REM versus Non-REM sleep disturbance specifically affects inter-specific emotion processing in family dogs (Canis familiaris).
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
26 06 2020
26 06 2020
Historique:
received:
05
02
2020
accepted:
01
06
2020
entrez:
28
6
2020
pubmed:
28
6
2020
medline:
15
12
2020
Statut:
epublish
Résumé
Dogs have outstanding capabilities to read human emotional expressions, both vocal and facial. It has also been shown that positively versus negatively valenced dog-human social interactions substantially affect dogs' subsequent sleep. In the present study, we manipulated dogs' (N = 15, in a within subject design) sleep structure by specifically disrupting REM versus Non-REM sleep, while maintaining equal sleep efficiency (monitored via non-invasive polysomnography). We found that both the number of awakenings as well as relative Non-REM (but not relative REM) duration influenced dogs' viewing patterns in a task where sad and happy human faces were simultaneously projected with sad or happy human voice playbacks. In accordance with the emotion laterality hypothesis, the interaction between sound valence and Non-REM sleep duration was specific to images projected to the left (regardless of image-sound congruency). These results reveal the first evidence of a causal link between sleep structure and inter-specific emotion-processing in the family dog.
Identifiants
pubmed: 32591578
doi: 10.1038/s41598-020-67092-5
pii: 10.1038/s41598-020-67092-5
pmc: PMC7319983
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
10492Références
Beattie, L., Kyle, S. D., Espie, C. A. & Biello, S. M. Social interactions, emotion and sleep: A systematic review and research agenda. Sleep. Med. Rev. 24, 83–100 (2015).
doi: 10.1016/j.smrv.2014.12.005
Benca, R. M. et al. Sleep and mood disorders. Sleep. Med. Rev. 1(1), 45–56 (1997).
doi: 10.1016/S1087-0792(97)90005-8
Van Der Helm, E., Gujar, N. & Walker, M. P. Sleep deprivation impairs the accurate recognition of human emotions. Sleep. 33(3), 335–42 (2010).
doi: 10.1093/sleep/33.3.335
Gujar, N., Yoo, S.-S., Hu, P. & Walker, M. P. Sleep deprivation amplifies reactivity of brain reward networks, biasing the appraisal of positive emotional experiences. J. Neurosci. 31(12), 4466–74 (2011).
doi: 10.1523/JNEUROSCI.3220-10.2011
Pallesen, S. et al. Sleep deprivation and hemispheric asymmetry for facial recognition reaction time and accuracy. Percept. Mot. Skills 98(3_suppl), 1305–14 (2004).
doi: 10.2466/pms.98.3c.1305-1314
Borod, J. C., Koff, E. & Caron, H. S. Right hemispheric specialization for the expression and appreciation of emotion: A focus on the face. In: Cognitive processing in the right hemisphere. Elsevier; p. 83–110 (1983).
Demaree, H. A., Everhart, D. E., Youngstrom, E. A. & Harrison, D. W. Brain lateralization of emotional processing: historical roots and a future incorporating “dominance”. Behav. Cogn. Neurosci. Rev. 4(1), 3–20 (2005).
doi: 10.1177/1534582305276837
Yoo, S.-S., Gujar, N., Hu, P., Jolesz, F. A. & Walker, M. P. The human emotional brain without sleep a prefrontal amygdala disconnect. Curr. Biol. 17(20), R877–R878 (2007).
doi: 10.1016/j.cub.2007.08.007
Franzen, P. L., Buysse, D. J., Dahl, R. E., Thompson, W. & Siegle, G. J. Sleep deprivation alters pupillary reactivity to emotional stimuli in healthy young adults. Biol. Psychol. 80(3), 300–5 (2009).
doi: 10.1016/j.biopsycho.2008.10.010
Sterpenich, V. et al. Sleep-related hippocampo-cortical interplay during emotional memory recollection. PLoS Biol. 5(11), e282 (2007).
doi: 10.1371/journal.pbio.0050282
Walker, M. P. & van der Helm, E. Overnight therapy? The role of sleep in emotional brain processing. Psychol. Bull. 135(5), 731–48 (2009 Sep).
doi: 10.1037/a0016570
Vogel, G. W. A review of REM sleep deprivation. Arch. Gen. Psychiatry 32(6), 749–61 (1975).
doi: 10.1001/archpsyc.1975.01760240077006
Kendall, A. P., Kautz, M. A., Russo, M. B. & Killgore, W. D. S. Effects of sleep deprivation on lateral visual attention. Int. J. Neurosci. 116(10), 1125–38 (2006).
doi: 10.1080/00207450500513922
Hare, B. & Tomasello, M. Human-like social skills in dogs? Trends Cogn. Sci. 9(9), 439–44 (2005).
doi: 10.1016/j.tics.2005.07.003
Parker, H. G., Shearin, A. L. & Ostrander, E. A. Man’s best friend becomes biology’s best in show: genome analyses in the domestic dog. Annu. Rev. Genet. 44, 309–36 (2010).
doi: 10.1146/annurev-genet-102808-115200
Miklósi, Á. & Topál, J. What does it take to become ‘best friends’? Evolutionary changes in canine social competence. Trends Cogn. Sci. 17(6), 287–94 (2013).
