Motivation and emotion/Book/2018/Anterior cingulate cortex and emotion

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Anterior cingulate cortex and emotion:
What is the role of the anterior cingulate cortex in emotion?

Overview[edit]

Example case study

Barry is a 34-year-old male who sustained extensive damage in the anterior cingulate cortex during a car accident. Prior to the car accident, Barry was attentive, empathetic and expressed his emotions openly. After his accident, Barry shows emotional flatness and reduced goal orientation. This emotional flatness is evident when Fabian, an old work colleague, visits Barry in hospital. Upon asking Barry of his plans after recovery, Fabian notices Barry's attention wanders and his verbal responses lack direction. Fabian expresses some concern to Barry, however, Barry fails to detect any emotional problems.

We detect changes in ourselves and others every day. These changes, or errors, are identified as something that is different than the usual or expected. Physically, a loose stepping stone or a change in temperature are considered errors. Emotionally, errors are detected through feelings or social situations when a reaction is different to expected. We use error feedback to adjust, and behave in ways that are meaningful and adaptive. The anterior cingulate cortex (ACC) is crucial in modulating and mediating errors to facilitate our reward-based learning mechanisms (Stevens, Hurley, & Taber, 2011).

“It is how we behave when we receive feedback, that determines who we are as a person” - Manuel Saint-Victor (M.D)


Focus Questions

  1. What is the anterior cingulate cortex?
  2. What is the role of the anterior cingulate cortex in emotion?
  3. How does the anterior cingulate cortex function to improve our lives?

The anterior cingulate cortex[edit]

Figure 1. The anterior cingulate cortex of left hemisphere highlighted in red.

The ACC is the brains[grammar?] frontal cingulate cortex division consisting of cytoarchitecture Brodmann areas 24, 32, & 33 (Allman, Hakeen, Erwin, Nimchinsky, & Hof, 2006). Located within the medial wall of each cerebral hemisphere (see Figure 1), the ACCs adjacent and superior to the corpus callosum (Stevens et al., 2011). The function of the ACC is primarily linked to visceromotor, endocrine, skeletal-motor, and higher cognitive controls such as reward-anticipation, morality, and emotion (Palomero-Gallagher, Vogt, Schleicher, Mayberg, & Zilles, 2008; Stevens et al., 2011).

Neuroanatomy and physiology[edit]

The complex anatomy of the ACC is divided into two major areas: dorsal-posterior and ventral-anterior. The dorsal-posterior position is referred to as the caudal or dorsal ACC (Stevens et al., 2011), or if using Vogt's conventional system, the middle cingulate cortex (MCC) (Palomero-Gallagher et al., 2008). The ventral-anterior position is referred to as the rostral or ventral ACC (Stevens et al., 2011), or if using Vogt’s, the ACC (Palomero-Gallagher et al., 2008). The two major areas of the ACC are further subdivided. The caudal or dorsal ACC (or MCC) is divided into posterior and anterior regions, and the rostral or ventral ACC (or ACC) is divided into the pregenual and subgenual regions (Stevens et al., 2011).

The Stroop task[edit]

The ACC is divided between cognition and emotion (Allman et al., 2006). The dorsal ACC (or MCC) has associations with cognition, and the ventral ACC has associations with emotion (Allman et al., 2006). This segregation can be confirmed using different versions of the Stroop effect task. The Stroop task measures delays in subject responses when presented with confounding or conflicting information (Macleod, 1991). In the counting (cognitive) Stroop task, words are presented multiple times as numbers and the participant reports the number of words (Song et al., 2017). In the emotional Stroop task, the participant is given a mix of emotional and neutral words and reports the colour of the word (Song et al., 2017). Activation of the dorsal ACC correlates with the counting Stroop, and activation of the ventral ACC correlates with the emotional Stroop (Allman et al., 2006; Song et al., 2017).

