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Rethinking the Emotional Brain
Open accessAbstract
I propose a reconceptualization of key phenomena important in the study of emotion-those phenomena that reflect functions and circuits related to survival, and that are shared by humans and other animals. The approach shifts the focus from questions about whether emotions that humans consciously feel are also present in other animals, and toward questions about the extent to which circuits and corresponding functions that are present in other animals (survival circuits and functions) are also present in humans. Survival circuit functions are not causally related to emotional feelings but obviously contribute to these, at least indirectly. The survival circuit concept integrates ideas about emotion, motivation, reinforcement, and arousal in the effort to understand how organisms survive and thrive by detecting and responding to challenges and opportunities in daily life.
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“This error, assuming that an action is equivalent to an emotion, which I call the mental inference fallacy (Barrett, 2017), has wreaked havoc with the scientific accumulation of knowledge about emotion (also see Barrett, 2012; LeDoux, 2012).”
From The theory of constructed emotion: an active inference account of interoception and categorization (2016) · cites this paper as LeDoux, 2012
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“Defensive survival circuits are evolutionarily wired to detect and respond to innate threats and to respond to novel threats that have been learned about in the past (35,36).”
From A higher-order theory of emotional consciousness (2017) · cites this paper as [36]
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“Approximately 153 billion GB of data were generated in 2013, with projected growth of 48% per year.67”
From Artificial Intelligence and Surgical Decision-making. (2020) · cites this paper as [67]
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“This fear circuit is involved in evaluation and detection of threat cues, eliciting and regulating emotional responses, and fear learning and extinction (LeDoux, 2012).”
From Anxiety and attention to threat: cognitive mechanisms and treatment with attention bias modification (2016) · cites this paper as LeDoux, 2012
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“In turn, CeA has direct connections to periaqueductal gray (PAG), a fundamental area that organizes the threat response (LeDoux, 2012).”
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“The importance of distinguishing between instinctive behaviours generated by the brainstem and felt emotions generated by the cortex has been previously discussed extensively (LeDoux, 2012; LeDoux, 2013; LeDoux, 2014a; LeDoux, 2014b; Rolls, 2014a; Rolls, 2014b; Scott, 2014).”
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“In other articles, ingredients also include basic behavioral adaptations like freezing, fleeing, and fighting, although there is no necessary one-to-one correspondence between a behavior and an emotion category (e.g., Barrett, 2012; LeDoux, 2012).”
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“…rats is just one of many lines of evidence, including research on humans, demonstrating a relationship between emotions and feelings comparable to that between nociception and pain (see Rose 2002; Berridge and Winkielman 2003; Damasio 2005; Rose 2007; LeDoux 2012 for a more detailed explanation).”
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“In contrast, the amygdala may be crucial for learning associations between aversive events (signaled in part by PAG) and other sensory cues (LeDoux, 2012).”
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“The term emotion has been notoriously difficult to define (Hamann, 2012; LeDoux, 2012) and it has even been asked how meaningful a categorical distinction between cognition and emotion (or “cognitive” and “affective” brain areas) is (Pessoa, 2008).”
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“SOCIAL APPROACH Several models of emotion and social cognition (e.g., Phillips et al., 2003a,b; Lieberman, 2007; LeDoux, 2012) include core processes subserving rapid or automatic (sometimes even unconscious) processing of information in terms of safety versus danger, which are intrinsically linked with behavioral ten…”
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Active Avoidance Learning Requires Prefrontal Suppression of Amygdala-Mediated Defensive Reactions
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“Thus, by gaining control over US delivery, subjects successfully inhibit the expression of deeply instated behavioral reactions that normally prevail in situations of expected threat (Fanselow and Lester, 1988; Blanchard et al., 2005; LeDoux, 2012).”
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“Prevailing models have localized fear learning largely to nuclei in the BLA (Phelps et al, 2004) although recent studies have asserted a possible role for the CMA (LeDoux, 2012).”
