Skip to main content

Fronto-striatal activity predicts anhedonia and positive empathy subtypes

Brain Imaging and Behavior volume 13, pages 1554–1565 (2019)Cite this article

Abstract

The dorsolateral prefrontal cortex, globus pallidus, and nucleus accumbens are important components of the reward circuit in the brain; and prior research suggests individuals with damage to these regions feel less pleasure (i.e., are anhedonic). However, little is known about how these brain regions relate to vicarious pleasure. Pilot fMRI data were collected from 20 participants (Mage = 22, SD = 7.0, 63% female) during a validated empathy induction paradigm that utilized video clips extracted from the television show “Extreme Makeover: Home Edition” to elicit empathic happiness (i.e. vicarious happiness) when targets display positive affect, and either empathic cheerfulness (i.e. the tendency to want to cheer someone up) or empathic concern (i.e. vicarious sadness) when targets display negative affect. Participants also completed the novel “Happy Faces” task—a behavioral measure of anhedonia—while fMRI was collected. fMRI data during task completion were used to predict trait empathy measured via self-report outside of the scanner, and accuracy on the “Happy Faces” task. Results indicate that globus pallidus activity during empathic concern-eliciting video clips significantly predicted self-reported trait empathic cheerfulness (R2 = 26%, p = 0.045). Furthermore, greater dorsolateral prefrontal cortex (DLPFC) activity during the Happy Faces task predicted accurate performance on the task (R2 = 34%, p < .05); and greater nucleus accumbens shell activity during the Happy Faces task predicted greater trait empathic happiness (R2 = 38%, p < .05). These results suggest that fronto-striatal circuitry contributes to our experience of anhedonia, empathic happiness, and empathic cheerfulness.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  • Adam, R., Leff, A., Sinha, N., Turner, C., Bays, P., Draganski, B., & Husain, M. (2012). Dopamine reverses reward insensitivity in apathy following globus pallidus lesions. Cortex, 49, 1292–1303. https://doi.org/10.1016/j.cortex.2012.04.013.

    Article  PubMed  Google Scholar 

  • Ambadar, Z., Cohn, J. F., & Reed, L. I. (2009). All smiles are not created equal: Morphology and timing of smiles perceived as amused, polite, and embarrassed/nervous. Journal of Nonverbal Behavior, 33, 17–34.

    Article  Google Scholar 

  • Anderson, rS. W., Barrash, J., Bechara, A., & Tranel, D. (2006). Impairments of emotion and real-world complex behavior following childhood- or adult-onset damage to ventromedial prefrontal cortex. Journal of the International Neuropsychological Society, 12, 224–235.

  • Anton J.M., Loonen, Arnt, F.A Schellekens and Svetlana A. Ivanova (2016). Circuits Regulating Pleasure and Happiness: A Focus on Addiction, Beyond the Ventral Striatum, Recent Advances in Drug Addiction Research and Clinical Applications, Dr. William Meil (Ed.), InTech, https://doi.org/10.5772/62707.

    Google Scholar 

  • Baliki, et al. (2013). Parceling human accumbens into putative core and shell dissociates encoding of values for reward and pain. Journal of Neuroscience, 33, 16383–16393.

    Article  CAS  Google Scholar 

  • Berridge, K. C., & Kringelbach, M. (2015). Pleasure Systems in the Brain. Neuron, 86, 646–664. https://doi.org/10.1016/j.neuron.2015.02.018.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhatia, K. P., & Marsden, C. D. (1994). The behavioral and motor consequences of focal lesions of the basal ganglia in man. Brain, 117, 859–876.

    Article  Google Scholar 

  • Blair, J. R., Leibenluft, E., & Pine, D. S. (2014). Conduct disorder and callous-unemotional traits in youth. The New England Journal of Medicine, 371, 2207–2216.

    Article  CAS  Google Scholar 

  • Castro, D.C. & Berridge, K.C. (2014). Opioid hedonic hotspot in nucleus accumbens shell: Mu, delta, and kappa maps for enhancement of sweetness “liking” and ”wanting.” Journal of Neuroscience, 34, 4239–4250.

