- Email: [email protected]
Social Learning: Peering Deeper into Ape Culture
Current Biology
Dispatches Social Learning: Peering Deeper into Ape Culture Andrew Whiten Centre for Social Learning and Cognitive Evolution, School of Psychology and Neuroscience, University of St Andrews, St Andrews, KY16 9JP, UK Correspondence: [email protected] https://doi.org/10.1016/j.cub.2019.07.003
The cultural repertoires of apes have been charted by identifying cultural differences between populations. A new approach focused on great apes’ intense ‘peering’ during social learning suggests that they may possess many more cultural elements than currently thought. A veritable deluge of studies has documented the cultural transmission of information from individual to individual across a range of vertebrate and invertebrate species [1]. Some of the earliest roots of this current research bonanza were in primatology, first in the famous mid-twentieth-century discovery of the spread of sweet-potato washing and other traditions among Japanese macaques [2], and later in field studies of the great apes [2]. Just a few years after her first reports of tool use in wild chimpanzees, Jane Goodall boldly wrote of ‘cultural elements in a chimpanzee community’ [3], fuelled both by observations of juveniles’ attention avidly focused on the technical skills of their elders (Figure 1) and early indications that chimpanzees behaved in different ways across African study sites, in ways not apparently explicable by ecological factors. By 1999, it was possible to document these differences in a systematic survey across research sites, revealing an unprecedent array of 39 such putative cultural variations in wild chimpanzees [4]. This discovery was soon followed by reports of similar arrays of 19–24 cultural variants in orangutans [5] and more recently by a further convergent report of 22 such putative traditions in gorillas [6]. The impressive scope of great ape cultures inferred by these studies was undreamt of half a century ago, as illustrated in a statement by Peter Medawar that ‘‘human beings owe their biological supremacy to the possession of a form of inheritance quite unlike that of other animals: . the apparatus of culture’’ [7]. Nevertheless, in a new study Caroline Schuppli and Carel van Schaik [8] now suggest that the scope of ape culture has been radically underestimated
by the focus on behavioural differences between communities. They advocate a new methodological approach that additionally accommodates cultural adaptations to local ecological contexts, and even cultural universals. Schuppli and van Schaik [8] concentrate on avid visual attention (Figure 1), labelling it ‘peering’. In an earlier paper that constitutes a crucial foundation for the present one, Schuppli and colleagues [9] systematically tested the validity of peering as an index of observational learning in young wild orangutans. This is important because peering itself need not necessarily implicate learning: for example, it might instead reflect intent to scrounge food items [10]. Young wild capuchins have been shown to preferentially watch the best adult nutcrackers [11], but this benefits their scrounging as well as any potential for observational learning. Accordingly, Schuppli and colleagues [9] applied multiple tests of the hypothesis that young orangutans’ peering serves primarily a learning function. All yielded confirmatory evidence. For example, in different contexts, such as stick-tool use and nest building, episodes of peering were followed by heightened rates of exploration of the items concerned. The frequency of peering was predicted by the complexity and difficulty of the procedures peered at and rose along with the learning of new skills and diminished as competence was manifested. Having assured themselves of the validity of peering as in index of social learning, the authors went on in the new paper [8] to document all the contexts in which peering occurs in the everyday lives of juvenile orangutans at two field sites, Suaq in Sumatra and Tuanan in Borneo. From these records the authors estimate
that over the course of their development, orangutans may engage in as many as 38,000 episodes of peering. Peering occurred in as many as 124–195 different contexts across the two sites, spanning a diverse range of activities including tool use, foraging choices and nest building. As the authors remark, these figures vastly exceed the fewer than 30 cultural variants earlier documented at these sites through the ‘traditional’ approach [12]. Thus, they conclude, ‘‘when looking closely at great ape skill acquisition, it seems that immatures learn virtually all of their skills socially’’ [8]. In 1976 Dawkins [13] proposed a cultural analogy of the gene — the meme — conceptualized as a ‘‘unit of cultural transmission’’ [13]. The term has since been assimilated into everyday discourse. Memes were suggested to
Figure 1. ‘Peering’ in chimpanzees. A young chimpanzee watches intently as its mother uses a stone hammer to crack a nut, at Bossou in West Africa. Schuppli and van Schaik have labelled such avid attention ‘peering’ and used this behaviour to index the extensive scope of all that juvenile apes appear to learn from the accumulated cultural knowledge of their community (photo: T. Matsuzawa and Primate Research Institute, Kyoto University).
