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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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“Spatial resolution, contrast resolution of individual subtraction images, and accuracy of the image deformation algorithm make it difficult to specify in detail the structures that are responsible for the observed changes in regional brain activity, as previously reported (Gautier et al., 2000;Reiman et al., 1997;Tata…”
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“Among these regions, the occipital and occipitotemporal cortices reportedly subserve as processing centers for visual cognition (Paradiso et al., 1999; Reiman et al., 1997; LeDoux, 2000).”
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“…have been implicated in neuroimaging studies of emotion (Phan, Wager, Taylor, & Liberzon, 2002 ), with the suggestion that cingulate and insula regions are involved in the monitoring of an individual's internal emotional state (Damasio et al., 2000; Simpson et al., 2000; Reiman et al., 1997).”
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“Reiman et al. (1997) also reported the involvement of the insula in the emotional response to potentially distressing thoughts or interoceptive sensory stimuli.”
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“, 2002) and may participate in the evaluation of potentially distressing sensory stimuli, serving as an alarm center for internally sensed dangers or homeostatic changes (Reiman et al., 1997).”
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“Similarly, bilateral AINS activates for internal (recall) but not external (video) generated sadness (Reiman et al., 1997), and personal recall of a negative and positive events activate AINS (e.g. Lane et al., 1997a, 1997b), while passive viewing of images of positive or negative emotions…”
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“So, the insula can be regarded as a central structure that integrates internal somatic cues of danger with emotional experience (Reiman et al., 1997; Damasio et al., 2000).”
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“Right anterior insula is implicated in second-order representations of emotional state, including feelings arising from the interpretation of interoceptive responses and self-generated emotion (Reiman et al. 1997; Critchley et al. 2004).”
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“For instance, the amygdala is believed to play a central role in fear response (LeDoux 2003; Whalen et al. 2001), whereas the subgenual anterior cingulate cortex is thought to be important in instances of sadness (Beauregard et al. 1998; Reiman et al. 1997).”
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“…(medial and ventrolateral prefrontal cortex, orbitofrontal cortex, ventral anterior cingulate) and the insular cortex have consistently been associated with conscious emotional experience (Bush, Luu, & Posner, 2000; Dunn & Everitt, 1988; Lane, 2006; Phillips et al., 2003a; Reiman et al., 1997).”
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“Activation of the occipital cortex in response to visual stimulation with pleasant and aversive pictures is very common (Kalin et al., 1997; Kosslyn et al., 1996; Lane et al., 1999, 1997a; Lang et al., 1998; Reiman et al., 1997).”
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“In addition, due to its connections to the cingulate cortex and the brainstem, the insula is considered important in maintaining homeostasis and in representing internal emotional states (Reiman et al., 1997; Damasio et al., 2000).”
BackgroundCortical activation in alexithymia as a response to emotional stimuli
Karlsson, H., Näätänen, P., & Stenman, H. (2008) · The British Journal of Psychiatry · doi:10.1192/bjp.bp.106.034728 · Cited by 105
Cognitive generation of affect in hypomania: an fMRI study
Malhi, G. S., Lagopoulos, J., Sachdev, P. S., Mitchell, P. B., Ivanovski, B., & Parker, G. B. (2004) · Bipolar Disorders · doi:10.1111/j.1399-5618.2004.00123.x · Cited by 106
Bases neuronales de la empatía
Moya‐Albiol, L., Sebastián, N. H., & Santacreu, M. C. B. (2010) · Revista de Neurología · doi:10.33588/rn.5002.2009111 · Cited by 114
“En la misma línea, al contrario que en investigaciones previas [46,47], se observó una disminución del flujo sanguíneo cerebral regional en la corteza prefrontal medial inferior derecha durante la presentación de imágenes emocionales en comparación con la presentación de imágenes neutras.”
