Abstract
Sleep is a critically important dimension of primate behavior, ecology, and evolution, yet primate sleep is under-studied because current methods of analyzing sleep are expensive, invasive, and time-consuming. In contrast to electroencephalography (EEG) and actigraphy, videography is a cost-effective and non-invasive method to study sleep architecture in animals. With video data, however, it is challenging to score subtle changes that occur in different sleep states, and technology has lagged behind innovations in EEG and actigraphy. Here, we applied Eulerian videography to magnify pixels relevant to scoring sleep from video, and then compared these results to analyses based on actigraphy and standard infrared videography. We studied four species of lemurs (Eulemur coronatus, Lemur catta, Propithecus coquereli, Varecia rubra) for 12-h periods per night, resulting in 6480 1-min epochs for analysis. Cramer’s V correlation between actigraphy-classified sleep and infrared videography-classified sleep revealed consistent results in eight of the nine 12-h videos scored. A sample of the infrared videography was then processed by Eulerian videography for movement magnification and re-coded. A second Cramer’s V correlation analysis, between two independent scorers coding the same Eulerian-processed video, found that interobserver agreement among Eulerian videography increased sleep vs. awake, NREM, and REM classifications by 7.1%, 46.7%, and 34.3%, respectively. Furthermore, Eulerian videography was more strongly correlated with actigraphy data when compared to results from standard infrared videography. The increase in agreement between the two scorers indicates that Eulerian videography has the potential to improve the identification of sleep states in lemurs and other primates, and thus to expand our understanding of sleep architecture without the need for EEG.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ancoli-Israel S, Cole R, Alessi C, Chambers M, Moorcroft W, Pollak CP (2003) The role of actigraphy in the study of sleep and circadian rhythms. Sleep 26:342–392. https://doi.org/10.1093/sleep/26.3.342
Andersen ML, Diaz MP, Murnane KS, Howell LL (2013) Effects of methamphetamine self-administration on actigraphy-based sleep parameters in rhesus monkeys. Psychopharmacology (Berl) 227:101–107. https://doi.org/10.1007/s00213-012-2943-2
Anderson JR (1998) Sleep, sleeping sites, and sleep-related activities: awakening to their significance. Am J Primatol 46:63–75. https://doi.org/10.1002/(SICI)1098-2345(1998)46:1%3c63:AID-AJP5%3e3.0.CO;2-T
Anderson JR (2000) Sleep-related behavioural adaptations in free-ranging anthropoid primates. Sleep Med Rev 4:355–373. https://doi.org/10.1053/smrv.2000.0105
Balakrishnan G, Durand F, Guttag J (2013) Detecting pulse from head motions in video. Proc IEEE Conf Comput Vis Pattern Recognit. https://doi.org/10.1109/CVPR.2013.440
Balzamo E, Bradley RJ, Rhodes JM (1972) Sleep ontogeny in the chimpanzee: from two months to forty-one months. Electroencephalogr Clin Neurophysiol 33:47–60. https://doi.org/10.1016/0013-4694(72)90024-7
Balzamo E, Van Beers P, Lagarde D (1998) Scoring of sleep and wakefulness by behavioral analysis from video recordings in rhesus monkeys: comparison with conventional EEG analysis. Electroencephalogr Clin Neurophysiol 106:206–212. https://doi.org/10.1016/s0013-4694(97)00152-1
Barrett CE, Noble P, Hanson E, Pine DS, Winslow JT, Nelson EE (2009) Early adverse rearing experiences alter sleep-wake patterns and plasma cortisol levels in juvenile rhesus monkeys. Psychoneuroendocrinology 34:1029–1040. https://doi.org/10.1016/j.psyneuen.2009.02.002
Bray J, Samson DR, Nunn CL (2017) Activity patterns in seven captive lemur species: evidence of cathemerality in Varecia and Lemur catta? Am J Primatol. https://doi.org/10.1002/ajp.22648
Campbell SS, Tobler I (1984) Animal sleep: a review of sleep duration across phylogeny. Neurosci Biobehav Rev 8:269–300. https://doi.org/10.1016/0149-7634(84)90054-X