Current Biology 29, R829–R850, September 9, 2019 ª 2019 Elsevier Ltd. R845
Current Biology
Dispatches
Figure 2. A ‘cultural iceberg’ of socially transmitted behaviour in apes. Schuppli and van Schaik [8] suggest that the most prevalent approach to identifying great ape cultural traditions by describing regional variations may so far have recognised only the tip of a ‘cultural iceberg’, the greater part of which has remained uncharted. The tip represents often complex and highly visible behaviours, here illustrated by chimpanzee nut-cracking, which occurs only in West Africa despite the widespread distribution of similar materials [1]. Schuppli and van Schaik [8] offer a new way to identify a second layer they suggest may contain scores of other traditions adapted to local ecologies, here illustrated by subterranean termite fishing by chimpanzees using a multi-tool-kit [1] and breaking twigs to suck out ants by orangutans [9,12]. Finally, a basal layer contains many culturally universal behaviours, here illustrated by chimpanzee leaf-sponging to drink water, and dietary preferences in orangutans [8,17] and gorillas [16].
include human catch-phrases and ways of making pots, but in principle any culture should be decomposable into a vast list of its constituent memes. Is this what we now have in Schuppli and van Schaik’s list of elements for the two orangutan sites? These appear to be offered as putative ‘units of cultural transmission’, picked out by the peering focused on them by juveniles. The difficulty here, and indeed in all attempts to describe a community’s cultural repertoire in terms of a discrete number of cultural units or elements, lies in what is to count as a unit. In humans, is Catholicism a meme, or is it constituted of numerous memes at lower levels, like angels, altars and prayers? Likewise, in orangutans, is using a tool to poke seeds out of a fruit a meme, or are constituent
parts like holding the tool in one’s mouth the memes? This fundamental question of ‘unit granularity’ is not explicitly addressed by the authors. Dawkins suggested that a gene be defined as any bit of DNA that ‘‘lasts for enough generations to serve as a unit of selection’’ [13]. This criterion can be directly applied to what is to count as a meme, transmitted across multiple cultural generations. Whether the elements defined by Schuppli and van Schaik [8] elements are indeed units of (cultural) selection is a challenge yet to be addressed. Some exciting beginnings have been made in identifying the operation of selection and cultural evolution in non-human species more generally, for example in birdsong [14].
R846 Current Biology 29, R829–R850, September 9, 2019
Schuppli and van Schaik [8] interpret their results through the analogy of an iceberg, representing the scope of ape culture (Figure 2). So far, they argue, we have glimpsed only its tip visible above the surface, which is made up of the most noticeable elements documented by the earlier cross-cultural studies, such as forms of tool use. Beneath these is a large set of behaviour patterns missed by the cross-cultural approaches because of their reliance on excluding elements explicable by local ecological circumstances. This weakness of the cross-cultural approach [4–6] was recognized by its proponents, seeing it as a first, broad-brush attempt to start to grasp the extent and scope of ape culture. The new study of Schuppli and van Schaik [8] is the first to provide an evidence-based means of delineating a much broader range of cultural adaptions to an ape community’s environment. The base layer of the pyramid includes behaviours that may even be universal in the species, yet still culturally acquired (‘knife use’ might be an equivalent in our own species, for example). These middle and lower parts of the iceberg include many basic and simple behavioural elements, such as selective food choice. It is far from implausible that cultural inheritance is important at this level, given the large size of apes’ dietary repertoire and the vastly greater array of potential items never ingested. Over 200–300 different items (varied parts of numerous species, including fruits, seeds, leaves, stems, pith, flowers, bark, and roots, not to mention vertebrate and invertebrate prey) may be eaten by chimpanzees [15], gorillas [16] and orangutans [17], including a highly selective sub-set of all the potential parts of the many hundreds of species that make up tropical forests. This means there may be well over 1,000 options that could in principle be explored individually, so the value of peering at and learning from the accumulated wisdom underlying the skills and choices of one’s mother, and later others, could indeed be very significant. Field experiments, so far conducted only with other primate species, confirm that infants’ diet selection can be highly dependent on the choices of their mother and her community [18].
