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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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“…identified in this study, during the suppression condition, has previously been postulated to be implicated in theory-of-mind tasks (inferences about the mental states of others) (Fletcher et al., 1995) and metacognitive representation of one’s own emotional state (Reiman et al., 1997; Lane, 2000).”
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“In fact, activation of the right anterior insula has been observed in many studies of recallgenerated emotions (Damasio et al. 2000; Phan et al. 2002; Reiman et al. 1997).”
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Crespo‐Facorro, B., Paradiso, S., Andreasen, N. C., OʼLeary, D. S., Watkins, G. L., Ponto, L. L. B., & Hichwa, R. D. (2001) · JAMA · doi:10.1001/jama.286.4.427 · Cited by 232
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“This region has also been reported as being activated in response to fearful, sad, and angry facial expressions during the performance of a gender-decision task (Blair et al 1999; Sprengelmeyer et al 1998), and during recallgenerated , but not film-generated, emotions (Reiman et al 1997).”
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“This supports the notion of Reiman et al. (1997) that it is the internally generated mood that activates the subgenual part rather than sadness itself.”
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“…visual regions are activated by aversive and disgusting visual stimuli, such as unpleasant scenes (Lane et al. 1999; Lang et al. 1998) and film excerpts (Reiman et al. 1997), and that the extrastriate cortical response to aversive stimuli may be modulated by limbic structures (Morris et al. 1998).”
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Cortical Sulcal Maps in Autism
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“Amygdalar activation has been observed in normal subjects to aversive stimuli other than faces, including aversive films and pictures (Irwin et al 1996; Lane et al 1997; Reiman et al 1997 ), aversive odors and tastes (Zald and Pardo 1997), fearful voices (Phillips et al 1998), threatening words (Isenberg et al 1999),…”
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“…as selective attention, sensory discrimination , working memory, word processing, timing, learning , and complex problem solving (Akshoomoff and Courchesne 1992; Leiner et al. 1993; Gao et al. 1996; Gibbon et al. 1997; Allen et al. 1997), and in externally generated emotion (Reiman et al. 1997).”
BackgroundDepersonalization disorder: thinking without feeling.
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“Morris et al., 1996 , and the insula in the percepŽ .tion of disgust Phillips et al., 1997 and negative Žemotions Reiman et al., 1997; Mayberg et al., .1999 , the latter study emphasizing the reciprocal roles of the lateral and orbito-medial prefrontal cortex and insula, amongst other regions, in changes in depressed…”
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“The insula is preferentially engaged in internally generated emotions or feeling states and has been regarded a relay station for signals coming from the internal milieu or viscera to regulate homeostasis.(55,60,61) Posterior cingulate cortex and the parahippocampal region have been reported to provide interface for t…”
BackgroundAssociation between interoception and empathy: Evidence from heartbeat-evoked brain potential
Fukushima, H., Terasawa, Y., & Umeda, S. (2011) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2010.10.015 · Cited by 209
“Importantly, these areas have been implicated in the subjective experience of emotion (Blood and Zatorre, 2001; Critchley et al., 2001; Damasio et al., 2000; Mayberg et al., 1999; Lane et al., 1997; Reiman et al., 1997).”
BackgroundThe function of the anterior temporal lobe: A review of the empirical evidence
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“…have found ATL activation to be activate independent of whether stimuli were pleasant or unpleasant (Lane et al., 1999; Maratos et al., 2001; Reiman et al., 1997) suggesting that this region is involved in some aspect of externally generated emotion independent of the particular emotion…”
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Wicker, B., Perrett, D. I., Baron‐Cohen, S., & Decety, J. (2003) · Neuropsychologia · doi:10.1016/s0028-3932(02)00144-6 · Cited by 200
“Several studies found similar medial prefrontal activation related to the experience of pleasant or unpleasant emotions when the inducing stimuli involved the presentation of slides, film clips, or recall of memories of emotional events[17,36,43] .”
