In their discussion of the ensemble of traits that may have shaped cognitive evolution, Coombs and Trestman point out how difficult it is to include several brain features that are nonetheless relevant for higher cognitive capabilities and their evolution. The problematic traits comprise those implicated in the regulation of cerebral states, such as the dopaminergic reward pathway, or neuroendocrine functions. These are hard to circumscribe and neatly define because of the distributed nature of brain circuits and functions. The mechanisms that control sleep stages belong to the same category. Nonetheless, despite the underlying anatomical and physiological complexity, the sleep phases merit to be considered as possible additional traits used to define the cognitively complex animal groups.

After the first observations in humans (Aserinsky & Kleitman, Reference Aserinsky and Kleitman1953), cats (Dement, Reference Dement1958), and other animals (Jouvet, Reference Jouvet1965), mammalian and avian sleep were recognized to comprise two main stages: REM and NREM sleep (Thakkar & Datta, Reference Thakkar, Datta, McNamara, Barton and Nunn2010). NREM sleep is composed of several phases that may differ among species, but always include a deep resting stage, characterized by slow (1–4 Hz) high-amplitude electroencephalographic waves (“delta”), low skeletal muscle tone, and slow, rolling eye movements (Brown et al., Reference Brown, Basheer, McKenna, Strecker and McCarley2012). Such deep NREM phase is often referred to as slow-wave sleep. Conversely, REM sleep is characterized by neocortical activation, with low-amplitude and high-frequency electroencephalographic waves similar to those occurring in wakefulness. The associated rapid eye movements may occur in isolation or in bursts coupled to synchronized field potentials in the pons, lateral geniculate nucleus, and occipital cortex. These ponto-geniculate-occipital waves are thought to determine the most vivid dream experience with visual imagery (Brown et al., Reference Brown, Basheer, McKenna, Strecker and McCarley2012). The classic interpretation is that the brain self-activates to rehearse behaviors typical of the waking stage, whose acting out is prevented by descending inhibition of antigravity muscles. Moreover, REM sleep is accompanied by occasional muscle twitches, which could contribute to refine the spinal cord synaptic circuits (Petersson et al., Reference Petersson, Waldenström, Fåhraeus and Schouenborg2003). Such interpretation of REM sleep remains somewhat controversial (e.g., Blumberg & Plumeau, Reference Blumberg and Plumeau2016; Senzai & Scanziani, Reference Senzai and Scanziani2022). Nonetheless, the tight coordination between activation of sensory and motor pathways during this stage is generally thought to foster sensorimotor integration and maintain the integrity of the circuits implicated in wake behaviors (Hobson, Reference Hobson2009; Blumberg, Dooley, Tiriac, Reference Blumberg, Dooley and Tiriac2022). In fact, abundant evidence in mammals shows that the ascending fiber pathways that sustain REM sleep, especially the cholinergic, exert parallel modulation of sensory (e.g., Gil, Connors, Amitai, Reference Gil, Connors and Amitai1997; Disney, Aoki, Hawken, Reference Disney, Aoki and Hawken2007; Bhattacharyya et al., Reference Bhattacharyya, Bießmann, Veit, Kretz and Rainer2012), motor (e.g., Desai & Walcott, Reference Desai and Walcott2006), and premotor (e.g., Aracri et al., Reference Aracri, Consonni, Morini, Perrella, Rodighiero, Amadeo and Becchetti2010; Aracri et al., Reference Aracri, Amadeo, Pasini, Fascio and Becchetti2013) neocortex regions. REM sleep duration peaks around birth, and is crucially involved in the development of higher cognition and behavior (Hobson, Reference Hobson2009). Conversely, slow-wave sleep is thought to favor metabolic and housekeeping neuronal functions in neurons as well as synaptic homeostasis (Hobson, Reference Hobson2009; Brown et al., Reference Brown, Basheer, McKenna, Strecker and McCarley2012; Rattenborg & Ungurean, Reference Rattenborg and Ungurean2023). In addition, slow-wave sleep appears to favor long-term memory consolidation (Klinzing, Niethard, Born, Reference Klinzing, Niethard and Born2019). Other NREM stages (particularly stage 2, with the characteristic electroencephalographic spindle waves) contribute to these mechanisms in mammals and birds. Because their presence in other animals is uncertain (with the likely exception of Octopus; Pophale et al., Reference Pophale, Shimizu, Mano, Iglesias, Martin, Hiroi, Asada, Andaluz, Van Dinh, Meshulam and Reiter2023), they will not be further discussed.