BackgroundA Bayesian Model of Category-Specific Emotional Brain Responses
Wager, T. D., Kang, J., Johnson, T. D., Nichols, T. E., Satpute, A. B., & Barrett, L. F. (2015) · PLOS Computational Biology · doi:10.1371/journal.pcbi.1004066 · Cited by 262
“Thus, in spite of groundbreaking advances in understanding the circuitry underlying basic behavioral adaptations for safety and reproduction (including ‘ threat ’ behaviors; [11]), there is no comprehensive model of the neurophysiological basis of emotional experience in humans.”
BackgroundDivergent midbrain circuits orchestrate escape and freezing responses to looming stimuli in mice
Shang, C., Chen, Z., Liu, A., Li, Y., Zhang, J., Qu, B., Yan, F., Zhang, Y., Liu, W., Liu, Z., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-03580-7 · Cited by 270
“Three general factors determining defensive behavioral patterns in response to threats have been proposed4: (1) environmental context (e.”
Rodent models of post-traumatic stress disorder: behavioral assessment
Verbitsky, A., Dopfel, D., & Zhang, N. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-0806-x · Cited by 264
The evolution of decision rules in complex environments
Fawcett, T. W., Fallenstein, B., Higginson, A. D., Houston, A. I., Mallpress, D. E. W., Trimmer, P. C., & McNamara, J. M. (2014) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2013.12.012 · Cited by 263
The neural basis of one's own conscious and unconscious emotional states
Smith, R. S., & Lane, R. D. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.08.003 · Cited by 253
Evolution of prefrontal cortex
Preuss, T. M., & Wise, S. P. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-021-01076-5 · Cited by 257
Insects have the capacity for subjective experience
Klein, C., & Barron, A. B. (2016) · Animal Sentience · doi:10.51291/2377-7478.1113 · Cited by 243
“The importance of distinguishing between instinctive behaviours generated by the brainstem and felt emotions generated by the cortex has been previously discussed extensively (LeDoux, 2012; LeDoux, 2013; LeDoux, 2014a; LeDoux, 2014b; Rolls, 2014a; Rolls, 2014b; Scott, 2014).”
BackgroundThe evolutionary origins of mood and its disorders
Nettle, D., & Bateson, M. (2012) · Current Biology · doi:10.1016/j.cub.2012.06.020 · Cited by 230
“and there are important homologues of these mechanisms in invertebrates too [4].”
BackgroundInfluentialInagaki, H. K., Panse, K. M., & Anderson, D. J. (2014) · Neuron · doi:10.1016/j.neuron.2014.09.032 · Cited by 214
“Food-deprivation creates a type of “global organismal state change” (Kim et al., 2013; LeDoux, 2012) that is multi-dimensional: it involves multiple physiological and behavioral changes.”
Olfaction as a marker for depression
Croy, I., & Hummel, T. R. (2016) · Journal of Neurology · doi:10.1007/s00415-016-8227-8 · Cited by 237
On the Nature of Fear and Anxiety Triggered by COVID-19
Coelho, C. M., Suttiwan, P., Arató, N., & Zsido, A. N. (2020) · Frontiers in Psychology · doi:10.3389/fpsyg.2020.581314 · Cited by 255
“Defensive behaviors are immediate responses (LeDoux, 2012) triggered by activity in survival circuits that detects threats (LeDoux, 2014) and leading to the conscious emotion of fear that follows immediately.”
BackgroundHow should neuroscience study emotions? by distinguishing emotion states, concepts, and experiences
Adolphs, R. (2016) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsw153 · Cited by 245
“mal neuroscience (LeDoux, 2012), but I think there is a simpler solution: do the same thing we as scientists do when we study”
BackgroundMethodTinnitus and anxiety disorders: a review
Pattyn, T., Van Den Eede, F., Vanneste, S., Cassiers, L., Veltman, D. J., Van De Heyning, P., & Sabbe, B. C. G. (2016) · Hearing Research · doi:10.1016/j.heares.2015.08.014 · Cited by 233
“This assumption would likewise hold for anxiety disorders where the vmPFC has been shown to be essential for the top-down control (suppression) of a threat response (Cain and Ledoux, 2008; Sullivan, 2003; Ledoux, 2012), which inference is also supported by Rauschecker et al.”
