Monocular learning of a spatial task enhances sleep in the right hemisphere of domestic chicks (Gallus gallus)

Abstract

Unihemispheric sleep is an aspect of cerebral lateralization of birds. During sleep, domestic chicks show brief periods during which one eye is open whilst the other remains shut. In this study, time spent in sleeping and in monocular-unihemispheric sleep (Mo-Un sleep) was investigated following the monocular learning of a spatial discrimination task. Two groups of experimental chicks from day 8 to day 11 post-hatching were trained in a spatial paradigm based on geometrical and topographical clues. One group performed the task with left eye open (LE-chicks), whilst another group performed the task with the right eye open (RE-chicks). LE-chick learned the task, whilst RE-chicks were unable to learn. Time spent in binocular sleep and right Mo-Un sleep (right eye closed and left hemisphere sleeping) was equal in both groups of chicks. Time spent in left Mo-Un sleep (left eye closed and right hemisphere sleeping) was significantly higher in LE-chicks than in RE-chicks. Laterality index reveals that LE-chicks had a significant bias towards more left Mo-Un sleep at any recording day, whilst RE-chicks showed a significant bias towards more right Mo-Un sleep at day 8 and 9 but not at days 10 and 11. RE-chick bias at days 8 and 9 could be attributed to a recovery process in left hemisphere connected to its activation/use effect during trials whilst recovery would be absent at days 10 and 11. LE-chicks bias would be associated with the formation of a spatial memory trace and with a recovery process in right hemisphere.

Unihemispheric sleep and asymmetrical sleep: behavioral, neurophysiological, and functional perspectives

“…In domestic chicks, the USWS should be considered a kind of local sleep. 100 , 101 In pigeons, the monocular visual stimulation during BS deprivation elicited an increase of SWS and the slope of slow waves only in the hyperpallium connected with the stimulated eye (visually processing region) during recovery but not in the nonvisual mesopallium. 157 It is suggested that local SWS increase is correlated with local synaptic plastic changes associated with the learning task and with improvement in the task performance after sleep.…”

“…Another group of chicks subjected to a spatial task showed subsequently more right Un-Mo sleep (left eye closure) related to a prevalent engagement of the right hemisphere in the task. 99 – 101 …”

“…Un-Mo sleep prevailed in the hemisphere that dominated during wakefulness, favoring a recovery process and consolidation of memory. 99 – 101 , 107 – 109 Because Un-Mo sleep episodes were intermingled with BSWS ones, the dominant hemisphere spent relatively more time sleeping (BSWS plus Un-Mo sleep) than the nondominant one. Concurrently, for the control of the environment, hen and antipredation chicks awoke the nondominant hemisphere and opened the contralateral eye.…”

Local Aspects of Avian Non-REM and REM Sleep

“…Given that the mallards had one eye open and seemed to use this eye to monitor their environment (see below), such asymmetries were classified as unihemispheric NREM sleep. Based on the relationships between unilateral eye closure and interhemispheric asymmetries in SWA described in EEG studies, eye state alone has been used as an indicator of unihemispheric sleep in several behavioral studies (Ball et al, 1988; Mascetti and Vallortigara, 2001; Boerema et al, 2003; Nelini et al, 2010, 2012; Mascetti, 2016). Finally, the AI thresholds used in dolphins and seals were recently employed to classify NREM sleep as unihemispheric, asymmetric, or symmetric in great frigatebirds ( Fregata minor ) in the wild where eye state could not be monitored (Rattenborg et al, 2016).…”

“…In future studies, it would be interesting to determine whether NREM sleep time or intensity increase unilaterally following sleep deprivation of only one hemisphere while fur seals sleep unihemispherically in the water. Finally, although unihemispheric sleep deprivation has not been performed in birds, several behavioral studies in chicken chicks have shown small, but significant, changes in the time spent with only the left or right eye closed in response to treatments thought to selectively activate one hemisphere or the other (e.g., Mascetti et al, 2007; Nelini et al, 2010, 2012; Quercia et al, 2018; reviewed in Mascetti, 2016), suggesting that sleep may be homeostatically regulated independently in each hemisphere. It will be important for future studies to determine the extent to which these changes in eye state correlate with changes in hemispheric sleep measured electrophysiologically (see Lesku et al, 2011b).…”