  • Cauda, F., Cavanna, A. E., D’agata, F., Sacco, K., Duca, S., & Geniniani, G. C. (2011). Functional connectivity and coactivation of the nucleus accumbens: A combined functional connectivity and structure-based meta-analysis. Journal of Cognitive Neuroscience, 23, 2864–2877.

    Article  Google Scholar 

  • Clark, L., Cools, R., & Robbins, T. W. (2004). The neuropsychology of ventral prefrontal cortex: Decision-making and reversal learning. Brain Cognition, 55, 41–53.

    Article  CAS  Google Scholar 

  • Cohn, J. F., Zlochower, A. J., Lien, J., & Ambadar, Z. (1999). Automatic face analysis by feature tracking has high convergent validity with manual FACS coding. Psychophysiology, 36, 35–43.

    Article  CAS  Google Scholar 

  • Dichter, G. S., Feldner, J. N., Petty, C., Bizzell, J., Ernst, M., & Smoski, M. J. (2009). The effects of psychotherapy on neural responses to rewards in major depression. Biological Psychiatry, 66, 886–897.

    Article  Google Scholar 

  • Dillon, D. G., Holmes, A. J., Birk, J. L., Brooks, N., Lyons-Ruth, K., & Pizzagali, D. A. (2009). Childhood adversity is associated with left basal ganglia dysfunction during reward anticipation in adulthood. Biological Psychiatry, 66, 206–213.

    Article  Google Scholar 

  • Heller, A. S., Johnstone, T., Shackman, A. S., Light, S. N., Peterson, M., Kolden, G., Kalin, N., & Davidson, R. J. (2009). Reduced capacity to sustain positive emotion in major depression reflects diminished maintenance of fronto-striatal brain activation. Proceedings of the National Academy of Sciences, 106, 22445–22450.

    Article  CAS  Google Scholar 

  • Heller, A. S., van Reekum, C. M., Schaefer, S. M., Lapate, R. C., Radler, B. T., Ryff, C. D., & Davidson, R. J. (2013). Sustained striatal activity predicts eudaimonic well-being and cortisol output. Psychological Science, 24, 2191–2200.

    Article  Google Scholar 

  • Kringelbach, M.L. & Berridge, K.C. (2012). The joyful mind. Scientific American, August, 40–45, 307.

  • Light, S. N., Coan, J. A., Zahn-Waxler, C., Frye, C., Goldsmith, H. H. & Davidson, R. J. (2009). Empathy is associated with dynamic change in prefrontal brain electrical activity during positive emotion in children. Child Development, 80, 1210–1231.

  • Light, S. N., Heller, A. S., Johnstone, T., Kolden, G. G., Peterson, M. J., Kalin, N., & Davidson, R. J. (2011). Reduced ventrolateral prefrontal cortex activity while inhibiting positive affect is associated with improvement in hedonic capacity after 8 weeks of antidepressant treatment in major depressive disorder. Biological Psychiatry, 70, 962–968.

    Article  CAS  Google Scholar 

  • Light, S. N., Moran, Z. D., Swander, L., Le, V., Cage, B., Burghy, C., Westbrooke, C., Greishar, L., & Davidson, R. J. (2015). Electromyographically assessed empathic concern and empathic happiness predict increased prosocial behavior in adults. Biological Psychology, 104, 116–129 PMCID: PMC5104350.

    Article  Google Scholar 

  • Lindquist, K. A., Satpute, A. B., Wager, T. D., Weber, J., & Feldman Barrett, L. (2013). The brain basis of positive and negative affect: Evidence from a meta-analysis of the human neuroimaging literature. Cerebral Cortex, 26, 1910–1922.

    Article  Google Scholar 

  • Miller, J. M., Vorel, S. R., Tranguch, A. J., Kenny, E. T., Mazzoni, P., van Gorp, W. G., & Kleber, H. D. (2006). Anhedonia after a selective bilateral lesion of the globus pallidus. American Journal of Psychiatry, 163, 786–788.

    Article  Google Scholar 

  • Morelli, S., Sacchet, M. D., & Zaki, J. (2015). Common and distinct neural correlates of personal and vicarious reward: A quantitative meta-analysis. Neuroimage, 112, 244–253. https://doi.org/10.1016/j.neuroimage.2014.12.056.