Spindle neurons[edit]

Figure 2. Drawing of a normal pyramidal cell (left) and Spindle-cell (right)

Von Economo neurons (VENs), or spindle neurons (see Figure 2), are projection-neurons found abundantly in layer-V of the human ACC and insular cortex (Allman et al., 2006; Allman et al., 2011; Stevens et al., 2011). Activation contributes to coordination, problem-solving, and emotional self-control (Allman et al., 2006; Allman et al., 2011). At birth, VENs cannot be discerned. At approximately four months old, VENs develop widespread connections throughout the ACC and insular cortex in the human brain (Allman et al., 2006; Allman et al., 2011).

VENs may be a recent evolutionary specialisation as they are responsible for intuitive awareness and perceptual recognition in animals with increased brain size and complex social cognition (Allman et al., 2006; Allman et al., 2011). This theory is supported by varying distributions of VEN density among species, allowing for rapid relay of socially relevant information over long distances in the brain (Allman et al., 2006; Nimchinsky et al., 1999). Phylogenetics can identify a difference in biochemical specificity within VEN (Stimpson et al., 2011). A study by Stimpson et al. (2011) used phylogenetic staining to show the difference in biochemical specificity within VENs. Stimpson et al. state the difference in ACC protein expression of VENs suggests humans evolved biochemical specialisations for interoceptive (gut-based emotion) sensitivity.

The role of the anterior cingulate cortex in emotion[edit]

Example Scenario 1

Imagine you're a university student and notice a flyer offering $50 for participation in a psychological study. You feel uneasy but need the money and attend the experiment. Prior to commencement, you're connected to brain measuring equipment that makes you even more uncomfortable. The experimenter asks if you’d like to proceed so you take a moment to think. You convince yourself it's safe and suppress your fears. The experiment is completed and you receive the reward of $50. Feeling good about the outcome, you leave feeling relieved and consider participating in future experiments.

Figure 3. Emotions connected via cognition

Emotion is a complex, subjective, and expressive experience categorised by physiological reactions and mental states of mind (Pessoa, 2008). Although no consensus has been reached in scientific literature, brain regions responsible for both emotion and cognitive control are suggested to share the neural circuitry responsible for conflict resolution between cognition and emotion (Pessoa, 2008; Song et al., 2017). Areas with higher degrees of connectivity such as the ACC have a role in integrating the cognitive neuronal circuitry for affect regulation (see Figure 3) (Pessoa, 2008; Stevens et al., 2011)

Activation by emotion[edit]

The ACC may be thought of as an interface between cognition and emotion (Allman et al., 2006). Each anatomical division may perform unique roles (see Table 1), however, there is also overlap between divisions allowing for the complexity of the ACC to integrate cognition and emotions with other cortical areas (Stevens et al., 2011).


Table 1
Divisions of ACC activated by emotion

Division of ACC Activates in response to Part of division Other commonly used acronyms
anterior Middle Cingulate Cortex (aMCC) Emotional appraisals, cognitive control, conflict monitoring, and error detection Caudal or dorsal ACC or MCC acACC or adACC
posterior Middle Cingulate Cortex (pMCC) Action selection, fear associated with faces, and learned fear Caudal or dorsal ACC or MCC pcACC or pdACC
pregenual Anterior Cingulate Cortex (pgACC) Affective processing, emotion regulation, and simple emotions Rostral or ventral ACC pACC
subgenual Anterior Cingulate Cortex (sgACC) Emotional reward value, emotional conflict evaluation, and simple emotions Rostral or ventral ACC sACC

Anterior and posterior caudal/dorsal ACC (or MCC)[edit]

The MCC activates predominantly to cognitive evaluations and emotional conflict (Pessoa, 2008; Stevens et al., 2011). A study by Vogt, Berger, and Derbyshire (2003) monitored the regulation of 45 total emotions. Within the anterior middle cingulate cortex (aMCC), Vogt found six locations activated in response to fearful faces. Additionally, meta-analyses show the aMCC is responsive to associations of fear (Phan, Wager, Taylor, & Liberzon, 2002). As aMCC activation corresponds to non-habitual responses in threatening situations, Shackman et al. (2011) proposed an adaptive model based on cognitive control theories. According to the adaptive control hypothesis, pain and negative affect engages a cognitive bias during uncertainty to derive an optimal solution similar to reinforcement learning (Shackman et al., 2011). Overall, the aMCC activates in response to: emotional appraisals, cognitive control, conflict monitoring, and error detection (Stevens et al., 2011).

