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Macaque monkeys show reversed ocular following responses to two-frame-motion stimulus presented with inter-stimulus intervals

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Abstract

When two-frame apparent motion stimuli are presented with an appropriate inter-stimulus interval (ISI), motion is perceived in the direction opposite to the actual image shift. Herein, we measured a simple eye movement, ocular following responses (OFRs), in macaque monkeys to examine the ISI reversal effect on oculomotor. Two-frame movies with an ISI induced reversed OFRs. Without ISI, the OFRs to the two-frame movie were induced in the direction of the stimulus shift. However, with ISIs ≥10 ms, OFRs in the direction opposite to the phase shift were observed. This directional reversal persisted for ISIs up to 160 ms; for longer ISIs virtually no ocular response was observed. Furthermore, longer exposure to the initial image (Motion onset delay: MOD) reduced OFRs. We show that these dependences on ISIs/MODs can be explained by the motion energy model. Furthermore, we examined the dependence on ISI reversal using various spatial frequencies. To account for our findings, the optimal frequency of the temporal filters of the energy model must decrease between 0.5 and 1 cycles/°, suggesting that there are at least two channels with different temporal characteristics. These results are consistent with those from humans, suggesting that the temporal filters embedded in human and macaque visual systems are similar. Thus, the macaque monkey is a good animal model for the early visual processing of humans to understand the neural substrates underlying the visual motion detectors that elicit OFRs.

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Acknowledgements

We are grateful to Dr. N. Kunori for valuable experimental assistance. We thank Ms. A. Muramatsu and Mr. T. Takasu-Mega for technical assistance and Ms. E. Shioya for secretarial assistance. This research was supported by KAKENHI (15K12134, 15K6709, 16H03297, 19K07840, 20K06920) and by the New Energy and Industrial Technology Development Organization (NEDO).

Funding

KAKENHI (15K12134, 15K6709, 16H03297, 19K07804, 20K06920), the New Energy and Industrial, Technology Development Organization (NEDO).

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Authors and Affiliations

  1. Human Informatics and Interaction Research Institute, National Institute of Advanced Industrial Science and Technology, Ibaraki, 305-8568, Japan

    Aya Takemura & Kenji Kawano

  2. Department of Pathology of Mental Diseases, National Institute of Mental health, National Center of Neurology and Psychiatry, Tokyo, 187-8553, Japan

    Junya Matsumoto, Ryota Hashimoto & Kenichiro Miura

  3. Department of Integrative Brain Science, Graduate School of Medicine, Kyoto University, Kyoto, 606-8501, Japan

    Kenji Kawano & Kenichiro Miura

  4. Dokkyo Medical University, Tochigi, 321-0293, Japan

    Kenji Kawano

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  1. Aya Takemura
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Correspondence to Kenichiro Miura.

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Takemura, A., Matsumoto, J., Hashimoto, R. et al. Macaque monkeys show reversed ocular following responses to two-frame-motion stimulus presented with inter-stimulus intervals. J Comput Neurosci 49, 273–282 (2021). https://doi.org/10.1007/s10827-020-00756-3

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