Current Biology
Dispatches Orangutan cultures and the evolution of material culture. Science 299, 102–105.
In the new ‘peering’ based study of Schuppli and van Schaik [8], and the challenge of its conclusions, we may be seeing a significant leap in our efforts to capture the true scope of ape culture. The underlying approach may significantly extend the methods applied to study social learning research in the future, in a variety of species other than apes.
6. Robbins, M.M., Ando, C., Fawcett, K.A., Gruiter, C.C., Hedwig, D., Iwata, Y., Lodwick, J.L., Masi, S., Salmi, R., Stoinski, T.S., et al. (2016). Behavioural variation in gorillas: evidence of potential cultural traits. PLoS One 11, e0160483.
REFERENCES
8. Schuppli, C., and van Schaik, C.P. (2019). Animal cultures: how we’ve only seen the tip of the iceberg. Evol. Hum. Sci. 1, e2.
1. Whiten, A. (2017). A second inheritance system: the extension of biology through culture. Interf. Focus 7, 20160142. 2. McGrew, W.C. (1992). Chimpanzee Material Culture: Implications for Human Evolution (Cambridge: Cambridge University Press).
7. Medawar, P. (1977). Unnatural science. The New York Review of Books, Feb. 3rd, 13–18.
9. Schuppli, C., Meulman, E.J.M., Forss, S.I.M., Aprilinayati, F., van Noordwijk, M.A., and van Schaik, C.P. (2016). Observational learning and socially induced practice of routine skills in immature orangutans. Anim. Behav. 119, 87–98.
3. van Lawick-Goodall, J. (1973). Cultural elements in a chimpanzee community. In Precultural Primate Behaviour, E. Menzel, ed. (Basel: Karger), pp. 144–184.
10. Corp, N., and Byrne, R.W. (2002). The ontogeny of manual skill in wild chimpanzees: evidence from feeding on the fruit of Saba florida. Behav. 139, 137–168.
4. Whiten, A., Goodall, J., McGrew, W.C., Nishida, T., Reynolds, V., Sugiyama, Y., Tutin, C.E.G., Wrangham, R.W., and Boesch, C. (1999). Cultures in chimpanzees. Nature 399, 682–685.
11. Ottoni, E.B., de Resende, B.D., and Izar, P. (2005). Watching the best nutcrackers: what capuchin monkeys (Cebus apella) know about others’ tool-using skills. Anim. Cogn. 8, 215–219.
5. van Schaik, C.P., Ancrenaz, M., Borgen, G., Galdikas, B., Knott, C.D., Singleton, I., Suzuki, A., Utami, S.S., and Merrill, M. (2003).
12. van Schaik, C.P., Ancrenaz, M., Djojoasmoro, R., Knott, C.D., Morrogh-Bernard, H.C., Nuzuar, K.O., Atmoko, S.S.U., and
van Noordwijk, M.A. (2009). Orangutan cultures re-visited. In Orangutans: Geographic Variation in Behavioral Ecology and Conservation, S.A. Wich, S.S.U. Atmoko, T.M. Setia, and C.P. van Schaik, eds. (Oxford: Oxford University Press), pp. 299–309. 13. Dawkins, R. (1976). The Selfish Gene (Oxford: Oxford University Press). 14. Aplin, L.M. (2019). Culture and cultural evolution in birds: a review of the evidence. Anim. Behav. 147, 179–187. 15. Inskipp, T. (2005). Chimpanzee (Pan troglodytes). In World Atlas of Great Apes and Their Conservation, J. Caldecott, and L. Miles, eds. (Berkeley: Univ California Press), pp. 53–81. 16. Ferriss, S. (2005). Western gorilla (Gorilla gorilla). In World Atlas of Great Apes and Their Conservation, J. Caldecott, and L. Miles, eds. (Berkeley: Univ California Press), pp. 105–127. 17. McConkey, K. (2005). Bornean orangutan (Pongo pygmaeus). In World Atlas of Great Apes and Their Conservation, J. Caldecott, and L. Miles, eds. (Berkeley: Univ California Press), pp. 161–183. 18. van de Waal, E., Borgeaud, C., and Whiten, A. (2013). Potent social learning and conformity shape a wild primate’s foraging decisions. Science 340, 483–485.