Studies of the posterior middle cingulate cortex (pMCC) show greater involvement with motor system processing when compared with the aMCC (Palomero-Gallagher, 2008). Further evidence segregating the subdivisions using receptor analysis indicates the pMCC is denser with gamma-aminobutyric acid (GABA) inhibitory receptors type-B that are synonymous with motor regions (Vogt et al., 2003). There is, however, no consistent involvement with the pMCC and simple emotions. A study by Vogt et al. (2003) found only one of the ten activations in response to fearful faces was linked with the pMCC. Additionally, Vogt et al. identified two activation sites for anger evoked diffusion within the pMCC. The association with motor processing and the marginal connectivity to fearful stimuli suggests the pMCCs role in mediating action response expressions to fear (Etkin, Egner, & Kalish, 2011; Stevens et al., 2011). Overall, the pMCC activates in response to: action selection, fear associated with faces, and learned fear (Stevens et al., 2011).

Pregenual and subgenual regions of the ACC[edit]

The ventral ACC activates predominantly to affective processing (Pessoa, 2008; Stevens et al., 2011). Imaging studies show that the pregenual ACC (pgACC) is widely connected to areas that evaluate internal/external stimuli (Yu et al., 2011). If the stimuli’s evaluated as motivational, the pgACC contributes to evoking an emotional reaction (Etkin et al., 2011; Stevens et al., 2011). A study by Beauregard, Levesque, and Bourgouin (2001) observed pgACC activity in participants actively inhibiting emotions in response to erotic stimuli. The limbic areas that typically respond were suppressed, indicating the pgACC contributes to top-down emotional regulation (Beauregard, Levesque, & Bourgouin, 2001). Projections from thalamic nuclei to the pgACC have been identified that contribute to pain related affect (Vogt et al., 2005), however, fewer are received when compared with the aMCC (Stevens et al., 2011). In the simple emotions study performed by Vogt et al. (2003), ten pgACC sites were activated in response to happiness in addition to low levels of ventral activity in response to sadness. When the results were localised, pain, happiness, fear, and sadness were independent of one another (Vogt et al., 2003). Overall, the pgACC activates in response to: affective processing, emotion regulation, and simple emotions.

Imaging studies show an anti-correlation between the pgACC and subgenual ACC (sgACC) (Stevens et al., 2011; Yu et al., 2011). The sgACC is sparsely connected to areas involving affective processing, however, there are reciprocal connections with the limbic system and autonomic centres (Etkins et al., 2011; Yu et al., 2011). Assessment and evaluation is shown to activate the sgACC during choices based on reward value (Stevens et al., 2011). When reward-based options are encountered, activation correlates with reward-based motivational, cognitive, and contextual variables (Stevens et al., 2011). Activation of the sgACC is also correlated with inhibition of fear, and emotional conflict-regulation (Etkin et al., 2011). A study by Etkin, Egner, Peraza, Kandel & Hirsch (2006) showed participants made delayed responses when presented with incongruent word labels and facial expressions. The sgACC was activated during the emotional conflict distinguishing itself in times of conflict regulation (Etkin et al., 2006). Like the pgACC, the sgACC contributes to simple emotions (Allman et al., 2006; Stevens et al., 2011; Vogt et al., 2003). The sgACC activates more sites in response to sadness than does the pgACC (Stevens et al., 2011). The contrary is true for happiness, such that the sgACC activates less (Stevens et al., 2011). In studies using positron-emission tomography, the sgACC is activated when subjects imagined situations relating to either anger or sadness (Allman et al., 2006). Overall, the sgACC activates in response to: emotional reward value, emotional conflict evaluation, and simple emotions.