BackgroundFunctional correlates of macroscopic high-frequency brain activity in the human visual system
Keil, A., Gruber, T., & Müller, M. M. (2001) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(01)00031-8 · Cited by 106
Volumetric MRI study of the insular cortex in individuals with current and past major depression
Takahashi, T., Yücel, M., Lorenzetti, V., Tanino, R., Whittle, S., Suzuki, M., Walterfang, M., Pantelis, C., & Allen, N. B. (2009) · Journal of Affective Disorders · doi:10.1016/j.jad.2009.06.003 · Cited by 104
Miyake, Y., Okamoto, Y., Onoda, K., Shirao, N., Okamoto, Y., Otagaki, Y., & Yamawaki, S. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2009.12.095 · Cited by 102
“Limbic structures are likely to respond to emotional stimuli at a sensory or perceptual level (Reiman et al., 1997), whereas the mPFC may be involved in cognitive aspects of emotional processing, such as attention to emotions, making appraisals or the identification of emotions (Drevets and…”
InfluentialFingelkurts, A. A., & Fingelkurts, A. A. (2009) · Cognitive Processing · doi:10.1007/s10339-009-0261-3 · Cited by 104
Pompei, F., Dima, D., Rubia, K., Kumari, V., & Frangou, S. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.04.055 · Cited by 101
“Reduced fronto-cingulate connectivity: a correlate of predisposition to BD Similarly to the insula, the vACC is integral to a network of brain regions involved in affect processing and generation (Reiman et al., 1997; Damasio et al., 2000).”
BackgroundChanges of the neurotransmitter serotonin but not of hormones during short time music perception
Evers, S., & Suhr, B. (2000) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s004060070031 · Cited by 100
Cameron, O. G., & Minoshima, S. (2002) · Psychosomatic Medicine · doi:10.1097/01.psy.0000038939.33335.32 · Cited by 99
Fabiansson, E. C., Denson, T. F., Moulds, M. L., Grisham, J. R., & Schira, M. M. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.09.078 · Cited by 100
Schaefer, A., Collette, F., Philippot, P., der Linden, M. V., Laureys, S., Delfiore, G., Degueldre, C., Maquet, P., Luxen, A., & Salmon, É. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00009-0 · Cited by 106
“Finally, it has to be pointed out that the expected activation of the amygdala for negative emotions did not emerge from our interactions, despite existing evidence of its involvement in negative emotions (e.g., Morris et al., 1998, 2001; Reiman et al., 1997; Whalen et al., 1998).”
BackgroundHigher serum glucose levels are associated with cerebral hypometabolism in Alzheimer regions
Burns, C. M., Chen, K., Kaszniak, A. W., Lee, W., Alexander, G. E., Bandy, D. J., Fleisher, A., Caselli, R. J., & Reiman, E. M. (2013) · Neurology · doi:10.1212/wnl.0b013e31828f17de · Cited by 101
“005 enables a reduction in type I errors without missing results that may have empirical importance.(15) The present study has retained this threshold for all imaging-related analyses.”
ResultSelf-citationThe Neurocircuitry of Fear, Stress, and Anxiety Disorders
Shin, L. M., & Liberzon, I. (2011) · FOCUS The Journal of Lifelong Learning in Psychiatry · doi:10.1176/foc.9.3.foc311 · Cited by 105
Fear in dreams and in wakefulness: Evidence for day/night affective homeostasis
Virginie Sterpenich, A., Perogamvros, L., Tononi, G., & Schwartz, S. (2019) · Human Brain Mapping · doi:10.1002/hbm.24843 · Cited by 110
A multiprocess perspective on the neuroscience of emotion.
Ochsner, K. N., & Barrett, L. F. (2001) · Cited by 97
Makris, N., Schlerf, J. E., Hodge, S. M., Haselgrove, C., Albaugh, M. D., Seidman, L. J., Rauch, S. L., Harris, G. J., Biederman, J., Caviness, V. S., et al. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2004.12.056 · Cited by 99
Canli, T., Zhao, Z., Desmond, J. E., Glover, G. H., & Gabrieli, J. D. E. (1999) · Psychobiology · doi:10.3758/bf03332139 · Cited by 102
Gender differences in cortical representation of rectal distension in healthy humans
Kern, M., Jaradeh, S. S., Arndorfer, R. C., Jesmanowicz, A., Hyde, J. S., & Shaker, R. (2001) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.2001.281.6.g1512 · Cited by 98
Azuma, R., Deeley, Q., Campbell, L., Daly, E., Giampietro, V., Brammer, M. J., Murphy, K. C., & Murphy, D. (2015) · Journal of Neurodevelopmental Disorders · doi:10.1186/1866-1955-7-1 · Cited by 99
“Activations in the cerebellum during facial emotion and other affective processing tasks have been reported by prior human studies [57,64,65,67,103,112-114].”
ResultWhalley, M. G., Rugg, M. D., Smith, A. P. R., Dolan, R. J., & Brewin, C. R. (2008) · Brain and Cognition · doi:10.1016/j.bandc.2008.05.008 · Cited by 101
“to suggest that different structures are involved in the processing of internally generated versus externally generated events (Lieberman, 2007; Reiman et al., 1997), and this distinction is blurred by script-driven imagery procedures.”