BackgroundInfluentialPace-Schott, E. F., Amole, M. C., Aue, T., Balconi, M., Bylsma, L. M., Critchley, H., Demaree, H. A., Friedman, B. H., Gooding, A. E. K., Gosseries, O., et al. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.05.002 · Cited by 221
“Carvalho, 2013; Panksepp, 2010), levels of arousal, actions (Bernroider and Panksepp, 2011; Gardiner, 2015), hedonics (pleasure and pain (Buck, 1985; Damasio and Carvalho, 2013; LeDoux, 2012; Panksepp, 2010), drives (Alcaro and Panksepp, 2011), cognitions (including per-”
InfluentialUnconscious processing of emotions and the right hemisphere
Gainotti, G. (2011) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2011.12.005 · Cited by 283
A Model for Basic Emotions Using Observations of Behavior in Drosophila
Gu, S., Wang, F., Patel, N. P., Bourgeois, J. A., & Huang, J. H. (2019) · Frontiers in Psychology · doi:10.3389/fpsyg.2019.00781 · Cited by 267
The neural subjective frame: from bodily signals to perceptual consciousness
Park, H.-D., & Tallon-Baudry, C. (2014) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2013.0208 · Cited by 246
“Emotions can be considered as being composed of two components: one being tightly related to the production of behavioural responses necessary for survival or maintenance of well-being [27], the other being the subjective feeling associated with an emotional stimulus or an emotional situation [15].”
BackgroundPeriaqueductal Gray Neuronal Activities Underlie Different Aspects of Defensive Behaviors
Deng, H., Xiao, X., & Wang, Z. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.4425-15.2016 · Cited by 224
Lindquist, K. A., Siegel, E. H., Quigley, K. S., & Barrett, L. F. (2013) · Psychological Bulletin · doi:10.1037/a0029038 · Cited by 245
“Other models of emotion that are not explicitly identified as psychological constructionist views but that share some of this tradition’s assumptions have also emerged (e.g., Boiger & Mesquita, in press; Coan, 2010; LeDoux, 2012).”
BackgroundPain and analgesia: the value of salience circuits
Borsook, D., Edwards, R., Elman, I., Becerra, L., & Levine, J. (2013) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2013.02.003 · Cited by 215
“As such, these areas that contribute to the emotional brain processes, ‘‘reflect functions and circuits related to survival’’ that integrate ‘‘motivation, reinforcement, and arousal’’ (LeDoux, 2012).”
BackgroundDolcos, F., Katsumi, Y., Moore, M., Berggren, N., de Gelder, B., Derakshan, N., Hamm, A. O., Koster, E. H. W., Ladouceur, C. D., Okon‐Singer, H., et al. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.08.017 · Cited by 247
“As alluded to above, one influential hypothesis has suggested that unconscious processing of emotional stimuli may arise through a subcortical pathway to the AMY, which involves the superior colliculus and the pulvinar (LeDoux, 2012).”
InfluentialUnexpected rewards induce dopamine-dependent positive emotion–like state changes in bumblebees
Solvi, C., Baciadonna, L., & Chıttka, L. (2016) · Science · doi:10.1126/science.aaf4454 · Cited by 217
A VTA GABAergic Neural Circuit Mediates Visually Evoked Innate Defensive Responses
Zhou, Z., Liu, X., Chen, S., Zhang, Z., Liu, Y., Montardy, Q., Tang, Y., Wei, P., Liu, N., Li, L., et al. (2019) · Neuron · doi:10.1016/j.neuron.2019.05.027 · Cited by 221
Time perception, emotions and mood disorders
Droit‐Volet, S. (2013) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2013.03.005 · Cited by 217
Stress exposure, food intake and emotional state.