How the anterior cingulate cortex functions to improve our emotional lives[edit]

Example Scenario 2

Imagine you are in a team-based hiking exercise with some strangers. You’re feeling motivated and decide to take some of the team’s heavier gear, but carrying the gear becomes strenuous after a couple of hours. Although you keep the pace, you become distracted as you feel your heart beat and breathing rate change. One of your team-mates senses this change and offers support.

Our emotions are on a constant continuum mediated and modulated by regions of the brain such as the ACC (Murphy, Brewer, Catmur, & Bird, 2017). To function effectively and to improve our emotional behaviours, the ACC performs an integral role regulating internal states available to awareness such as ones own heart rhythm (Ernst et al., 2013). By understanding the internal states of ourselves and others through experimental and clinical literature we can appreciate how the ACC functions to improve our emotional lives.

Theory of mind: interoception[edit]

Figure 4. Interoception and the body.

Having a theory of mind is referred to as having an understanding in another’s beliefs, intentions, and feelings achieved through exteroceptive, proprioceptive, and interoceptive signals (Ondobaka, Kilner, & Friston, 2017). The processing of internal visceral and automatic information (see Figure 4) informs an individual of intentions and beliefs that guide behaviour (Ondobaka et al., 2017). By becoming more self aware of our own bodily states and others, we are able to make critical top-down decisions to become more adaptive as both individuals and group members (Thom et al., 2014).

Interoception[edit]

Interoception is the subjective awareness of the body's internal physiological states such as heart rate, temperature and hunger (Murphy et al., 2017; Thom et al., 2004). Interoception is a foundation for self-awareness and socio-affective abilities involving emotion and a contributor to higher order social cognition (Murphy et al., 2017). Although research is still unclear, emotional experiences are both mediated and modulated by interoceptive awareness (Ernst, et al., 2013). Along with the insular cortex and somatosensory afferent transmission, the ACC is credited to be a primary component for interoceptive awareness (Ernst, et al., 2013; Khalsa, Rudrauf, Feinstein, & Tranel, 2009; Murphy et al., 2017). Accurately perceiving internal states is important for general health, and atypical interoceptive sensitivity is found to be associated with physical health disorders such as diabetes and obesity (Werner, Jung, Duschek, & Schandry, 2009). A model proposed by Quattrocki and Friston (2014) suggests a failure of interoceptive sensitivity prevents contextualisation of internal and external emotional signals resulting in an impoverished sense of self and social difficulties.

Adventure racers and the interoceptive model[edit]

Figure 5. Hiking as a team successfully requires the use of interoception.

For safety and performance reasons, it is important to be aware of one's physiological state and others emotions during activities such as hiking (see Figure 5). Individuals who respond well to high-degree stressors are theorised to have an improved and well-contextualised interoceptive sense (Paulus et al., 2009). High stressors impair cognitive function, alter emotional regulation, and result in interpersonal challenges (Paulus et al., 2009; Richardson, 2017). Although high levels of stress can be detrimental, individuals are able to recover, adapt to, and even thrive under these conditions (Southwick, Vythilingam, & Charney, 2005). A study by Thom et al. (2014) used functional magnetic resonance imaging to examine changes of adventure racers in brain regions contributing to emotional processing and social awareness such as the insular, amygdala, and ACC. Thom et al. found greater activation in the right insular and the dorsal ACC when compared to control groups, and suggested adventure racers utilise these regions to process emotions in others more effectively possibly-being advantageous under stressful team-based conditions. Results by Thom et al. provide context to the modulation of neural circuitry that contributes to optimal performance under stressful conditions, and also supports the MCCs role in emotional appraisal (Stevens et al., 2011).