Structural basis of empathy and the domain general region in the anterior insular cortex
Mutschler, I., Reinbold, C., Wankerl, J., Seifritz, E., & Ball, T. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00177 · Cited by 92
Kemp, A. H. (2002) · NeuroImage · doi:10.1006/nimg.2002.1298 · Cited by 94
Affect modulates appetite‐related brain activity to images of food
Killgore, W. D. S., & Yurgelun-Todd, D. A. (2006) · International Journal of Eating Disorders · doi:10.1002/eat.20240 · Cited by 99
Schmitt, A. G., Upadhyay, N., Martin, J. A., Rojas, S., Strüder, H. K., & Boecker, H. (2019) · Brain Plasticity · doi:10.3233/bpl-190081 · Cited by 97
“alarm center for internally-sensed dangers or homeo767 static changes [72].”
BackgroundExpecting unpleasant stimuli–an fMRI study
Herwig, U., Abler, B., Walter, H., & Erk, S. (2007) · Psychiatry Research: Neuroimaging · doi:10.1016/j.pscychresns.2006.02.007 · Cited by 92
“The recall of emotional situations in the absence of concrete stimuli was reported to involve ACC, insula, thalamus and hypothalamus (Lane et al., 1997; Reiman et al., 1997).”
BackgroundHu, S., Wei, N., Wang, Q.-D., Yan, L.-Q., Wei, E., Zhang, M.-M., Hu, J., Huang, M., Zhou, W.-H., & Xu, Y. (2008) · American Journal of Neuroradiology · doi:10.3174/ajnr.a1260 · Cited by 94
Abstract Representations of Associated Emotions in the Human Brain
Kim, J., Schultz, J., Rohe, T., Wallraven, C., Lee, S., & Bülthoff, H. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.4059-14.2015 · Cited by 98
Gainotti, G. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.02.004 · Cited by 89
Dinges, D. F., Rider, R., Dorrian, J., McGlinchey, E. L., Rogers, N. L., Cizman, Z., Goldenstein, S. K., Vogler, C., Venkataraman, S., & Metaxas, D. (2005) · PubMed · Cited by 89
Lane, R. D., & Garfield, D. (2005) · Neuropsychoanalysis · doi:10.1080/15294145.2005.10773468 · Cited by 89
Self-citationSuardi, A. C., Sotgiu, I., Costa, T., Cauda, F., & Rusconi, M. L. (2016) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-016-0414-7 · Cited by 91
“Five of the eight studies (Lane et al., 2009; Lane et al., 1997; Lane et al., 1998; Marci et al., 2007; Reiman et al., 1997) asked participants to listen to prerecorded audio scripts of autobiographical emotional experiences referring to each contrasted condition.”
BackgroundInfluentialLow spatial frequency filtering modulates early brain processing of affective complex pictures
Alorda, C., Serrano‐Pedraza, I., Bueno, J. J. C., Sierra-Vázquez, V., & Montoya, P. (2007) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2007.06.017 · Cited by 86
Masaoka, Y., Koiwa, N., & Homma, I. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2005.086124 · Cited by 85
“This area responds not only to olfaction but also to visual and auditory stimuli (Reiman et al. 1997), suggesting that the area participates in monitoring emotions for personally relevant decision making.”
BackgroundHuman brain potentials related to the emotional expression, repetition, and gender of faces
Marinković, K., & Halgren, E. (1998) · Psychobiology · doi:10.3758/bf03330621 · Cited by 85
Frangou, S., Kington, J., Raymont, V., & Shergill, S. S. (2007) · European Psychiatry · doi:10.1016/j.eurpsy.2007.05.002 · Cited by 84
“response to external stimuli [27] and when evaluating one’s own emotional state [21] and together with the VPFC form part of the network involved in many aspects of affective judgement.”
BackgroundFitzgerald, D. A., Posse, S., Moore, G. J., Tancer, M. E., Nathan, P. J., & Phan, K. L. (2004) · Neuroscience Letters · doi:10.1016/j.neulet.2004.08.007 · Cited by 86
Bremner, J. D., Mishra, S., Campanella, C., Shah, M., Kasher, N., Evans, S., Fani, N., Shah, A. J., Reiff, C. M., Davis, L. L., et al. (2017) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2017.00157 · Cited by 87
“This level of significance has been shown to optimize the reduction of risk of both Type 1 and Type 2 errors (131, 132).”
Background
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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