Cruz-Aguilar MA, Ayala-Guerrero F, Jiménez-Anguiano A, Santillán-Doherty AM, García-Orduña F, Velázquez-Moctezuma J (2015) Sleep in the spider monkey (Ateles geoffroyi): a semi-restrictive, non-invasive, polysomnographic study. Am J Primatol 77:200–210. https://doi.org/10.1002/ajp.22322
Davis A, Rubinstein M, Wadhwa N, Mysore GJ, Durand F, Freeman WT (2014) The visual microphone: passive recovery of sound from video. ACM Trans Graphics 33:1–79. https://doi.org/10.1145/2601097.2601119
Deng F, Dong J, Wang X, Fang Y, Liu Y, Yu Z, Liu J, Chen F (2018) Design and implementation of a noncontact sleep monitoring system using infrared cameras and motion sensor. IEEE Trans Instrum Meas 67:1555–1563. https://doi.org/10.1109/TIM.2017.2779358
Durmer JS, Dinges DF (2005) Neurocognitive consequences of sleep deprivation. Semin Neurol 25:117–129. https://doi.org/10.1055/s-2005-867080
Estrada A, Garber PA, Rylands AB, Roos C, Fernandez-Duque E, Di Fiore A, Nekaris KA, Nijman V, Heymann EW, Lambert JE, Rovero F, Barelli C, Setchell JM, Gillespie TR, Mittermeier RA, Arregoitia LV, de Guinea M, Gouveia S, Dobrovolski R, Shanee S, Shanee N, Boyle SA, Fuentes A, MacKinnon KC, Amato KR, Meyer ALS, Wich S, Sussman RW, Pan R, Kone I, Li B (2017) Impending extinction crisis of the world’s primates: why primates matter. Sci Adv 3:e1600946. https://doi.org/10.1126/sciadv.1600946
Field A (2013) Discovering Statistics Using IBM SPSS Statistics. Sage Publications Ltd
Freemon FR, McNew JJ, Adey WR (1969) Sleep of unrestrained chimpanzee: cortical and subcortical recordings. Exp Neurol 25:129–137. https://doi.org/10.1016/0014-4886(69)90076-4
Johnson NL, Kirchner HL, Rosen CL, Storfer-Isser A, Cartar LN, Ancoli-Israel S, Emancipator JL, Kibler AM, Redline S (2007) Sleep estimation using wrist actigraphy in adolescents with and without sleep disordered breathing: a comparison of three data modes. Sleep 30:899–905. https://doi.org/10.1093/sleep/30.7.899
Kantha SS, Suzuki J (2006a) Sleep profile and longevity in three generations of a family of captive Bolivian Aotus. Int J Primatol 27:779–790
Kantha SS, Suzuki J (2006b) Sleep quantitation in common marmoset, cotton top tamarin and squirrel monkey by non-invasive actigraphy. Comp Biochem Physiol Mol Integr Physiol 144:203–210. https://doi.org/10.1016/j.cbpa.2006.02.043
Kripke DF, Bert J (1968) Techniques for telemetry of chimpanzee sleep electroencephalogram. J Appl Physiol 25:461–462
Kripke DF, Reite ML, Pegram GV, Stephens LM, Lewis OF (1968) Nocturnal sleep in rhesus monkeys. Electroencephalogr Clin Neurophysiol 24:581–586. https://doi.org/10.1016/0013-4694(68)90047-3
Martin-Ordas G, Call J (2011) Memory processing in great apes: the effect of time and sleep. Biol Lett 7:829–832
McCoy JG, Strecker RE (2011) The cognitive cost of sleep lost. Neurobiol Learn Mem 96:564–582. https://doi.org/10.1016/j.nlm.2011.07.004
McNamara P, Capellini I, Harris E, Nunn CL, Barton RA, Preston B (2008) The phylogeny of sleep database: a new resource for sleep scientists. Open Sleep J 1:11–14. https://doi.org/10.2174/1874620900801010011
McNew JJ, Howe RC, Adey WR (1971) The sleep cycle and subcortical-cortical EEG relations to the unrestrained chimpanzee. Electroencephalogr Clin Neurophysiol 30:489–503. https://doi.org/10.1016/0013-4694(71)90146-5
McNew JJ, Burson RC, Hoshizaki T, Adey WR (1972) Sleep-wake cycle of an unrestrained isolated chimpanzee under entrained and free running conditions. Aerosp Med 43:155–161
Mizuno Y, Takeshita H, Matsuzawa T (2006) Behavior of infant chimpanzees during the night in the first 4 months of life: smiling and suckling in relation to behavioral state. Infancy 9:221–240
Morimura N, Fujisawa M, Mori Y, Teramoto M (2012) Environmental influences on sleep behavior in captive male chimpanzees (Pan troglodytes). Int J Primatol 33:822–829
Muñoz-Delgado J, Luna-Villegas G, Mondragón-CeballoS R, Fernández-Guardiola A (1995) Behavioral characterization of sleep in stumptail macaques (Macaca arctoides) in exterior captivity by means of high-sensitivity videorecording. Am J Primatol 36(3):245–249