Atypical interoception[edit]

Atypical interoception contributes to risky behaviours, psychopathy, and affective disorders with modified insular and ACC functions (Ernst et al, 2013). Alexithymia is a condition involving difficulties identifying and describing emotions characterised by atypical interoceptive sensitivity, maladaptive coping mechanisms, and neuroticism (Ernst et al., 2013; Murphy et al., 2017). Ernst et al. (2013) examined the involvement of the insular and the ACC with alexithymics by investigating their relationships with the excitatory neurotransmitter glutamate, and the inhibitory neurotransmitter GABA. Using proton magnetic resonance spectroscopy, high insular levels of glutamate, and high ventral ACC levels of GABA were detected in alexithymics (Ernst et al., 2013). Ernst et al. suggests increases of dorsal ACC activity may represent emotional suppression resulting from glutamate mediated insular activity. This leads to GABA mediated inhibition of the ventral ACC, displayed through emotional flatness (Ernst et al., 2013).

Improving negative emotions[edit]

Figure 6. Alaska Guardsmen teach drug awareness and coping strategies to cadets.

Negative emotions are associated with activation of the ACC which modulates behaviour (Stevens et al., 2011). Tikasz et al. (2016) showed hyper-activation of the ACC among violent men with schizophrenia in response to negative stimuli when compared with healthy control participants. To the contrary, disorders such as depression and post-traumatic stress disorder display below normal activation in the sgACC and aMCC (Stevens et al., 2011). A study by Ohmatsu et al. (2014) explored ACC modulation through pedal exercise. Using electroencephalograph measures, Ohmatsu et al. found decreases in negative emotion linked with the ACC and increases in positive emotion linked with the serotonin system. Exercise is not the only modulator of the ACC. coping mechanisms play a significant role in negative emotions (see Figure 6). A study by Perlman and Pelphrey (2010) found children faced with a challenging task possessing greater coping strategies had increased dorsal ACC activity. Temperamental children, however, had increased ventral ACC activity when challenged suggesting reduced cognition and higher reliance on emotions during difficulties (Perlman and Pelphrey, 2010). These findings indicate activation of the ACC varies on a continuum like basis and may be modulated through exercise and well-developed coping strategies.

Conclusion[edit]

The ACC consists of specialised spindle shaped cells that provide the neural circuitry for complex cognitive and emotional functions[for example?]. Divided into two major divisions and four subdivisions, the ACC acts as an interface between cognition and emotion with other brain regions. The subdivisions of the ACC activate in response to emotional appraisals, emotional conflict evaluation, error detection, affect processing, reward value, and simple emotions{{example}. Emotional experiences are both mediated and modulated by interoceptive awareness[for example?]. Thus, accurately perceiving internal states is vital for making top-down decisions to become more adaptive as an individual or a team member. Negative emotions, while unpleasant, are regulated by the ACC and may be reduced through exercise and effective coping strategies.

The take-home message: By identifying how you respond to unexpected changes, you can influence your emotional reactions to adapt to your environment.

Quiz questions[edit]

Test your knowledge of this topic by answering multiple choice questions. Choose the correct answer and click "Submit":

Which region of the anterior cingulate cortex is associated with cognition more than emotion?

Rostral
Inferior
Dorsal
Ventral
Posterior

Which of the following roles does the anterior cingulate cortex have in emotion?

Responsible for the perception of emotions
Integrates neural circuitry for affect regulation
Decision making in response to emotions
Synthesis of neurotransmitters responsible for activating emotion
Consists of spindle neurons (present in all great apes) that transmit solely negative emotions.

How does the anterior cingulate cortex function to improve our emotional lives?