BackgroundMethodZhu, J., Yung, W., Chow, B., Chan, Y., & Wang, J. (2006) · Brain Research Reviews · doi:10.1016/j.brainresrev.2006.01.003 · Cited by 201
Saxena, S., Brody, A. L., Ho, M. L., Alborzian, S., Maidment, K. M., Zohrabi, N., Ho, M. K., Huang, S., Wu, H.-M., & Baxter, L. R. (2002) · Archives of General Psychiatry · doi:10.1001/archpsyc.59.3.250 · Cited by 201
Social psychology as a natural kind
Mitchell, J. P. (2009) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2009.03.008 · Cited by 210
Oliveri, M., Babiloni, C., Filippi, M. M., Caltagirone, C., Babiloni, F., Cicinelli, P., Traversa, R., Palmieri, M. G., & Rossini, P. M. (2003) · Experimental Brain Research · doi:10.1007/s00221-002-1346-8 · Cited by 200
Grimm, S., Schmidt, C. F., Bermpohl, F., Heinzel, A., Dahlem, Y., Wyss, M., Hell, D., Boesiger, P., Boeker, H., & Northoff, G. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2005.09.006 · Cited by 195
“Another study that induced emotions by evoking memories or imagery of personally relevant events with affective impact also showed activation in the PACC (Reiman et al., 1997).”
BackgroundA preferential increase in the extrastriate response to signals of danger
Surguladze, S. A., Brammer, M. J., Young, A. W., Andrew, C., Travis, M. J., Williams, S., & Phillips, M. L. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00085-5 · Cited by 197
“Additionally, in response to visual presentations of different types of emotional compared with nonemotional scene, greater activation within these visual regions have been reported (Reiman et al., 1997; Lane et al., 1997, 1999), irrespective of the perceptual complexity of the stimuli (Taylor et al.”
BackgroundA relation between rest and the self in the brain?
Wicker, B., Ruby, P. M., Royet, J., & Fonlupt, P. (2003) · Brain Research Reviews · doi:10.1016/j.brainresrev.2003.08.003 · Cited by 195
The Effect of Emotional Content on Visual Recognition Memory: A PET Activation Study
Taylor, S. F., Liberzon, I., Fig, L. M., Decker, L. R., Minoshima, S., & Koeppe, R. A. (1998) · NeuroImage · doi:10.1006/nimg.1998.0356 · Cited by 198
The emotional modulation of cognitive processing: an fMRI study
Simpson, J. R., Öngür, D., Akbudak, E., Conturo, T. E., Ollinger, J. M., Snyder, A. Z., Gusnard, D. A., & Raichle, M. E. (2000) · Journal of Cognitive Neuroscience · doi:10.1162/089892900564019 · Cited by 190
Crespo‐Facorro, B. (2000) · Schizophrenia Research · doi:10.1016/s0920-9964(00)00028-1 · Cited by 189
Kumfor, F., & Piguet, O. (2012) · Neuropsychology Review · doi:10.1007/s11065-012-9201-6 · Cited by 202
“Some evidence also suggests that the insula may be recruited when tasks are more cognitively demanding (Reiman et al. 1997), such as on emotion labelling tasks.”
BackgroundAn emotional Stroop functional MRI study of euthymic bipolar disorder
Malhi, G. S., Lagopoulos, J., Sachdev, P. S., Ivanovski, B., & Shnier, R. (2005) · Bipolar Disorders · doi:10.1111/j.1399-5618.2005.00255.x · Cited by 190
Movies and narratives as naturalistic stimuli in neuroimaging
Jääskeläinen, I. P., Sams, M. E., Glerean, E., & Ahveninen, J. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.117445 · Cited by 202
“Today, several decades later, movies and narratives have seen use as naturalistic stimuli in a wealth of neuroimaging studies (Aftanas et al., 1998; Cahill et al., 1996; Decety and Chaminade, 2003; Dimpfel et al., 2003; Dougherty et al., 1999; Gilbert et al., 1989; Jones and Fox, 1992; Karama et al., 2002; Krause et a…”
BackgroundCerebellum and psychiatric disorders
Baldaçara, L., Borgio, J. G. F., Lacerda, A. L. T. D., & Jackowski, A. P. (2008) · Revista Brasileira de Psiquiatria · doi:10.1590/s1516-44462008000300016 · Cited by 183
Tabert, M. H., Borod, J. C., Tang, C. Y., Lange, G., Wei, T.-C., Johnson, R., Nusbaum, A. O., & Buchsbaum, M. S. (2001) · Neuropsychologia · doi:10.1016/s0028-3932(00)00157-3 · Cited by 187
“[77] Reiman EM, Lane RD, Ahern GL, Schwartz GE, Davidson RJ, Friston KJ, et al.”