    Article  Google Scholar 

  • Niedenthal, P. M., Mermillod, M., Maringer, M., & Hess, U. (2010). The simulation of smiles (SIMS) model: Embodied simulation and the meaning of facial expression. Behavioral and Brain Sciences, 33, 417–480.

    Article  Google Scholar 

  • Seara-Cardoso, A., & Viding, E. (2014). Functional neuroscience of psychopathic personality in adults. Journal of Personality, 83, 723–737.

    Article  Google Scholar 

  • Singer, T., Seymour, B., O’Doherty, J., Kaube, H., Dolan, R. J., & Frith, C. D. (2004). Empathy for pain involves the affective but not sensory components of pain. Science, 303, 1157–1162.

    Article  CAS  Google Scholar 

  • Soucy Chartier, I., & Provencher, M. D. (2013). Behavioral activation for depression: Efficacy, effectiveness and dissemination. Journal of Affective Disorders, 145, 292–299.

    Article  Google Scholar 

  • Szczepanski, S. M., & Knight, R. T. (2014). Insights into human behavior from lesions to the prefrontal cortex. Neuron, 83(5), 1002–1018.

    Article  CAS  Google Scholar 

  • Tindell, A. J., Berridge, K. C., & Aldridge, J. W. (2004). Ventral pallidal representation of pavlovian cues and reward: Population and rate codes. Journal of Neuroscience, 24, 1058–1068.

    Article  CAS  Google Scholar 

  • Treadway, M. T., & Zald, D. H. (2011). Reconsidering anhedonia in depression: Lessons from translational neuroscience. Neuroscience and Biobehavioral Reviews, 35, 537–555. https://doi.org/10.1016/j.neubiorev.2010.06.006.

    Article  PubMed  Google Scholar 

  • Vijayaraghavan, L., Vaidya, J. G., Humphreys, C. T., Beglinger, L. J., & Paradiso, S. (2008). Emotional and motivational changes after bilateral lesions of the globus pallidus. Neuropsychology, 22, 412–418.

    Article  Google Scholar 

  • Zacharopoulos, G., Lancaster, T. M., Bracht, T., Ihssen, N., Maio, G. R., & Linden, D. E. J. (2016). A hedonism hub in the human brain. Cerebral Cortex, 26, 3921–3927. https://doi.org/10.1093/cercor/bhw197.

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This study was funded by a 2015–2016 Seed grant from the Joint Georgia State University/Georgia Tech Center for Advanced Brain Imaging (CABI).

Author information

Authors and Affiliations

  1. Neuroscience Institute, Georgia State University, 100 Piedmont Ave SE, Atlanta, GA, 30303, USA

    Grazia Mirabito

  2. Department of Psychology, Georgia State University, 140 Decatur Street, Atlanta, GA, 30303, USA

    Zinat Taiwo

  3. Dynamic Cognition Laboratory, Washington University in St. Louis, Campus Box 1125, One Brookings Drive, St. Louis, MO, 63130, USA

    Matt Bezdek

  4. Positive Affective Neuroscience Laboratory, Department of Psychology, Georgia State University, 140 Decatur Street, Atlanta, GA, 30303, USA

    Sharee N. Light

  5. Center for Advanced Brain Imaging (CABI), 831 Marietta St NW, Atlanta, GA, 30318, USA

    Sharee N. Light

Authors
  1. Grazia Mirabito
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zinat Taiwo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Matt Bezdek
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sharee N. Light
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sharee N. Light.

Ethics declarations

Conflict of interest

Grazia Mirabito declares that she has no conflict of interest. Zinat Taiwo declares that she has no conflict of interest. Dr. Matt Bezdek declares that he has no conflict of interest. Dr. Sharee N. Light declares that she has no conflict of interest.

Ethical approval

All procedures performed were in accordance with the ethical standards of the Center for Advanced Brain Imaging Institutional Review Board (IRB) and with the 1964 Helsinki declaration and its later amendments. Informed consent was obtained from all individual participants included in the study.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Mirabito, G., Taiwo, Z., Bezdek, M. et al. Fronto-striatal activity predicts anhedonia and positive empathy subtypes. Brain Imaging and Behavior 13, 1554–1565 (2019). https://doi.org/10.1007/s11682-019-00081-z

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-019-00081-z

Keywords

  • fMRI
  • Positive empathy
  • Anhedonia