Glia: A Gate Controlling Animal Behavior? Claire Wyart1,* and Andrew Prendergast1,2
pinie`re (ICM), Spinal Sensory Signaling team, Sorbonne Universite , 47 bld hoˆpital, Paris 75013, France du Cerveau et de la Moelle e of Cardiovascular Medicine, Yale University, New Haven, CT 06511, USA *Correspondence: [email protected] https://doi.org/10.1016/j.cub.2019.07.058 1Institut
2Department
Although glia are known to have the potential to alter neuronal activity, their behavioral relevance is not well understood. A recent study has discovered that, when zebrafish give up on performing a visuo-motor task, glia integrate information from neuromodulatory neurons to stop motor output. The word ‘glia’ is derived from the ancient Greek word glia for glue, as glial cells were initially discovered in the search for connective tissue in the brain [1]. Glia are non-neuronal cells of the nervous system and the term covers astrocytes, oligodendrocytes, oligodendrocyte progenitor cells, ependymal cells, radial glial cells and microglial cells (the macrophages of the CNS which enter from the periphery). There are at least as many, if not more,
glial cells than neurons in the brain, yet their importance has long been underappreciated, glia being overshadowed by their glamorous, more electrically-excitable neighbours. Modern neuroscience has, however, revealed a diversity of crucial functions for glia, which intimately communicate with neurons to ensure the development, maintenance, and function of the brain. For example, oligodendrocytes build the myelin sheaths that surround axons of
specific neurons to modulate conduction properties, and can do so in an activitydependent manner [2]. Oligodendrocyte progenitor cells are excitable cells [3]. Microglia shape the migration of inhibitory neurons in the brain during development [4], thereby influencing the critical excitation–inhibition balance in the cortex, and have also been implicated in synaptic pruning during the refinement period of neural circuit formation. Astrocytes contribute to many
Current Biology 29, R829–R850, September 9, 2019 ª 2019 Elsevier Ltd. R847
Dispatches Social Learning: Peering Deeper into Ape Culture Andrew Whiten Centre for Social Learning and Cognitive Evolution, School of Psychology and Neuroscience, University of St Andrews, St Andrews, KY16 9JP, UK Correspondence: [email protected] https://doi.org/10.1016/j.cub.2019.07.003
The cultural repertoires of apes have been charted by identifying cultural differences between populations. A new approach focused on great apes’ intense ‘peering’ during social learning suggests that they may possess many more cultural elements than currently thought. A veritable deluge of studies has documented the cultural transmission of information from individual to individual across a range of vertebrate and invertebrate species [1]. Some of the earliest roots of this current research bonanza were in primatology, first in the famous mid-twentieth-century discovery of the spread of sweet-potato washing and other traditions among Japanese macaques [2], and later in field studies of the great apes [2]. Just a few years after her first reports of tool use in wild chimpanzees, Jane Goodall boldly wrote of ‘cultural elements in a chimpanzee community’ [3], fuelled both by observations of juveniles’ attention avidly focused on the technical skills of their elders (Figure 1) and early indications that chimpanzees behaved in different ways across African study sites, in ways not apparently explicable by ecological factors. By 1999, it was possible to document these differences in a systematic survey across research sites, revealing an unprecedent array of 39 such putative cultural variations in wild chimpanzees [4]. This discovery was soon followed by reports of similar arrays of 19–24 cultural variants in orangutans [5] and more recently by a further convergent report of 22 such putative traditions in gorillas [6]. The impressive scope of great ape cultures inferred by these studies was undreamt of half a century ago, as illustrated in a statement by Peter Medawar that ‘‘human beings owe their biological supremacy to the possession of a form of inheritance quite unlike that of other animals: . the apparatus of culture’’ [7]. Nevertheless, in a new study Caroline Schuppli and Carel van Schaik [8] now suggest that the scope of ape culture has been radically underestimated
