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Sleep influences cognitive performance in lemurs

  • David R. SamsonEmail author
  • Alexander Vining
  • Charles L. Nunn
Original Paper

Abstract

Primates spend almost half their lives asleep, yet little is known about how sleep influences their waking cognition. We hypothesized that diurnal and cathemeral lemurs differ in their need for consistent, non-segmented sleep for next-day cognitive function—including long-term memory consolidation, self-control, foraging efficiency, and sociality. Specifically, we expected that strictly diurnal Propithecus is more reliant on uninterrupted sleep for cognitive performance, as compared to four other lemur species that are more flexibly active (i.e., cathemeral). We experimentally inhibited sleep and tested next-day performance in 30 individuals of 5 lemur species over 960 total nights at the Duke Lemur Center in Durham, North Carolina. Each set of pair-housed lemurs experienced a sleep restriction and/or deprivation protocol and was subsequently tested in a variety of fitness-relevant cognitive tasks. Within-subject comparisons of performance on these tasks were made by switching the pair from the experimental sleep inhibited condition to a normal sleep environment, thus ensuring cognitive equivalency among individuals. We validated effectiveness of the protocol via actigraphy and infrared videography. Our results suggest that ‘normal’ non-disrupted sleep improved memory consolidation for all lemurs. Additionally, on nights of normal sleep, diurnal lemurs performed better in foraging efficiency tasks than cathemeral lemurs. Social behaviors changed in species-specific ways after exposure to experimental conditions, and self-control was not significantly linked with sleep condition. Based on these findings, the links between sleep, learning, and memory consolidation appear to be evolutionarily conserved in primates.

Keywords

Lemur Activity Sleep Cognition Primate evolution 

Notes

Acknowledgements

We are grateful to the staff at the Duke Lemur Center and offer thanks to Erin Ehmke and David Brewer for continuous support through all aspects of this research. We thank Emilie Melvin, Amanda Lee, Jack Grady, Alex Antezana, James Yu, and Sean Basile for countless volunteer hours. This research was supported by Duke University.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and institutional guidelines for the care and use of animals were followed. All procedures performed in the study involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

Supplementary material

10071_2019_1266_MOESM1_ESM.docx (24 kb)
Supplementary material 1 (DOCX 23 kb)
10071_2019_1266_MOESM2_ESM.jpg (69 kb)
Supplementary material 2 (JPEG 68 kb)