Allows us to forget emotionally charged events
Provides us with the ability to exert cognitive control over decision making
Responsible for arousal, alertness, and awakening the brain in response to sensory information
Plays an important role in emotional awareness
Evaluates the unlearned emotional value of internal body states


See also[edit]

References.[edit]

Allman, J. M., Hakeem, A., Erwin, J. M., Nimchinsky, E., & Hof, P. (2006). The anterior cingulate cortex: The evolution of an interface between emotion and cognition. Annals New York Academy of Sciences, 935. 107-117. https://doi.org/10.1111/j.1749-6632.2001.tb03476.x

Allman, J. M., Tetreault, N. A., Hakeem, A. Y., Manaye, K. F., Semendeferi, K., Erwin, J. M., … Hof, P. R. (2011). The von Economo neurons in fronto-insular and anterior cingulate cortex. Annals of the New York Academy of Sciences, 1225, 59-71. https://doi.org/10.1111/j.1749-6632.2011.06011.x

Beauregard, M., Levesque, J., & Bourgouin, P. (2001). Neural correlates of conscious self-regulation of emotion. The Journal of Neuroscience, 21, 6993-7000.

Ernst, J., Boker, H., Hattenschwiler, J., Schupbach, D., Northoff, G., Seifritz, E., & Grimm, S. (2013). The association of interoceptive awareness and alexithymia with neurotransmitter concentrations in insula and anterior cingulate. Social Cognitive and Affective Neuroscience, 9(6), 1-7. https://doi.org/10.1093/scan/nst058

Etkin, A., Egner, T., & Kalisch, R. (2011). Emotional processing in anterior cingulate and medial prefrontal cortex. Trends in Cognitive Sciences, 15, 85-93. https://doi.org/10.1016/j.tics.2010.11.004

Etkin, A., Egner, T., Peraza, D. M., Kandel, E. R., & Hirsch, J. (2006). Resolving emotional conflict: a role for the rostral anterior cingulate cortex in modulating activity in the amygdala. Neuron, 51, 871-882. https://doi.org/10.1016/j.neuron.2006.07.029

Khalsa, S. S., Rudrauf, D., Feinstein, J. S., & Tranel, D. (2009). The pathways of interoceptive awareness. Nature Neuroscience, 12, 1494-1496. https://doi.org/10.1038/nn.2411

MacLeod, C. M. (1991). Half a century of research on the Stroop effect: an integrative review. Psychological bulletin, 109, 163-203. https://doi.org/10.1037/0033-2909.109.2.163

Murphy, J., Brewer, R., Catmur, C., & Bird, G. (2017). Interoception and psychopathology: A developmental neuroscience perspective. Development of Cognitive Neuroscience, 23, 45-56. https://doi.org/10.1016/j.dcn.2016.12.006

Nimchinsky, E. A., Gillissen, E., Allman, J. M., Perl, D. P., Erwin, J. M., & Hof, P. R. (1999). A neuronal morphologic type unique to humans and great apes. Proceedings of the National Academy of Sciences of the United States of America, 96, 5268-5273.

Ohmatsu, S., Nakano, H., Tominaga, T., Terakawa, Y., Murata, T., & Morioka, S. (2014). Activation of the serotonergic system by pedaling exercise changes anterior cingulate cortex activity and improves negative emotion. Behavioural Brain Research, 270, 112-117. https://doi.org/10.1016/j.bbr.2014.04.017

Ondobaka, S., Kilner, J., & Friston, K. (2017). The role of interoceptive inference in theory of mind. Brain Cognition, 112, 64-68. https://doi.org/10.1016/j.bandc.2015.08.002

Paulus, M. P., Potterat, E. G., Taylor, M. K., Van Orden, K. F., Bauman, J., Momen, N. … Swain, J. L. (2009). A neuroscience approach to optimizing brain resources for human performance in extreme environments. Neuroscience and Biobehavioral Reviews, 33, 1080-1088. https://doi.org/10.1016/j.neubiorev.2009.05.003

Perlman, S. B., & Pelphrey, K. A. (2010). Regulatory Brain Development: Balancing Emotion and Cognition. Social Neuroscience, 5, 533-542. https://doi.org/10.1080/17470911003683219

Pessoa, L. (2008). On the relationship between emotion and cognition. Nature Reviews Neuroscience, 9, 148-158. https://doi.org/10.1038/nrn2317