Reduced thalamic volume in high-functioning individuals with autism
Tsatsanis, K., Rourke, B. P., Klin, A., Volkmar, F. R., Cicchetti, D. V., & Schultz, R. T. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(02)01530-5 · Cited by 185
Ovarian steroids and serotonin neural function
Bethea, C. L., Pecins-Thompson, M., Schutzer, W. E., Gundlah, C., & Lu, Z. (1998) · Molecular Neurobiology · doi:10.1007/bf02914268 · Cited by 184
Neuroanatomic Correlates of Psychopathologic Components of Major Depressive Disorder
Milak, M. S., Parsey, R. V., Keilp, J. G., Oquendo, M. A., Malone, K. M., & Mann, J. J. (2005) · Archives of General Psychiatry · doi:10.1001/archpsyc.62.4.397 · Cited by 179
The Kuleshov Effect: the influence of contextual framing on emotional attributions
Mobbs, D., Weiskopf, N., Lau, H. C., Featherstone, E., Dolan, R. J., & Frith, C. D. (2006) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsl014 · Cited by 178
“Given the visual properties of this region, activity may also reflect the holding or recall of the contextual image in mind (Nakamura et al., 1994; Reiman et al., 1997; Lane et al., 1997).”
BackgroundGoel, V. (2003) · NeuroImage · doi:10.1016/j.neuroimage.2003.07.027 · Cited by 181
“A number of studies have activated these structures in emotion regulation tasks (Davidson et al., 2000a, 2000b; Reiman et al., 1997).”
BackgroundGerber, A. J., Posner, J. E., Gorman, D. A., Colibazzi, T., Yu, S., Wang, Z., Kangarlu, A., Hongtu Zhu, B., Russell, J. A., & Peterson, B. S. (2008) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2008.02.032 · Cited by 186
“…monitoring and assessment of the salience of the stimulus (i.e., that monitors the need for allocating attentional resources to processing of the stimulus) during the processing of stimuli that are ambiguous and yet biologically relevant (Reiman et al., 1997; Silvestri & Kapp, 1998; Whalen, 1998).”
BackgroundInfluentialThe neurobiology of retinoic acid in affective disorders
Bremner, J. D., & McCaffery, P. J. A. (2007) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2007.07.001 · Cited by 182
FMRI Study of Emotional Speech Comprehension
Beaucousin, V., Lacheret-Dujour, A., Turbelin, M., Morel, M., Mazoyer, B. M., & Tzourio‐Mazoyer, N. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhj151 · Cited by 173
“The areas involved in affective prosody processing were uncovered in the difference between brain activity during affective classification of sentences enounced by actors and during affective classification of sentences produced by Kali lacking affective prosody (AffAct--AffKali).”
BackgroundInfluentialDoes Anxiety Cause Freezing of Gait in Parkinson's Disease?
Ehgoetz Martens, K. A., Ellard, C. G., & Almeida, Q. J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0106561 · Cited by 171
“A recent review highlighted that nearly 60% of emotional induction studies reported activation of the insula [47], and furthermore the insula has been suggested to participate in evaluation of distressing thoughts and interoceptive emotional responses [48].”
BackgroundGruber, A. J., & McDonald, R. J. (2012) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2012.00050 · Cited by 173
“Several studies in humans have demonstrated a reliable correlation between amygdala activation and emotionally valenced stimuli (Breiter et al., 1996; Reiman et al., 1997), which can even occur without subjects’ awareness (Whalen et al., 1998).”
BackgroundModulation of Emotional Appraisal by False Physiological Feedback during fMRI
Gray, M. A., Harrison, N. A., Wiens, S., & Critchley, H. D. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000546 · Cited by 170
“Insula activation is observed during other conditions that engender emotional arousal, for example emotional recall [36–38] and appraisal of disgust stimuli [39–40].”
BackgroundSPECT [I-123]iomazenil measurement of the benzodiazepine receptor in panic disorder
Bremner, J. D., Innis, R. B., White, T. G., Fujita, M., Silbersweig, D., Goddard, A. W., Staib, L. H., Stern, E. R., Cappiello, A., Woods, S. W., et al. (2000) · Biological Psychiatry · doi:10.1016/s0006-3223(99)00188-2 · Cited by 169
“This threshold is based on prior studies showing a low level of Type I error using this cutoff as the criteria (Reiman et al 1997).”
