Article price
EUR €25.00USD $30.00
Primates must solve complex spatial problems when foraging, such as finding patchy resources and navigating between different locations. However, the nature of the cognitive representations supporting these types of behaviors is currently unclear. In humans, there has been great debate concerning the relative importance of egocentric representations (which are viewer-dependent) versus allocentric representations (which are based on aspects of the external environment). Comparative studies of nonhuman apes can illuminate which aspects of human spatial cognition are shared with other primates, versus which aspects are unique to our lineage. The current studies therefore examined spatial cognitive development in one of our closest living relatives, bonobos (Pan paniscus) across contexts. The first study assessed how younger bonobos encode locations in a place-response task in which apes first learn that one of two locations is consistently baited with a reward, and then must approach the two locations from a flipped perspective. The second study examined how a larger age sample of bonobos responded to a spatial relations task in which they first experience that one location is baited, and then can generalize this learning to a new set of targets. Results indicated that while bonobos exhibited a predominantly allocentric strategy in the first study, they consistently exhibited an egocentric strategy in the second. Together, these results show that bonobos can use both strategies to encode spatial information, and illuminate the complementary contributions to cognition made by egocentric and allocentric representations.
Context influences spatial frames of reference in bonobos (Pan paniscus)
in Behaviour
Sections
References
AcredoloL.P. (1978). Development of spatial orientation in infancy. — Dev. Psychol. 14: 224-234.
AcredoloL.P. (1979). Laboratory versus home: the effect of environment on the 9-month-old infant’s choice of spatial reference system. — Dev. Psychol. 15: 666-667.
AcredoloL.P.EvansD. (1980). Developmental changes in the effects of landmarks on infant spatial behavior. — Dev. Psychol. 16: 312-318.
Albiach-SerranoA.CallJ.BarthJ. (2010). Great apes track hidden objects after changes in the objects’ position and in subject’s orientation. — Am. J. Primatol. 72: 349-359.
BaayenR.H. (2008). Analyzing linguistic data. A practical introduction to statistics. — Cambridge University PressCambridge, MA.
BatesD. (2010). The LME4 package: linear mixed-effects models using S4 classes. — Available online at http://www.R-project.org.
BolkerB.M.BrooksM.E.ClarkC.J.GeangeS.W.PoulsenJ.R.StevensM.H.H.WhiteJ.S.S. (2008). Generalized linear mixed models: a practical guide for ecology and evolution. — Trends Ecol. Evol. 24: 127-135.
BrownP.LevinsonS. (1992). ‘Left’ and ‘right’ in Tenejapa: investigating a linguistic conceptual gap. — Z. Phonetik Sprachwissensch. Kommunikationsforsch. 45: 590-611.
BrownP.LevinsonS.C. (2000). Frames of spatial reference and their acquisition in Tenejapan Tzeltal. — In: Culture thought and development ( NucciL.SaxeG.TurielE. eds). Lawrence ErlbaumMahwah, NJ p. 167-197.
BurgessN. (2006). Spatial memory: how egocentric and allocentric combine. — Trends Cogn. Sci. 10: 551-557.
BurgessN. (2008). Spatial cognition and the brain. — Ann. NY Acad. Sci. 1124: 77-97.
ChengK. (1986). A purely geometric module in the rat’s spatial representation. — Cognition 23: 149-178.
GallistelC.R. (1990). The organization of learning. — Bradford Books/MIT PressCambridge, MA.
GentnerD. (2007). Spatial cognition in apes and humans. — Trends Cogn. Sci. 11: 192-194.
HareB. (2007). From nonhuman to human mind: what changed and why. — Curr. Dir. Psychol. Sci. 16: 60-64.
HareB.WobberV.WrangamR. (2012). The self-domestication hypothesis: evolution of bonobo psychology is due to selection against aggression. — Anim. Behav. 83: 573-585.
HaunD.B.M.RapoldC.J.CallJ.JanzenG.LevinsonS.C. (2006a). Cognitive cladistics and cultural override in Hominid spatial cognition. — Proc. Natl. Acad. Sci. USA 103: 17568-17573.
