Shining new light on mammalian diving physiology using wearable near-infrared spectroscopy

J. Chris McKnight*, Kimberley A. Bennett, Mathijs Bronkhorst, Debbie J. F. Russell, Steve Balfour, Ryan Milne, Matt Bivins, Simon E. W. Moss, Willy Colier, Ailsa J. Hall, Dave Thompson

*Corresponding author for this work

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    Abstract

    Investigation of marine mammal dive-by-dive blood distribution and oxygenation has been limited by a lack of non-invasive technology for use in freely diving animals. Here, we developed a non-invasive near-infrared spectroscopy (NIRS) device to measure relative changes in blood volume and haemoglobin oxygenation continuously in the blubber and brain of voluntarily diving harbour seals. Our results show that seals routinely exhibit preparatory peripheral vasoconstriction accompanied by increased cerebral blood volume approximately 15 s before submersion. These anticipatory adjustments confirm that blood redistribution in seals is under some degree of cognitive control that precedes the mammalian dive response. Seals also routinely increase cerebral oxygenation at a consistent time during each dive, despite a lack of access to ambient air. We suggest that this frequent and reproducible reoxygenation pattern, without access to ambient air, is underpinned by previously unrecognised changes in cerebral drainage. The ability to track blood volume and oxygenation in different tissues using NIRS will facilitate a more accurate understanding of physiological plasticity in diving animals in an increasingly disturbed and exploited environment.
    Original languageEnglish
    Article numbere3000306
    Number of pages6
    JournalPLoS Biology
    Volume17
    Issue number6
    Early online date18 Jun 2019
    DOIs
    Publication statusPublished - 18 Jun 2019

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    Diving
    Near infrared spectroscopy
    Near-Infrared Spectroscopy
    blood volume
    Physiology
    near-infrared spectroscopy
    seals
    Oxygenation
    Blood
    physiology
    Blood Volume
    Seals
    Phoca
    Air
    blubber
    air
    Phoca vitulina
    vasoconstriction
    blood
    marine mammals

    Cite this

    McKnight, J. C., Bennett, K. A., Bronkhorst, M., Russell, D. J. F., Balfour, S., Milne, R., ... Thompson, D. (2019). Shining new light on mammalian diving physiology using wearable near-infrared spectroscopy. PLoS Biology, 17(6), [e3000306]. https://doi.org/10.1371/journal.pbio.3000306
    McKnight, J. Chris ; Bennett, Kimberley A. ; Bronkhorst, Mathijs ; Russell, Debbie J. F. ; Balfour, Steve ; Milne, Ryan ; Bivins, Matt ; Moss, Simon E. W. ; Colier, Willy ; Hall, Ailsa J. ; Thompson, Dave. / Shining new light on mammalian diving physiology using wearable near-infrared spectroscopy. In: PLoS Biology. 2019 ; Vol. 17, No. 6.
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    title = "Shining new light on mammalian diving physiology using wearable near-infrared spectroscopy",
    abstract = "Investigation of marine mammal dive-by-dive blood distribution and oxygenation has been limited by a lack of non-invasive technology for use in freely diving animals. Here, we developed a non-invasive near-infrared spectroscopy (NIRS) device to measure relative changes in blood volume and haemoglobin oxygenation continuously in the blubber and brain of voluntarily diving harbour seals. Our results show that seals routinely exhibit preparatory peripheral vasoconstriction accompanied by increased cerebral blood volume approximately 15 s before submersion. These anticipatory adjustments confirm that blood redistribution in seals is under some degree of cognitive control that precedes the mammalian dive response. Seals also routinely increase cerebral oxygenation at a consistent time during each dive, despite a lack of access to ambient air. We suggest that this frequent and reproducible reoxygenation pattern, without access to ambient air, is underpinned by previously unrecognised changes in cerebral drainage. The ability to track blood volume and oxygenation in different tissues using NIRS will facilitate a more accurate understanding of physiological plasticity in diving animals in an increasingly disturbed and exploited environment.",
    author = "McKnight, {J. Chris} and Bennett, {Kimberley A.} and Mathijs Bronkhorst and Russell, {Debbie J. F.} and Steve Balfour and Ryan Milne and Matt Bivins and Moss, {Simon E. W.} and Willy Colier and Hall, {Ailsa J.} and Dave Thompson",
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    McKnight, JC, Bennett, KA, Bronkhorst, M, Russell, DJF, Balfour, S, Milne, R, Bivins, M, Moss, SEW, Colier, W, Hall, AJ & Thompson, D 2019, 'Shining new light on mammalian diving physiology using wearable near-infrared spectroscopy', PLoS Biology, vol. 17, no. 6, e3000306. https://doi.org/10.1371/journal.pbio.3000306

    Shining new light on mammalian diving physiology using wearable near-infrared spectroscopy. / McKnight, J. Chris; Bennett, Kimberley A. ; Bronkhorst, Mathijs ; Russell, Debbie J. F.; Balfour, Steve; Milne, Ryan; Bivins, Matt; Moss, Simon E. W.; Colier, Willy; Hall, Ailsa J.; Thompson, Dave.

    In: PLoS Biology, Vol. 17, No. 6, e3000306, 18.06.2019.

    Research output: Contribution to journalArticle

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    AU - Bennett, Kimberley A.

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    AU - Balfour, Steve

    AU - Milne, Ryan

    AU - Bivins, Matt

    AU - Moss, Simon E. W.

    AU - Colier, Willy

    AU - Hall, Ailsa J.

    AU - Thompson, Dave

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    AB - Investigation of marine mammal dive-by-dive blood distribution and oxygenation has been limited by a lack of non-invasive technology for use in freely diving animals. Here, we developed a non-invasive near-infrared spectroscopy (NIRS) device to measure relative changes in blood volume and haemoglobin oxygenation continuously in the blubber and brain of voluntarily diving harbour seals. Our results show that seals routinely exhibit preparatory peripheral vasoconstriction accompanied by increased cerebral blood volume approximately 15 s before submersion. These anticipatory adjustments confirm that blood redistribution in seals is under some degree of cognitive control that precedes the mammalian dive response. Seals also routinely increase cerebral oxygenation at a consistent time during each dive, despite a lack of access to ambient air. We suggest that this frequent and reproducible reoxygenation pattern, without access to ambient air, is underpinned by previously unrecognised changes in cerebral drainage. The ability to track blood volume and oxygenation in different tissues using NIRS will facilitate a more accurate understanding of physiological plasticity in diving animals in an increasingly disturbed and exploited environment.

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