References

  1. Albrecht U (2012) Circadian rhythms and sleep: the metabolic connection. Eur J Physiol 463:23–30CrossRefGoogle Scholar
  2. Ambrosini M, Mariucci G, Colarieti L, Bruschelli G, Carobi C, Giuditta A (1993) The structure of sleep is related to the learning ability of rats. Eur J Neurosci 5:269–275CrossRefGoogle Scholar
  3. Andersen ML, Diaz MP, Murnane KS, Howell LL (2013) Effects of methamphetamine self-administration on actigraphy-based sleep parameters in rhesus monkeys. Psychopharmacology 227:101–107.  https://doi.org/10.1007/s00213-012-2943-2 CrossRefGoogle Scholar
  4. 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 CrossRefGoogle Scholar
  5. Bartoń K (2015) Package ‘MuMIn’: multi-model inference. R package version 1.15.6Google Scholar
  6. Basner M, Rao H, Goel N, Dinges DF (2013) Sleep deprivation and neurobehavioral dynamics. Curr Opin Neurobiol 23:854–863CrossRefGoogle Scholar
  7. Bates D, Maecher M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  8. Beaulieu I, Godbout R (2000) Spatial learning on the Morris Water Maze Test after a short-term paradoxical sleep deprivation in the rat. Brain Cogn 42:27–31Google Scholar
  9. Bonnet M, Arand D (2005) Acute sleep deprivation. In: Kryger M, Roth KT, Dement W (eds) Principles and practices of sleep medicine. Elsevier Saunders, PhiladelphiaGoogle Scholar
  10. 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 Google Scholar
  11. Capellini I, McNamara P, Preston B, Nunn C, Barton R (2009) Does sleep play a role in memory consolidation? A comparative test. PLoS One.  https://doi.org/10.1371/journal.pone.0004609 Google Scholar
  12. Colquhoun IC (2006) Predation and cathemerality: comparing the impact of predators on the activity patterns of lemurids and ceboids. Folia Primatol 77:143–165.  https://doi.org/10.1159/000089701 CrossRefGoogle Scholar
  13. Curtis DJ, Rasmussen MA (2006) The evolution of cathemerality in primates and other mammals: a comparative and chronoecological approach. Folia Primatol 77:178–193.  https://doi.org/10.1159/000089703 CrossRefGoogle Scholar
  14. Curtis DJ, Zaramody A, Martin RD (1999) Cathemerality in the mongoose lemur Eulemur mongoz. Am J Primatol 47:279–298.  https://doi.org/10.1002/(SICI)1098-2345(1999)47:4%3C279::AID-AJP2%3E3.0.CO;2-U CrossRefGoogle Scholar
  15. Datta S (2000) Avoidance task training potentiates phasic pontine-wave density in the rat: a mechanism for sleep-dependent plasticity. J Neurosci 20:8607–8613CrossRefGoogle Scholar
  16. Diamond A (1990) Developmental time course in human infants and infant monkeys and the neural bases of inhibitory control in reaching. Ann N Y Acad Sci 608:637–676CrossRefGoogle Scholar
  17. Donati G, Borgognini-Tarli SM (2006) From darkness to daylight: cathemeral activity in primates. J Anthropol Sci 84:7–32Google Scholar
  18. Donati G, Santini L, Razafindramanana J, Boitani L, Borgognini-Tarli S (2013) (Un-)expected nocturnal activity in “diurnal” lemur catta supports cathemerality as one of the key adaptations of the lemurid radiation. Am J Phys Anthropol 150:99–106CrossRefGoogle Scholar
  19. Durmer JS, Dinges DF (2005) Neurocognitive consequences of sleep deprivation. Semi Neurol 25:117–129.  https://doi.org/10.1055/s-2005-867080 CrossRefGoogle Scholar
  20. Goel N, Rao H, Durmer JS, Dinges DF (2009) Neurocognitive consequences of sleep deprivation. Semin Neurol 29:320–339CrossRefGoogle Scholar
  21. Gruart-Masso A, Nadal-Alemany R, Coll-Andreu M, Portell-Cortès I, Martí-Nicolovius M (1995) Effects of pretraining paradoxical sleep deprivation upon two-way active avoidance. Behav Brain Res 72:181–183CrossRefGoogle Scholar
  22. Halassa MM, Florian C, Fellin T, Munoz JR, Lee SY, Abel T, Frank MG (2009) Astrocytic modulation of sleep homeostasis and cognitive consequences of sleep loss. Neuron 61:213–219CrossRefGoogle Scholar
  23. Hobson JA, Pace-Schott EF (2002) The cognitive neuroscience of sleep: neuronal systems, consciousness and learning. Nat Rev Neurosci 3:679–693CrossRefGoogle Scholar
  24. Kantha SS, Suzuki J (2006) Sleep profile and longevity in three generations of a family of captive Bolivian Aotus. Int J Primatol 27:779–790CrossRefGoogle Scholar
  25. LaFleur M, Sauther M, Cuozzo F, Yamashita N, Youssouf IAJ, Bender R (2014) Cathemerality in wild ring-tailed lemurs (Lemur catta) in the spiny forest of Tsimanampetsotsa National Park: camera trap data and preliminary behavioral observations. Primates 55:207–217CrossRefGoogle Scholar
  26. MacLean EL, Hare B, Nunn CL, Addessi E, Amici F, Anderson RC, Barnard AM (2014) The evolution of self-control. Proc Natl Acad Sci 111:E2140–E2148CrossRefGoogle Scholar
  27. Martin-Ordas G, Call J (2011) Memory processing in great apes: the effect of time and sleep. Biol Lett 7:829–832.  https://doi.org/10.1098/rsbl.2011.0437 CrossRefGoogle Scholar
  28. McNamara P, Auerbach S (2010) Evolutionary medicine of sleep disorders: toward science of sleep duration. In: McNamara P, Barton RA, Nunn CL (eds) Evolution of sleep. Cambridge University Press, Cambridge, pp 107–122Google Scholar
  29. Meldrum RC, Barnes J, Hay C (2015) Sleep deprivation, low self-control, and delinquency: a test of the strength model of self-control. J Youth Adolesc 44:465–477CrossRefGoogle Scholar