Recent results show that brain stages analogous to the REM and NREM sleep of mammals and birds are also present in other vertebrates, namely reptiles (Shein-Idelson et al., Reference Shein-Idelson, Ondracek, Liaw, Reiter and Laurent2016; Libourel et al., Reference Libourel, Barrillot, Arthaud, Massot, Morel, Beuf, Herrel and Luppi2018). Analogous evidence is available in the zebrafish Danio rerio (Leung et al., Reference Leung, Wang, Madelaine, Skariah, Kawakami, Deisseroth, Urban and Mourrain2019), but the studies about Amphibia and Pisces are still extremely scarce (Rattenborg & Ungurean, Reference Rattenborg and Ungurean2023). Conversely, in most of the invertebrates studied to date, only one form of sleep is observed. This is often denoted as quiet sleep and presents analogies to slow-wave sleep (Rattenborg & Ungurean, Reference Rattenborg and Ungurean2023). The striking exception is constituted by cephalopods and euarthropods. Studies in cephalopods have revealed both quiet and active forms of sleep, with the latter resembling REM sleep (Iglesias et al., Reference Iglesias, Boal, Frank, Zeil and Hanlon2019; Medeiros et al., Reference Medeiros, Paiva, Lopes, Blanco, Lima, Oliveira, Medeiros, Sequerra, de Souza, Leite and Ribeiro2021; Pophale et al., Reference Pophale, Shimizu, Mano, Iglesias, Martin, Hiroi, Asada, Andaluz, Van Dinh, Meshulam and Reiter2023). Among the arthropods, a REM sleep-like state has been described in jumping spiders (Rößler et al., Reference Rößler, Kim, De Agrò, Jordan, Galizia and Shamble2022), and suggestive evidence has been obtained from honeybees, Drosophila, and crayfish (Rattenborg & Ungurean, Reference Rattenborg and Ungurean2023). These findings are especially intriguing since vertebrates, cephalopods, and euarthropods comprise the cognitively complex lineages as defined by Coombs and Trestman. Hence, the appearance of REM sleep-like stages could mark an essential step in the functional coupling of visual processing and the visuomotor (or sensorimotor, in general) elaboration that is assumed by these authors to be essential for the evolution of higher cognitive faculties.

Do sleep stages satisfy the four key conditions for a good operational definition of cognitively-relevant traits? The universality condition is satisfied, as sleep phases are now recognized throughout the animal kingdom. In some groups, however, sleep architecture may be hard to determine, thus violating the observability condition, especially because of the difficulties of carrying out electrical measurements in minuscule brains. Technological advances, such as the possibility of using optical probes of cell activity (e.g., Leung et al., Reference Leung, Wang, Madelaine, Skariah, Kawakami, Deisseroth, Urban and Mourrain2019), will no doubt solve most of these issues. Regardless, the criterion of inclusivity appears to be respected, as sleep stages are observed in all cognitively complex lineages (Rattenborg & Ungurean, Reference Rattenborg and Ungurean2023), whereas exclusivity seems to apply to REM sleep-like, but not NREM sleep-like stage(s). In fact, the latter state(s) (quiet sleep) appears to be almost universally distributed among animal phyla and is likely related to fundamental metabolic and synaptic homeostasis in the central nervous systems (Dworak et al., Reference Dworak, McCarley, Kim, Kalinchuk and Basheer2010; Brown et al., Reference Brown, Basheer, McKenna, Strecker and McCarley2012; Rattenborg & Ungurean, Reference Rattenborg and Ungurean2023). In conclusion, the resurgence of sleep studies across the animal kingdom in the last ten years fosters the hope that a broader identification and a deeper characterization of sleep stages in different animal groups will be reached in the near future. Such studies would lead to evolutionary-founded insight about some elusive cognitive functions of sleep and their relation with the evolution of higher cognitive abilities.