by the focus on behavioural differences between communities. They advocate a new methodological approach that additionally accommodates cultural adaptations to local ecological contexts, and even cultural universals. Schuppli and van Schaik [8] concentrate on avid visual attention (Figure 1), labelling it ‘peering’. In an earlier paper that constitutes a crucial foundation for the present one, Schuppli and colleagues [9] systematically tested the validity of peering as an index of observational learning in young wild orangutans. This is important because peering itself need not necessarily implicate learning: for example, it might instead reflect intent to scrounge food items [10]. Young wild capuchins have been shown to preferentially watch the best adult nutcrackers [11], but this benefits their scrounging as well as any potential for observational learning. Accordingly, Schuppli and colleagues [9] applied multiple tests of the hypothesis that young orangutans’ peering serves primarily a learning function. All yielded confirmatory evidence. For example, in different contexts, such as stick-tool use and nest building, episodes of peering were followed by heightened rates of exploration of the items concerned. The frequency of peering was predicted by the complexity and difficulty of the procedures peered at and rose along with the learning of new skills and diminished as competence was manifested. Having assured themselves of the validity of peering as in index of social learning, the authors went on in the new paper [8] to document all the contexts in which peering occurs in the everyday lives of juvenile orangutans at two field sites, Suaq in Sumatra and Tuanan in Borneo. From these records the authors estimate
that over the course of their development, orangutans may engage in as many as 38,000 episodes of peering. Peering occurred in as many as 124–195 different contexts across the two sites, spanning a diverse range of activities including tool use, foraging choices and nest building. As the authors remark, these figures vastly exceed the fewer than 30 cultural variants earlier documented at these sites through the ‘traditional’ approach [12]. Thus, they conclude, ‘‘when looking closely at great ape skill acquisition, it seems that immatures learn virtually all of their skills socially’’ [8]. In 1976 Dawkins [13] proposed a cultural analogy of the gene — the meme — conceptualized as a ‘‘unit of cultural transmission’’ [13]. The term has since been assimilated into everyday discourse. Memes were suggested to
Figure 1. ‘Peering’ in chimpanzees. A young chimpanzee watches intently as its mother uses a stone hammer to crack a nut, at Bossou in West Africa. Schuppli and van Schaik have labelled such avid attention ‘peering’ and used this behaviour to index the extensive scope of all that juvenile apes appear to learn from the accumulated cultural knowledge of their community (photo: T. Matsuzawa and Primate Research Institute, Kyoto University).
Current Biology 29, R829–R850, September 9, 2019 ª 2019 Elsevier Ltd. R845
Current Biology
Dispatches
Figure 2. A ‘cultural iceberg’ of socially transmitted behaviour in apes. Schuppli and van Schaik [8] suggest that the most prevalent approach to identifying great ape cultural traditions by describing regional variations may so far have recognised only the tip of a ‘cultural iceberg’, the greater part of which has remained uncharted. The tip represents often complex and highly visible behaviours, here illustrated by chimpanzee nut-cracking, which occurs only in West Africa despite the widespread distribution of similar materials [1]. Schuppli and van Schaik [8] offer a new way to identify a second layer they suggest may contain scores of other traditions adapted to local ecologies, here illustrated by subterranean termite fishing by chimpanzees using a multi-tool-kit [1] and breaking twigs to suck out ants by orangutans [9,12]. Finally, a basal layer contains many culturally universal behaviours, here illustrated by chimpanzee leaf-sponging to drink water, and dietary preferences in orangutans [8,17] and gorillas [16].
include human catch-phrases and ways of making pots, but in principle any culture should be decomposable into a vast list of its constituent memes. Is this what we now have in Schuppli and van Schaik’s list of elements for the two orangutan sites? These appear to be offered as putative ‘units of cultural transmission’, picked out by the peering focused on them by juveniles. The difficulty here, and indeed in all attempts to describe a community’s cultural repertoire in terms of a discrete number of cultural units or elements, lies in what is to count as a unit. In humans, is Catholicism a meme, or is it constituted of numerous memes at lower levels, like angels, altars and prayers? Likewise, in orangutans, is using a tool to poke seeds out of a fruit a meme, or are constituent
parts like holding the tool in one’s mouth the memes? This fundamental question of ‘unit granularity’ is not explicitly addressed by the authors. Dawkins suggested that a gene be defined as any bit of DNA that ‘‘lasts for enough generations to serve as a unit of selection’’ [13]. This criterion can be directly applied to what is to count as a meme, transmitted across multiple cultural generations. Whether the elements defined by Schuppli and van Schaik [8] elements are indeed units of (cultural) selection is a challenge yet to be addressed. Some exciting beginnings have been made in identifying the operation of selection and cultural evolution in non-human species more generally, for example in birdsong [14].