Phan, K. L., Wager, T. Taylor, S. F., & Liberzon, I. (2002). Functional neuroanatomy of emotion: A meta-analysis of emotion activation studies in PET and fMRI. Neuroimage, 16, 331-348. https://doi.org/10.1006/nimg.2002.1087

Quattrocki, E., & Friston, K. (2014). Autism: oxytocin and interoception. Neuroscience and Biobehavioural Reviews, 47, 410-430. https://doi.org/10.1016/j.neubiorev.2014.09.012

Richardson, C. M. E. (2017). Emotion regulation in the context of daily stress: Impact on daily affect. Personality and Individual Differences, 112, 150-156. https://doi.org/10.1016/j.paid.2017.02.058

Shackman, A. J., Salomons, T. V., Slagter, H. A., Fox, A. S., Winter, J. J., & Davidson, R. J. (2011). The integration of negative affect, pain and cognitive control in the cingulate cortex. Nature Reviews Neuroscience, 12, 154-167. https://doi.org/10.1038/nrn2994

Song, S., Zilverstand, A., Song, H., Uquillas, F. D. O., Wang, Y., Xie, C., … Zou, Z. (2017). The influence of emotional interference on cognitive control: A meta-analysis of neuroimaging studies using the emotional Stroop task. Scientific Reports, 7(2088), 1-9. https://doi.org/10.1038/s41598-017-02266-2

Southwick, S. M., Vythilingam, M., & Charney, D. S. (2005). The psychobiology of depression and resilience to stress: Implications for prevention and treatment. Annual Review of Clinical Psychology, 1, 255-91. https://doi.org/10.1146/annurev.clinpsy.1.102803.143948

Stevens, F. L., Hurley, R. A., & Taber, K. H. (2011). Anterior Cingulate Cortex: Unique Role in Cognition and Emotion. The Journal of Neuropsychiatry and Clinical Neurosciences, 23, 121-125. https://doi.org/10.1176/jnp.23.2.jnp121

Stimpson, C. D., Tetreault, N. A., Allman, J. M., Jacobs, B., Butti, C., Hof, P. R., Sherwood, C. C. (2011). Biochemical specificity of von Economo neurons in hominoids. American Journal of Human Biology, 23, 22-28. https://doi.org/10.1002/ajhb.21135

Thom, N. J., Johnson, D. C., Flagan, T., Simmons, A. N., Kotturi, S. A., Van Orden, K. F., Potterat, E. G., Swain, J. L., & Paulus, M. P. (2014). Detecting emotion in others: increased insula and decreased medial prefrontal cortex activation during emotion processing in elite adventure racers. Social Cognitive and Affective Neuroscience, 9, 225-231. https://doi.org/10.1093/scan/nss127

Tikasz, A., Potvin, S., Lungo, O., Joyal, C. C., Hodgins, S., Mendrek, A., & Dumais, A. (2016). Anterior cingulate hyperactivations during negative emotion processing among men with schizophrenia and a history of violent behavior. Neuropsychiatric Disease and Treatment, 15, 1397-410. https://doi.org/10.2147/NDT.S107545

Vogt, B. A., Berger, G. R., & Derbyshire, S. W. G. (2003). Structural and Functional Dichotomy of Human Midcingulate Cortex. European Journal of Neuroscience, 18, 3134-3144. https://doi.org/10.1038/nrn1704

Werner, N. S., Jung, K., Duschek, S., & Schandry, R. (2009). Enhanced cardiac perception is associated with benefits in decision-making. Psychophysiology, 46, 1123-1129. https://doi.org/10.1111/j.1469-8986.2009.00855.x

Yu, C., Zhou, Y., Liu, Y., Jiang, T., Dong, H., Zhang, Y., Walter, M. (2011). Functional segregation of the human cingulate cortex is confirmed by functional connectivity based neuroanatomical parcellation. NeuroImage, 54, 2571-2581. https://doi.org/10.1016/j.neuroimage.2010.11.018

External links[edit]