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Differential regulation of observational fear and neural oscillations by serotonin and dopamine in the mouse anterior cingulate cortex

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Abstract

Rationale

The aberrant regulation of serotonin (5-HT) and dopamine (DA) in the brain has been implicated in neuropsychiatric disorders associated with marked impairments in empathy, such as schizophrenia and autism. Many psychiatric drugs bind to both types of receptors, and the anterior cingulate cortex (ACC) is known to be centrally involved with empathy. However, the relationship between the 5-HT/DA system in the ACC and empathic behavior is not yet well known.

Objectives

We investigated the role of 5-HT/DA in empathy-like behavior and in the regulation of ACC neural activity.

Methods

An observational fear learning task was conducted following microinjections of 5-HT, DA, 5-HT and DA, methysergide (5-HT receptor antagonist), SCH-23390 (DA D1 receptor antagonist), or haloperidol (DA D2 receptor antagonist) into the mouse ACC. The ACC neural activity influenced by 5-HT and DA was electrophysiologically characterized in vitro and in vivo.

Results

The microinjection of haloperidol, but not methysergide or SCH-23390, decreased the fear response of observing mice. The administration of 5-HT and 5-HT and DA together, but not DA alone, reduced the freezing response of observing mice. 5-HT enhanced delta-band activity and reduced alpha- and gamma-band activities in the ACC, whereas DA reduced only alpha-band activity. Based on entropy, reduced complexity of ACC neural activity was observed with 5-HT treatment.

Conclusions

The current results demonstrated that DA D2 receptors in the ACC are required for observational fear learning, whereas increased 5-HT levels disrupt observational fear and alter the regularity of ACC neural oscillations.

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Acknowledgments

This work was supported by the Korea Health 21 R&D grant (HI12C0035) funded by Ministry of Health and Welfare, and M.W.J was supported by the Research Center Program of the Institute for Basic Science, Korea.

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  1. Department of Bio and Brain Engineering, Korea Advanced Institute of Science and Technology (KAIST), Daejeon, 305-701, Republic of Korea

    Byung Sun Kim, Junghee Lee, Minji Bang, Bo Am Seo, Arshi Khalid & Daejong Jeon

  2. Center for Synaptic Brain Dysfunctions, Institute for Basic Science and Department of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST), Daejeon, 305-701, Republic of Korea

    Min Whan Jung

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  1. Byung Sun Kim
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Kim, B.S., Lee, J., Bang, M. et al. Differential regulation of observational fear and neural oscillations by serotonin and dopamine in the mouse anterior cingulate cortex. Psychopharmacology 231, 4371–4381 (2014). https://doi.org/10.1007/s00213-014-3581-7

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