R846 Current Biology 29, R829–R850, September 9, 2019
Schuppli and van Schaik [8] interpret their results through the analogy of an iceberg, representing the scope of ape culture (Figure 2). So far, they argue, we have glimpsed only its tip visible above the surface, which is made up of the most noticeable elements documented by the earlier cross-cultural studies, such as forms of tool use. Beneath these is a large set of behaviour patterns missed by the cross-cultural approaches because of their reliance on excluding elements explicable by local ecological circumstances. This weakness of the cross-cultural approach [4–6] was recognized by its proponents, seeing it as a first, broad-brush attempt to start to grasp the extent and scope of ape culture. The new study of Schuppli and van Schaik [8] is the first to provide an evidence-based means of delineating a much broader range of cultural adaptions to an ape community’s environment. The base layer of the pyramid includes behaviours that may even be universal in the species, yet still culturally acquired (‘knife use’ might be an equivalent in our own species, for example). These middle and lower parts of the iceberg include many basic and simple behavioural elements, such as selective food choice. It is far from implausible that cultural inheritance is important at this level, given the large size of apes’ dietary repertoire and the vastly greater array of potential items never ingested. Over 200–300 different items (varied parts of numerous species, including fruits, seeds, leaves, stems, pith, flowers, bark, and roots, not to mention vertebrate and invertebrate prey) may be eaten by chimpanzees [15], gorillas [16] and orangutans [17], including a highly selective sub-set of all the potential parts of the many hundreds of species that make up tropical forests. This means there may be well over 1,000 options that could in principle be explored individually, so the value of peering at and learning from the accumulated wisdom underlying the skills and choices of one’s mother, and later others, could indeed be very significant. Field experiments, so far conducted only with other primate species, confirm that infants’ diet selection can be highly dependent on the choices of their mother and her community [18].
Current Biology
Dispatches Orangutan cultures and the evolution of material culture. Science 299, 102–105.
In the new ‘peering’ based study of Schuppli and van Schaik [8], and the challenge of its conclusions, we may be seeing a significant leap in our efforts to capture the true scope of ape culture. The underlying approach may significantly extend the methods applied to study social learning research in the future, in a variety of species other than apes.
6. Robbins, M.M., Ando, C., Fawcett, K.A., Gruiter, C.C., Hedwig, D., Iwata, Y., Lodwick, J.L., Masi, S., Salmi, R., Stoinski, T.S., et al. (2016). Behavioural variation in gorillas: evidence of potential cultural traits. PLoS One 11, e0160483.
REFERENCES
8. Schuppli, C., and van Schaik, C.P. (2019). Animal cultures: how we’ve only seen the tip of the iceberg. Evol. Hum. Sci. 1, e2.
1. Whiten, A. (2017). A second inheritance system: the extension of biology through culture. Interf. Focus 7, 20160142. 2. McGrew, W.C. (1992). Chimpanzee Material Culture: Implications for Human Evolution (Cambridge: Cambridge University Press).
7. Medawar, P. (1977). Unnatural science. The New York Review of Books, Feb. 3rd, 13–18.
9. Schuppli, C., Meulman, E.J.M., Forss, S.I.M., Aprilinayati, F., van Noordwijk, M.A., and van Schaik, C.P. (2016). Observational learning and socially induced practice of routine skills in immature orangutans. Anim. Behav. 119, 87–98.
3. van Lawick-Goodall, J. (1973). Cultural elements in a chimpanzee community. In Precultural Primate Behaviour, E. Menzel, ed. (Basel: Karger), pp. 144–184.
10. Corp, N., and Byrne, R.W. (2002). The ontogeny of manual skill in wild chimpanzees: evidence from feeding on the fruit of Saba florida. Behav. 139, 137–168.