MethodThe interaction of emotional and cognitive neural systems in emotionally guided response inhibition
Shafritz, K. M., Collins, S. H., & Blumberg, H. P. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2005.11.053 · Cited by 167
“, 1997), viewing and recalling emotional film clips (Lane et al., 1997; Reiman et al., 1997), recalling emotional life events (George et al.”
BackgroundShelley, B. P., & Trimble, M. (2004) · The World Journal of Biological Psychiatry · doi:10.1080/15622970410029933 · Cited by 172
“A study using [15O] PET investigated the brain regions that participated in externally and internally generated human emotion (Reiman et al. 1997).”
MethodParadiso, S., Andreasen, N. C., Crespo‐Facorro, B., OʼLeary, D. S., Watkins, G. L., Ponto, L. L. B., & Hichwa, R. D. (2003) · American Journal of Psychiatry · doi:10.1176/appi.ajp.160.10.1775 · Cited by 167
“Functional imaging studies have also shown that the thalamus is associated with visually induced negative affect (65, 66).”
BackgroundNeural abnormalities during cognitive generation of affect in Treatment-Resistant depression
Kumari, V., Mitterschiffthaler, M. T., Teasdale, J. D., Malhi, G. S., Brown, R. G., Giampietro, V., Brammer, M. J., Poon, L., Simmons, A., Williams, S. C. R., et al. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(02)01785-7 · Cited by 166
Cognitive generation of affect in bipolar depression: an fMRI study
Malhi, G. S., Lagopoulos, J., Ward, P. B., Kumari, V., Mitchell, P. B., Parker, G. B., Ivanovski, B., & Sachdev, P. S. (2004) · European Journal of Neuroscience · doi:10.1111/j.0953-816x.2003.03159.x · Cited by 168
A functional anatomic study of emotion in schizophrenia
Taylor, S. F., Liberzon, I., Decker, L. R., & Koeppe, R. (2002) · Schizophrenia Research · doi:10.1016/s0920-9964(01)00403-0 · Cited by 165
Neural correlates of frustration
Abler, B., Walter, H., & Erk, S. (2005) · Neuroreport · doi:10.1097/00001756-200505120-00003 · Cited by 164
“Internally generated sadness was previously associated with activation in the anterior insular cortex, and a role for this brain area in generating emotional responses to distressing interoceptive stimuli has been inferred [21].”
BackgroundBaron Short, E., Kose, S., Mu, Q., Borckardt, J., Newberg, A., George, M. S., & Kozel, F. A. (2010) · Evidence-Based Complementary and Alternative Medicine · doi:10.1093/ecam/nem163 · Cited by 159
“These individual t-maps were used to generate group t-maps at the second level in a random effects model analysis (14).”
MethodRegional brain activity in women grieving a romantic relationship breakup
Najib, A., Lorberbaum, J. P., Kose, S., Bohning, D. E., & George, M. S. (2004) · American Journal of Psychiatry · doi:10.1176/appi.ajp.161.12.2245 · Cited by 161
Cortical Substrates for the Perception of Dyspnea
von Leupoldt, A., & Dahme, B. (2005) · CHEST Journal · doi:10.1378/chest.128.1.345 · Cited by 156
The effect of graded aversive stimuli on limbic and visual activation
Taylor, S. F., Liberzon, I., & Koeppe, R. A. (2000) · Neuropsychologia · doi:10.1016/s0028-3932(00)00032-4 · Cited by 159
Bolus isoproterenol infusions provide a reliable method for assessing interoceptive awareness
Khalsa, S. S., Rudrauf, D., Sandesara, C., Olshansky, B., & Tranel, D. (2009) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2008.08.010 · Cited by 155
Schmahl, C., Elzinga, B., Vermetten, E., Sanislow, C., McGlashan, T., & Bremner, J. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(02)01720-1 · Cited by 148
“A threshold z score of 2.58 has been demonstrated by Reiman et al (1997) to be associated with a low rate of false positive activations and to constitute the most optimal trade-off between type I and type II statistical errors.”
Influential
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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