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Daily orexinergic modulation of the rat superficial layers of the superior colliculus – implications for intrinsic clock activities in the visual system

View ORCID ProfileLukasz Chrobok, View ORCID ProfileJagoda Stanislawa Jeczmien-Lazur, View ORCID ProfileMonika Bubka, View ORCID ProfileKamil Pradel, Aleksandra Klekocinska, View ORCID ProfileJasmin Daniela Klich, View ORCID ProfileAmalia Ridla Rahim, View ORCID ProfileJihwan Myung, View ORCID ProfileMariusz Kepczynski, View ORCID ProfileMarian Henryk Lewandowski
doi: https://doi.org/10.1101/2021.02.20.432093
Lukasz Chrobok
1Department of Neurophysiology and Chronobiology, Institute of Zoology and Biomedical Research, Jagiellonian University in Krakow, Gronostajowa Street 9, 30-387 Krakow, Poland
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  • ORCID record for Lukasz Chrobok
  • For correspondence: lukasz.chrobok@uj.edu.pl
Jagoda Stanislawa Jeczmien-Lazur
1Department of Neurophysiology and Chronobiology, Institute of Zoology and Biomedical Research, Jagiellonian University in Krakow, Gronostajowa Street 9, 30-387 Krakow, Poland
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Monika Bubka
2Department of Glycoconjugate Biochemistry, Institute of Zoology and Biomedical Research, Jagiellonian University in Krakow, Gronostajowa Street 9, 30-387 Krakow, Poland
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Kamil Pradel
1Department of Neurophysiology and Chronobiology, Institute of Zoology and Biomedical Research, Jagiellonian University in Krakow, Gronostajowa Street 9, 30-387 Krakow, Poland
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Aleksandra Klekocinska
1Department of Neurophysiology and Chronobiology, Institute of Zoology and Biomedical Research, Jagiellonian University in Krakow, Gronostajowa Street 9, 30-387 Krakow, Poland
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Jasmin Daniela Klich
1Department of Neurophysiology and Chronobiology, Institute of Zoology and Biomedical Research, Jagiellonian University in Krakow, Gronostajowa Street 9, 30-387 Krakow, Poland
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Amalia Ridla Rahim
3Graduate Institute of Mind, Brain, and Consciousness, Taipei Medical University, 172-1 Sec. 2 Keelung Road, Da’an District, Taipei 106, Taiwan
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Jihwan Myung
3Graduate Institute of Mind, Brain, and Consciousness, Taipei Medical University, 172-1 Sec. 2 Keelung Road, Da’an District, Taipei 106, Taiwan
4Brain and Consciousness Research Centre, Taipei Medical University-Shuang Ho Hospital, Ministry of Health and Welfare, 291 Zhongzheng Road, Zhonghe District, New Taipei City 235, Taiwan
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Mariusz Kepczynski
5Department of Physical Chemistry and Electrochemistry, Faculty of Chemistry, Jagiellonian University in Krakow, Gronostajowa Street 2, 30-387 Krakow, Poland
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Marian Henryk Lewandowski
1Department of Neurophysiology and Chronobiology, Institute of Zoology and Biomedical Research, Jagiellonian University in Krakow, Gronostajowa Street 9, 30-387 Krakow, Poland
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  • For correspondence: lukasz.chrobok@uj.edu.pl
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Abstract

The orexinergic system delivers excitation for multiple brain centres to facilitate behavioural arousal, with its malfunction resulting in narcolepsy, somnolence, and notably, visual hallucinations. Since the circadian clock underlies the daily arousal, a timed coordination is expected between the orexin system and its target subcortical visual system, including the superior colliculus (SC). Here, we use a combination of electrophysiological, immunohistochemical, and molecular approaches across 24 h, together with the neuronal tract tracing methods in rodents to elucidate the daily coordination between the orexin system and the superficial layers of the SC. We find the daily orexinergic innervation onto the SC, coinciding with the daily silencing of spontaneous firing in this visual brain area. We identify autonomous daily and circadian expression of clock genes in the SC, which may underlie these day-night changes. Additionally, we establish the lateral hypothalamic origin of orexin innervation to the SC and that the SC neurons robustly respond to orexin A via OX2 receptor in both excitatory and GABAA receptor-dependent inhibitory manners. Together, our evidence supports that the clock coordination between the orexinergic input and its response in the SC provides arousal-related excitation needed to detect sparse visual information during the behaviourally active phase.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Funding: This work was financially supported by project grant ‘Sonatina II’ 2018/28/C/NZ4/00099 given to LC from the Polish National Science Centre. The research was carried out using equipment purchased through financial support from the European Regional Development Fund in the framework of the Polish Innovation Economy Operational Program (contract No. POIG.02.01.00-12-023/08). JM was supported by the Taiwan Ministry of Science and Technology (109-2320-B-038-020, 109-2314-B-038-071, 109-2314-B-038-106 -MY3, 108-2321-B-006-023-MY2, 107-2410-H-038-004-MY2), the Higher Education Sprout Project by the Taiwan Ministry of Education (DP2-109-21121-01-N-01), and Taipei Medical University (TMU107-AE1-B15, 107-3805-003-110, 107TMU-SHH-03).

  • Conflict of interest: The authors declare no competing financial interests.

  • Ethics approval: Experiments were approved by the Local (Krakow) Ethical Commission and performed in accordance with the European Community Council Directive of 24 November 1986 (86/0609/ EEC) and the Polish Animal Welfare Act of 23 May 2012 (82/2012) and by the Institutional Animal Care and Use Committee of Taipei Medical University (IACUC Approval No: LAC-2019-0118).

  • Data availability: The data that support the findings of this study are available from the corresponding author upon reasonable request.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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Posted February 20, 2021.
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Daily orexinergic modulation of the rat superficial layers of the superior colliculus – implications for intrinsic clock activities in the visual system
Lukasz Chrobok, Jagoda Stanislawa Jeczmien-Lazur, Monika Bubka, Kamil Pradel, Aleksandra Klekocinska, Jasmin Daniela Klich, Amalia Ridla Rahim, Jihwan Myung, Mariusz Kepczynski, Marian Henryk Lewandowski
bioRxiv 2021.02.20.432093; doi: https://doi.org/10.1101/2021.02.20.432093
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Daily orexinergic modulation of the rat superficial layers of the superior colliculus – implications for intrinsic clock activities in the visual system
Lukasz Chrobok, Jagoda Stanislawa Jeczmien-Lazur, Monika Bubka, Kamil Pradel, Aleksandra Klekocinska, Jasmin Daniela Klich, Amalia Ridla Rahim, Jihwan Myung, Mariusz Kepczynski, Marian Henryk Lewandowski
bioRxiv 2021.02.20.432093; doi: https://doi.org/10.1101/2021.02.20.432093

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