4. Whiten, A., Goodall, J., McGrew, W.C., Nishida, T., Reynolds, V., Sugiyama, Y., Tutin, C.E.G., Wrangham, R.W., and Boesch, C. (1999). Cultures in chimpanzees. Nature 399, 682–685.
11. Ottoni, E.B., de Resende, B.D., and Izar, P. (2005). Watching the best nutcrackers: what capuchin monkeys (Cebus apella) know about others’ tool-using skills. Anim. Cogn. 8, 215–219.
5. van Schaik, C.P., Ancrenaz, M., Borgen, G., Galdikas, B., Knott, C.D., Singleton, I., Suzuki, A., Utami, S.S., and Merrill, M. (2003).
12. van Schaik, C.P., Ancrenaz, M., Djojoasmoro, R., Knott, C.D., Morrogh-Bernard, H.C., Nuzuar, K.O., Atmoko, S.S.U., and
van Noordwijk, M.A. (2009). Orangutan cultures re-visited. In Orangutans: Geographic Variation in Behavioral Ecology and Conservation, S.A. Wich, S.S.U. Atmoko, T.M. Setia, and C.P. van Schaik, eds. (Oxford: Oxford University Press), pp. 299–309. 13. Dawkins, R. (1976). The Selfish Gene (Oxford: Oxford University Press). 14. Aplin, L.M. (2019). Culture and cultural evolution in birds: a review of the evidence. Anim. Behav. 147, 179–187. 15. Inskipp, T. (2005). Chimpanzee (Pan troglodytes). In World Atlas of Great Apes and Their Conservation, J. Caldecott, and L. Miles, eds. (Berkeley: Univ California Press), pp. 53–81. 16. Ferriss, S. (2005). Western gorilla (Gorilla gorilla). In World Atlas of Great Apes and Their Conservation, J. Caldecott, and L. Miles, eds. (Berkeley: Univ California Press), pp. 105–127. 17. McConkey, K. (2005). Bornean orangutan (Pongo pygmaeus). In World Atlas of Great Apes and Their Conservation, J. Caldecott, and L. Miles, eds. (Berkeley: Univ California Press), pp. 161–183. 18. van de Waal, E., Borgeaud, C., and Whiten, A. (2013). Potent social learning and conformity shape a wild primate’s foraging decisions. Science 340, 483–485.
Glia: A Gate Controlling Animal Behavior? Claire Wyart1,* and Andrew Prendergast1,2
pinie`re (ICM), Spinal Sensory Signaling team, Sorbonne Universite , 47 bld hoˆpital, Paris 75013, France du Cerveau et de la Moelle e of Cardiovascular Medicine, Yale University, New Haven, CT 06511, USA *Correspondence: [email protected] https://doi.org/10.1016/j.cub.2019.07.058 1Institut
2Department
Although glia are known to have the potential to alter neuronal activity, their behavioral relevance is not well understood. A recent study has discovered that, when zebrafish give up on performing a visuo-motor task, glia integrate information from neuromodulatory neurons to stop motor output. The word ‘glia’ is derived from the ancient Greek word glia for glue, as glial cells were initially discovered in the search for connective tissue in the brain [1]. Glia are non-neuronal cells of the nervous system and the term covers astrocytes, oligodendrocytes, oligodendrocyte progenitor cells, ependymal cells, radial glial cells and microglial cells (the macrophages of the CNS which enter from the periphery). There are at least as many, if not more,
glial cells than neurons in the brain, yet their importance has long been underappreciated, glia being overshadowed by their glamorous, more electrically-excitable neighbours. Modern neuroscience has, however, revealed a diversity of crucial functions for glia, which intimately communicate with neurons to ensure the development, maintenance, and function of the brain. For example, oligodendrocytes build the myelin sheaths that surround axons of
specific neurons to modulate conduction properties, and can do so in an activitydependent manner [2]. Oligodendrocyte progenitor cells are excitable cells [3]. Microglia shape the migration of inhibitory neurons in the brain during development [4], thereby influencing the critical excitation–inhibition balance in the cortex, and have also been implicated in synaptic pruning during the refinement period of neural circuit formation. Astrocytes contribute to many
Current Biology 29, R829–R850, September 9, 2019 ª 2019 Elsevier Ltd. R847