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Bilateral lesions of the medial frontal cortex disrupt recognition of social hierarchy during antiphonal communication in naked mole-rats (Heterocephalus glaber)

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Abstract

Generation of the motor patterns of emotional sounds in mammals occurs in the periaqueductal gray matter of the midbrain and is not directly controlled by the cortex. The medial frontal cortex indirectly controls vocalizations, based on the recognition of social context. We examined whether the medial frontal cortex was responsible for antiphonal vocalization, or turn-taking, in naked mole-rats. In normal turn-taking, naked mole-rats vocalize more frequently to dominant individuals than to subordinate ones. Bilateral lesions of the medial frontal cortex disrupted differentiation of call rates to the stimulus animals, which had varied social relationships to the subject. However, medial frontal cortex lesions did not affect either the acoustic properties of the vocalizations or the timing of the vocal exchanges. This suggests that the medial frontal cortex may be involved in social cognition or decision making during turn-taking, while other regions of the brain regulate when animals vocalize and the vocalizations themselves.

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Abbreviations

PAG:

Periaqueductal gray matter

mFC:

Medial frontal cortex

PBS:

Phosphate-buffered saline

DAB:

3.3′-diaminobenzidine

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Acknowledgments

Dr. K. Tanaka and Dr. T. Uekita provided advice on statistical modeling, and Dr. Y. Seki provided advice on experimental procedures. The following individuals were involved in the maintenance of the naked mole-rats and contributed worthwhile suggestions: M. Inada, H. Kagawa, T. Mizota, R. Nakagawa, S. Nambu, C. Suzuki, K. Suzuki, Dr. R. Takahashi, Dr. N. Tokimoto, S. Tokin, I. Tomizawa, and R. Yonemoto. This work was supported by Grant-in-Aid 19-285 from the Japan Society for the Promotion of Science Fellows to SY and by Grant-in-Aids for Scientific Research 13035006 and 23240033 to KO, and by JST-ERATO Okanoya Emotional Information Project. The experiments were approved by the Wako Animal Experiment Committee of the Riken Brain Science Institute (H19-2B109 and H21-2-243).

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Authors and Affiliations

  1. Laboratory for Biolinguistics, Riken Brain Science Institute, 2-1 Hirosawa, Wako, Saitama, 351-0198, Japan

    Shigeto Yosida & Kazuo Okanoya

  2. Graduate School of Science and Technology, Chiba University, 1-33 Yayoi, Inage, Chiba, 263-8522, Japan

    Shigeto Yosida

  3. Japan Society for the Promotion of Science, 6 Ichibanmachi, Chiyoda, Tokyo, 102-8472, Japan

    Shigeto Yosida

  4. ERATO, Okanoya Emotional Information Project, Japan Science and Technology Agency, 4-1-8, Honcho, Kawaguchi, Saitama, 332-0012, Japan

    Kazuo Okanoya

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  1. Shigeto Yosida
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Correspondence to Kazuo Okanoya.

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Yosida, S., Okanoya, K. Bilateral lesions of the medial frontal cortex disrupt recognition of social hierarchy during antiphonal communication in naked mole-rats (Heterocephalus glaber). J Comp Physiol A 198, 109–117 (2012). https://doi.org/10.1007/s00359-011-0692-z

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  • DOI: https://doi.org/10.1007/s00359-011-0692-z

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