Nunn CL, Samson DR (2018) Sleep in a comparative context: investigating how human sleep differs from sleep in other primates. Am J Phys Anthropol 166:601–612. https://doi.org/10.1002/ajpa.23427
Nunn CL, McNamara P, Capellini I, Preston P, Barton RA (2010) Primate sleep in phylogenetic perspective. In: McNamara P, Barton RA, Nunn CL (eds) Evolution of sleep: phylogenetic and functional perspectives. Cambridge University Press, New York, pp 123–144
Samson DR, Nunn CL (2015) Sleep intensity and the evolution of human cognition. Evol Anthropol 24:225–237
Samson DR, Shumaker RW (2013) Documenting orang-utan sleep architecture: sleeping platform complexity increases sleep quality in captive Pongo. Behaviour 150:845–861
Samson D, Bray J, Nunn C (2015) Cathemerality and sleep intensity in seven captive lemur species. Am J Phys Anthropol 156:275
Samson D, Yetish G, Crittenden A, Mabulla I, Mabulla A, Nunn C (2016) What is segmented sleep? Actigraphy field validation for daytime sleep and nighttime wake. Sleep Health. https://doi.org/10.1016/j.sleh.2016.09.006
Samson DR, Bray J, Nunn CL (2018) The cost of deep sleep: environmental influences on sleep regulation are greater for diurnal lemurs. Am J Phys Anthropol 166:578–589. https://doi.org/10.1002/ajpa.23455
Samson DR, Vining A, Nunn CL (2019) Sleep influences cognitive performance in lemurs. Anim Cogn. https://doi.org/10.1007/s10071-019-01266-1
Shumaker RW, Samson DR, Schoenemann TP (2014) The effects of sleeping platforms on next day cognition in captive orangutans (Pongo spp). Am J Phys Anthropol 153:238
Stone KL, Ancoli-Israel S (2017) Actigraphy. In: Kryger M, Roth T, Dement W (eds) Principles and practice of sleep medicine, 6th edn. Elsevier, Philadelphia, pp 1671–1678
Team RC (2013) R: a language and environment for statistical computing
Van Hillegondsberg L, Carr J, Brey N, Henning F (2017) Using Eulerian video magnification to enhance detection of fasciculations in people with amyotrophic lateral sclerosis. Muscle Nerve 56:1063–1067. https://doi.org/10.1002/mus.25690
Videan EN (2006) Bed-building in captive chimpanzees (Pan troglodytes): the importance of early rearing. Am J Primatol 68:745–751. https://doi.org/10.1002/ajp.20265
Weitzman ED, Kripke DF, Pollak C, Dominguez J (1965) Cyclic activity in sleep of Macaca mulatta. Arch Neurol 12:463–467. https://doi.org/10.1001/archneur.1965.00460290019003
Wu H, Rubinstein M, Shih E, Guttag J, Durand F, Freeman W (2012) Eulerian video magnification for revealing subtle changes in the world. ACM Trans Graphics 31:1–8. https://doi.org/10.1145/2185520.2185561
Zhdanova IV, Geiger DA, Schwagerl AL, Leclair OU, Killiany R, Taylor JA, Rosene DL, Moss MB, Madras BK (2002) Melatonin promotes sleep in three species of diurnal nonhuman primates. Physiol Behav 75:523–529. https://doi.org/10.1016/s0031-9384(02)00654-6
Acknowledgements
We thank Alexander Vining for his work in processing and preparing the Eulerian videography segment, and the entire Duke Lemur Center staff, especially Erin Ehmke and David Brewer, for their support and assistance. We also thank the editor and three anonymous reviewers for their helpful comments on an earlier version of this manuscript. EM thanks Leslie Digby for her mentorship and review of drafts of this work, and CN thanks Michael Platt for suggesting Eulerian video magnification as a means to score primate sleep. This research was supported by Duke University. This research complied with animal care regulations and applicable national laws for the collection of ethical primate research.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Melvin, E., Samson, D. & Nunn, C.L. Eulerian videography technology improves classification of sleep architecture in primates. Primates 60, 467–475 (2019). https://doi.org/10.1007/s10329-019-00744-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10329-019-00744-x