HaunD.B.M.CallJ.JanzenG.LevinsonS.C. (2006b). Evolutionary psychology of spatial representations in the Hominidae. — Curr. Biol. 16: 1736-1740.
HermerL.SpelkeE. (1994). A geometric process for spatial reorientation in young children. — Nature 370: 57-59.
Hermer-VazquezL.SpelkeE.KatnelsonA.S. (1999). Sources of flexibility in human cognition: dual-task studies of space and language. — Cogn. Psychol. 39: 3-36.
Hermer-VazquezL.MoffetA.MunkholmP. (2001). Language, space, and the development of cognitive flexibility in humans: the case of two spatial memory tasks. — Cognition 79: 263-299.
HerrmannE.HareB.CallJ.TomaselloM. (2010). Differences in the cognitive skills of bonobos and chimpanzees. — PLoS One 5: e12438.
HoffmanM.L.BeranM.J. (2006). Chimpanzees (Pan troglodytes) remember the location of a hidden food item after altering their orientation to a spatial array. — J. Comp. Psychol. 120: 389-393.
HribarA.CallJ. (2011). Great apes use landmark cues over spatial relations to find hidden food. — Anim. Cogn. 14: 623-635.
HribarA.HaunD.CallJ. (2011). Great apes’ strategies to map spatial relations. — Anim. Cogn. 14: 511-523.
JansonC.H. (1998). Experimental evidence for spatial memory in wild brown capuchin monkeys (Cebus apella). — Anim. Behav. 55: 1229-1243.
JansonC.H. (2007). Experimental evidence for route integration and strategic planning in wild capuchin monkeys. — Anim. Cogn. 10: 341-356.
JansonC.H.ByrneR. (2007). What wild primates know about resources: opening up the black box. — Anim. Cogn. 10: 357-367.
KanngiesserP.CallJ. (2010). Bonobos, chimpanzees, gorillas, and orangutans use feature and spatial cues in two spatial memory tasks. — Anim. Cogn. 13: 419-430.
KanoT. (1992). The last ape: pygmy chimpanzee behavior and ecology. — Stanford University PressStanford, CA.
LearmonthA.E.NewcombeN.S.SheridanN.JonesM. (2008). Why size counts: children’s spatial reorientation in large and small enclosures. — Dev. Sci. 11: 414-426.
LeeS.A.SpelkeE. (2010). Two systems of spatial representation underlying navigation. — Exp. Brain Res. 206: 179-188.
LevinsonS.C. (1996). Frames of reference and Molyneux’s question: cross-linguistic evidence. — In: Language and space. Language speech and communication ( BloomP.PetersonM.A.NadelL.GarrettM.F. eds). MIT PressCambridge, MA p. 385-436.
LevinsonS.C.KitaS.HaunD.B.M.RaschB.H. (2002). Returning the tables: language affects spatial reasoning. — Cognition 84: 144-188.
LiP.GleitmanL. (2002). Turning the tables: language and spatial reasoning. — Cognition 83: 265-294.
MaguireE.A.BurgessN.DonnettJ.G.FrackowiakR.S.J.FrithC.D.O’KeefeJ. (1998). Knowning where and getting there: a human navigation network. — Science 280: 921-923.
MajidA.BowermanM.KitaS.HaunD.LevinsonS. (2004). Can language restructure cognition? The case for space. — Trends Cogn. Sci. 8: 108-114.
MalenkyR.K.WranghamR.W. (1993). A quantitative comparison of terrestrial herbaceous food consumption by Pan paniscus in the Lomako Forest, Zaire, and Pan troglodytes in the Kibale Forest, Uganda. — Am. J. Primatol. 32: 1-12.
Martin-OrdasG.HaunD.ColmenaresF.CallJ. (2010). Keeping track of time: evidence for episodic-like memory in great apes. — Anim. Cogn. 13: 331-340.
MatsuzawaT. (2007). Comparative cognitive development. — Dev. Sci. 10: 97-103.
MatsuzawaT.TomonagaM.TanakaM. (eds) (2006). Cognitive development in chimpanzees. — SpringerTokyo.
MendesN. (2008). Spatial memory in chimpanzees: single-trial learning and 24 hour and 3 month long-term memory. — Folia Primatol. 79: 283-304.