doi: 10.1016/j.tics.2013.04.005
Buttelmann, D. & Tomasello, M. Can domestic dogs (Canis familiaris) use referential emotional expressions to locate hidden food? Anim. Cogn. 16(1), 137–45 (2013).
doi: 10.1007/s10071-012-0560-4
Nagasawa, M., Murai, K., Mogi, K. & Kikusui, T. Dogs can discriminate human smiling faces from blank expressions. Anim. Cogn. 14(4), 525–33 (2011).
doi: 10.1007/s10071-011-0386-5
Müller, C. A., Schmitt, K., Barber, A. L. A. & Huber, L. Dogs can discriminate emotional expressions of human faces. Curr. Biol. 25(5), 601–5 (2015).
doi: 10.1016/j.cub.2014.12.055
Guo, K., Meints, K., Hall, C., Hall, S. & Mills, D. Left gaze bias in humans, rhesus monkeys and domestic dogs. Anim. Cogn. 12(3), 409–18 (2009).
doi: 10.1007/s10071-008-0199-3
Quaranta, A., Siniscalchi, M. & Vallortigara, G. Asymmetric tail-wagging responses by dogs to different emotive stimuli. Curr. Biol. 17(6), R199–201 (2007).
doi: 10.1016/j.cub.2007.02.008
Davidson, R. J., Ekman, P., Saron, C. D., Senulis, J. A. & Friesen, W. V. Approach-withdrawal and cerebral asymmetry: emotional expression and brain physiology: I. J. Pers. Soc. Psychol. 58(2), 330 (1990).
doi: 10.1037/0022-3514.58.2.330
Siniscalchi, M., Lusito, R., Vallortigara, G. & Quaranta, A. Seeing left-or right-asymmetric tail wagging produces different emotional responses in dogs. Curr. Biol. 23(22), 2279–82. (2013).
doi: 10.1016/j.cub.2013.09.027
Racca, A., Guo, K., Meints, K. & Mills, D. S. Reading faces: differential lateral gaze bias in processing canine and human facial expressions in dogs and 4-year-old children. PLoS One. 7(4), e36076 (2012).
doi: 10.1371/journal.pone.0036076
Bunford, N., Andics, A., Kis, A., Miklósi, Á. & Gácsi, M. Canis familiaris as a model for non-invasive comparative neuroscience. Trends Neurosci. 40(7), 438–52. (2017).
doi: 10.1016/j.tins.2017.05.003
Bódizs, R, Kis, A., Gácsi, M. & Topál, J. Sleep in the dog: comparative, behavioural and translational relevance. Curr Opin Behav Sci.under revi (2019).
Kis, A. et al. Development of a non-invasive polysomnography technique for dogs (Canis familiaris). Physiol. Behav. 130, 149–56 (2014).
doi: 10.1016/j.physbeh.2014.04.004
Kis, A. et al. Sleep macrostructure is modulated by positive and negative social experience in adult pet dogs. Proc. R. Soc. B Biol. Sci. 284(1865), 20171883 (2017).
doi: 10.1098/rspb.2017.1883
Goldstein, A. N. & Walker, M. P. The role of sleep in emotional brain function. Annu. Rev. Clin. Psychol. 10, 679–708 (2014).
doi: 10.1146/annurev-clinpsy-032813-153716
Agnew, H. W. Jr., Webb, W. B. & Williams, R. L. The first night effect: an Eeg studyof sleep. Psychophysiology. 2(3), 263–6 (1966).
doi: 10.1111/j.1469-8986.1966.tb02650.x
Albuquerque, N. et al. Dogs recognize dog and human emotions. Biol. Lett. 12(1), 20150883 (2016).
doi: 10.1098/rsbl.2015.0883
Takahashi, Y., Ebihara, S., Nakamura, Y., Nishi, C. & Takahashi, K. Circadian sleep and waking patterns in the laboratory dog. Sleep. Res. 1, 144 (1972).
Endo, T. et al. Selective REM sleep deprivation in humans: effects on sleep and sleep EEG. Am. J. Physiol. Integr. Comp. Physiol 274(4), R1186–94 (1998).
doi: 10.1152/ajpregu.1998.274.4.R1186
Langner, O. et al. Presentation and validation of the Radboud Faces Database. Cogn. Emot. 24(8), 1377–88. (2010).
doi: 10.1080/02699930903485076
Anikin, A. & Persson, T. Nonlinguistic vocalizations from online amateur videos for emotion research: A validated corpus. Behav. Res. Methods 49(2), 758–71. (2017).
doi: 10.3758/s13428-016-0736-y
Polimanti O. Piéron, H.-Le Problème Physiologique Du Sommeil. (1913).
Franzen, P. L., Siegle, G. J. & Buysse, D. J. Relationships between affect, vigilance, and sleepiness following sleep deprivation. J. Sleep. Res. 17(1), 34–41 (2008).
doi: 10.1111/j.1365-2869.2008.00635.x
Ehrlichman H. Duality and unity of the brain: Unified functioning and specialization of the hemispheres. (1986)
Andics, A. et al. Neural mechanisms for lexical processing in dogs. Science 353(6303), 1030–2 (2016).
doi: 10.1126/science.aaf3777
Andics, A. Erratum for the report “Neural mechanisms for lexical processing in dogs” by A. Andics, A Gábor, M Gácsi, T Faragó, D Szabó, A Miklósi Sci. 356 (2017).