”
BackgroundA general theory of consciousness I:Consciousness and adaptation
Peper, A. (2020) · Communicative & Integrative Biology · doi:10.1080/19420889.2020.1713967 · Cited by 26
Short-term hormone treatment modulates emotion response circuitry in postmenopausal women
Love, T., Smith, Y. R., Persad, C. C., Tkaczyk, A., & Zubieta, J. (2009) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.12.056 · Cited by 24
Parsing positive emotion in relation to agentic and affiliative components of extraversion
Morrone-Strupinsky, J. V., & Lane, R. D. (2006) · Personality and Individual Differences · doi:10.1016/j.paid.2006.10.005 · Cited by 25
Self-citationWittbrodt, M. T., Moazzami, K., Lima, B. B., Alam, Z. S., Corry, D. T., Hammadah, M., Campanella, C., Ward, L. A., Quyyumi, A. A., Shah, A. J., et al. (2019) · Journal of Affective Disorders · doi:10.1016/j.jad.2019.05.018 · Cited by 26
“005 (uncorrected) which has been shown to minimize both Type I and Type II errors in brain imaging research (Lane et al., 1997; Reiman et al., 1997).”
BackgroundSocial Capital and the Human Psyche: Why is Social Life “Capital”?
Savage, J., & Satoshi Kanazawa, A. (2004) · Sociological Theory · doi:10.1111/j.0735-2751.2004.00231.x · Cited by 23
Phillips, M. L., & Mataix‐Cols, D. (2004) · CNS Spectrums · doi:10.1017/s1092852900009214 · Cited by 25
Reciprocal Links between Emotion and Attention
(2004) · Elsevier eBooks · doi:10.1016/b978-012264841-0/50022-6 · Cited by 27
Fear in dreams and in wakefulness: Evidence for day/night affective homeostasis
Sterpenich, V, Perogamvros, L., Tononi, G., & Schwartz, S. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/534099 · Cited by 99
Metadata
- 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
- Venue
- American Journal of Psychiatry
- Published
- 1997-07-01
- Volume
- 154
- Issue
- 7
- Pages
- 918-925
- ISSN
- 0002-953X (ISSN-L)
- 1535-7228
- 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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