  30. Miller NL, Matsangas P, Shattuck LG (2008) Fatigue and its effect on performance in military environments. In: Hancock PA, Szalma JL (eds) Performance under stress. Ashgate Publishing Company, Burlington, pp 235–249Google Scholar
  31. Nair D, Zhang SX, Ramesh V, Hakim F, Kaushal N, Wang Y, Gozal D (2011) Sleep fragmentation induces cognitive deficits via nicotinamide adenine dinucleotide phosphate oxidase-dependent pathways in mouse. Am J Respir Crit Care Med 184:1305–1312CrossRefGoogle Scholar
  32. Nishida M, Pearsall J, Buckner RL, Walker MP (2009) REM sleep, prefrontal theta, and the consolidation of human emotional memory. Cereb Cortex 19:1158–1166.  https://doi.org/10.1093/cercor/bhn155 CrossRefGoogle Scholar
  33. Nunn CL, Samson DR (2018) Sleep in a comparative context: investigating how human sleep differs from sleep in other primates. Am J Phys Anthropol.  https://doi.org/10.1002/ajpa.23427 Google Scholar
  34. Nunn CL, McNamara P, Capellini I, Preston BT, Barton RA (2010) Primate sleep in phylogenetic perspective. In: McNamara P, Barton RA, Nunn CL (eds) Evolution and sleep: phylogenetic and functional perspectives. Cambridge University Press, New York, pp 123–145Google Scholar
  35. Peigneux P, Laureys S, Delbeuck X, Maquet P (2001) Sleeping brain, learning brain. The role of sleep for memory systems. NeuroReport 12:A111–A124CrossRefGoogle Scholar
  36. Perelman P, Johnson WE, Roos C, Seuánez HN, Horvath JE, Moreira MA, Pecon-Slattery J (2011) A molecular phylogeny of living primates. PLoS Genet 7:e1001342.  https://doi.org/10.1371/journal.pgen.1001342 CrossRefGoogle Scholar
  37. Rea MS, Figueiro MG, Jones GE, Glander KE (2014) Daily activity and light exposure levels for five species of lemurs at the Duke Lemur Center. Am J Phys Anthropol 153:68–77CrossRefGoogle Scholar
  38. Rosati AG, Rodriguez K, Hare B (2014) The ecology of spatial memory in four lemur species. Anim Cogn 17:947–961CrossRefGoogle Scholar
  39. Samson DR, Nunn CL (2015) Sleep intensity and the evolution of human cognition. Evol Anthropol 24:225–237CrossRefGoogle Scholar
  40. 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.  https://doi.org/10.1002/ajpa.23455 Google Scholar
  41. Sauther ML, Sussman RW, Gould L (1999) The socioecology of the ringtailed lemur: thirty-five years of research. Evol Anthropol 8:120–132CrossRefGoogle Scholar
  42. Shannon W, Li T, Xian H, Wang J, Deych E, Gonzalez C (2015) Functional actigraphy data analysis. Package ‘Actigraphy’Google Scholar
  43. 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 153:238Google Scholar
  44. Siegel JM (2009) Sleep viewed as a state of adaptive inactivity. Nat Neurosci 10:747–751CrossRefGoogle Scholar
  45. Smith CT, Conway JM, Rose GM (1998) Brief paradoxical sleep deprivation impairs reference, but not working, memory in the radial arm maze task. Neurobiol Learn Mem 69:211–217CrossRefGoogle Scholar
  46. Stone KL, Ancoli-Israel A (2011) Actigraphy. In: Kryger MH, Roth T, William C (eds) Principles and practice of sleep medicine. Elsevier Saunders, St. Louis, pp 1668–1675CrossRefGoogle Scholar
  47. Team RC (2016) R: a language and environment for statistical computing. Team RC, ViennaGoogle Scholar
  48. Vyazovskiy VV, Delogu A (2014) NREM and REM sleep: complementary roles in recovery after wakefulness. Neuroscientist 20:203–219.  https://doi.org/10.1177/1073858413518152 CrossRefGoogle Scholar
  49. Walker MP (2009) The role of sleep in cognition and emotion. Ann N Y Acad 1156:168–197CrossRefGoogle Scholar
  50. Walker MP, Stickgold R (2004) Sleep-dependent learning and memory consolidation. Neuron 44:121–133.  https://doi.org/10.1016/j.neuron.2004.08.031 CrossRefGoogle Scholar
  51. Walker MP, Stickgold R (2006) Sleep, memory, and plasticity. Annu Rev Psychol 57:139–166CrossRefGoogle Scholar
  52. Wang J, Xian H, Licis A, Deych E, Ding J, McLeland J, Shannon W (2011) Measuring the impact of apnea and obesity on circadian activity patterns using functional linear modeling of actigraphy data. J Circadian Rhythm 1:1.  https://doi.org/10.1186/1740-3391-9-11 Google Scholar
  53. Webb WB (1988) Theoretical presentation: an objective behavioral model of sleep. Sleep 11:488–496CrossRefGoogle Scholar
  54. Wright PC (1999) Lemur traits and Madagascar ecology: coping with an island environment. Am J Phys Anthropol 29:31–72CrossRefGoogle Scholar
  55. Xie L, Kang H, Xu Q, Chen MJ, Liao Y, Thiyagarajan M, Iliff JJ (2013) Sleep drives metabolite clearance from the adult brain. Science 342:373–377CrossRefGoogle Scholar
  56. Youngblood BD, Smagin GN, Elkins PD, Ryan DH, Harris RB (1999) The effects of paradoxical sleep deprivation and valine on spatial learning and brain 5-HT metabolism. Physiol Behav 67:643–649CrossRefGoogle Scholar
  57. Zhdanova IV, Geiger DA, Schwagerl AL, Leclair OU, Killiany R, Taylor JA, Madras BK (2002) Melatonin promotes sleep in three species of diurnal nonhuman primates. Physiol Behav 75:523–529CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of AnthropologyUniversity of TorontoMississaugaCanada
  2. 2.Animal Behavior Graduate GroupUniversity of CaliforniaDavisUSA
  3. 3.Duke Global Health InstituteDuke UniversityDurhamUSA
  4. 4.Department of Evolutionary AnthropologyDuke UniversityDurhamUSA

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