Ulrich‐Lai, Y. M., Fulton, S., Wilson, M., Petrovich, G. D., & Rinaman, L. (2015) · PubMed · doi:10.3109/10253890.2015.1062981 · Cited by 225
“Extensive work over the last two decades has focused on determining the brain substrates underlying fear and its behavioral sequelae (LeDoux, 2012; Seymour & Dolan, 2008), and similar efforts have been directed towards examining the central substrates of hunger, food intake and energy balance…”
Sex for fun: a synthesis of human and animal neurobiology
Georgiadis, J. R., Kringelbach, M. L., & Pfaus, J. G. (2012) · Nature Reviews Urology · doi:10.1038/nrurol.2012.151 · Cited by 201
“The restructuring of sexual behaviour —and other survival behaviours 124 —into these three phases is critical in order to achieve a meaningful species comparison; although introspection and subjective feel ings are major topics in human research, it is impossible to know how animals perceive the…”
BackgroundViewpoints: Approaches to defining and investigating fear
Mobbs, D., Adolphs, R., Fanselow, M. S., Barrett, L. F., LeDoux, J. E., Ressler, K., & Tye, K. M. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0456-6 · Cited by 202
Self-citationSpecific basal forebrain-cortical cholinergic circuits coordinate cognitive operations
Záborszky, L., Gombkoto, P., Varsanyi, P., Gielow, M. R., Poe, G., Role, L. W., Ananth, M., Rajebhosale, P., Talmage, D. A., Hasselmo, M. E., et al. (2018) · The Journal of Neuroscience · doi:10.1523/jneurosci.1676-18.2018 · Cited by 202
The neural circuits of innate fear: detection, integration, action, and memorization
Silva, B. A., Gross, C. T., & Gräff, J. (2016) · Learning & Memory · doi:10.1101/lm.042812.116 · Cited by 186
“This system consists of a set of nuclei located in the hypothalamic medial zone: the anterior hypothalamic nucleus (AH), the dorsomedial portion of the ventromedial hypothalamus (VMHdm), and the dorsal premammillary nucleus (PMD).”
BackgroundThe Functional and Structural Neural Basis of Individual Differences in Loss Aversion
Canessa, N., Crespi, C., Motterlini, M., Baud‐Bovy, G., Chierchia, G., Pantaleo, G., Tettamanti, M., & Cappa, S. F. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.0497-13.2013 · Cited by 217
“These structures are critical in the detection of, as well as in the physiological and behavioral response to, aversive events and potential threats (Sehlmeyer et al., 2009; Schlund et al., 2010; LeDoux, 2012).”
BackgroundThe sound of emotions—Towards a unifying neural network perspective of affective sound processing
Frühholz, S., Trost, W. J., & Kotz, S. A. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.05.002 · Cited by 213
Emotional modulation of interval timing and time perception
Lake, J. I., LaBar, K. S., & Meck, W. H. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.03.003 · Cited by 202
Metadata
- Authors
- LeDoux, J.
- Affiliations
- New York University (US)
- Corresponding author
- LeDoux, Joseph
- ORCID
- LeDoux, Joseph
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2012-02
- Volume
- 73
- Issue
- 4
- Pages
- 653-676
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC3625946
- OpenAlex
- W2108845151
- Cited by
- 1,594
- References
- 409
- Citations by year
- 2026: 110 · 2025: 85 · 2024: 111 · 2023: 115 · 2022: 118 · 2021: 120 · 2020: 140 · 2019: 132 · 2018: 127 · 2017: 107 · 2016: 118 · 2015: 118 · 2014: 87 · 2013: 74 · 2012: 30
- FWCI
- 49.96
- Type
- journal article
- Language
- en
- Update notices
- erratum (2012-03-08)
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (R01MH038774, R01MH046516)
- National Institute on Drug Abuse (R01DA029053)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- emotions, emotional brain, motivation, reinforcement, arousal, animal emotions, neural circuits, survival function
- MeSH terms
- Animals, Brain, Brain Mapping, Emotions, Humans, Motivation, Neural Pathways, Survival
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