MenzelC.R.Savage-RumbaughE.S.MenzelE.W. (2002). Bonobo (Pan paniscus) spatial memory and communication in a 20-hectare forest. — Int. J. Primatol. 23: 601-619.
MenzelE.W. (1973). Chimpanzee spatial memory organization. — Science 182: 943-945.
NewcombeN.S.HuttenlocherJ. (2006). Development of spatial cognition. — In: Handbook of child psychologyVol. II: cognition perception and language ( DamonW.LernerR.M.KuhnD.SieglerR.S. eds). WileyNew York, NY p. 734-776.
NewcombeN.S.RatliffK.R. (2007). Explaining the development of spatial reorientation: modularity-plus-language versus the emergence of adaptive combination. — In: Emerging landscapes of mind: mapping the nature of change in spatial cognitive development ( PlumertJ.SpencerJ. eds). Oxford University PressNew York, NY p. 53-76.
NewcombeN.S.HuttenlocherJ.DrummeyA.WileyJ.G. (1998). The development of spatial location coding: place learning and dead reckoning in the second and third years. — Cogn. Dev. 13: 185-200.
NormandE.BanS.D.BoeschC. (2009). Forest chimpanzees (Pan troglodytes verus) remember the location of numerous fruit trees. — Anim. Cogn. 12: 797-807.
NormandE.BoeschC. (2009). Sophisticated Euclidean maps in forest chimpanzees. — Anim. Behav. 77: 1195-1201.
PackardM.G. (1996). Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. — Neurobiol. Learn. Mem. 65: 65-72.
PackardM.G. (1999). Glutamate infused posttraining into the hippocampus or caudate-putamen differentially strengthens place and response learning. — Proc. Natl. Acad. Sci. USA 96: 12881-12886.
PackardM.G. (2009). Exhumed from thought: basal ganglia and response learning in the plus-maze. — Behav. Brain Res. 199: 24-31.
PackardM.G.GoodmanJ. (2013). Factors that influence the relative use of multiple memory systems. — Hippocampus 23: 1044-1052.
PedersonE.DanzigerE.WilkinsD.G.LevinsonS.C.KitaS.SenftG. (1998). Semantic typology and spatial conceptualization. — Language 74: 557-589.
PoldrackR.A.ClarkM.A.Pare-BlagoevE.J.ShohamyD.Creso MoyanJ.MyersC. (2001). Interactive memory systems in the human brain. — Nature 414: 546.
PoldrackR.A.PackardM.G. (2003). Competition among multiple memory systems: converging evidence from animal and human brain studies. — Neuropsychologia 41: 245-251.
R Development Core Team (2011). A language and environment for statistical computing. — http://www.R-project.org.
RatliffK.R.NewcombeN.S. (2008). Reorienting when clues conflct: evidence for an adaptive-combination view. — Psychol. Sci. 19: 1301-1307.
RosatiA.G.HareB. (2012). Chimpanzees and bonobos exhibit divergent spatial memory development. — Dev. Sci. 15: 840-853.
RosatiA.G.RodriguezK.HareB. (2014). The ecology of spatial memory in four lemur species. — Anim. Cogn.in press DOI:10.1007/s10071-014-0727-2.
RosatiA.G.WobberV.HughesK.SantosL.R. (in press). How is human cognitive development unique? — Comp. Dev. Psychol.
SherryD.F.SchacterD.L. (1987). The evolution of multiple memory systems. — Psychol. Rev. 94: 439-454.
ShettleworthS.J. (1998). Cognition evolution and behavior. — Oxford University PressNew York, NY.
SpelkeE.LeeS.A.IzardV. (2010). Beyond core knowledge: natural geometry. — Cogn. Sci. 1: 1-22.
TolmanE.C. (1948). Cognitive maps in rats and men. — Psychol. Rev. 55: 189-208.
WangR.F.SpelkeE.S. (2002). Human spatial representation: insights from animals. — Trends Cogn. Sci. 6: 376-382.
WhiteF.J. (1998). Seasonality and socioecology: the importance of variation in fruit abundance to bonobo sociality. — Int. J. Primatol. 19: 1013-1027.
WhiteF.J.WranghamR.W. (1988). Feeding competition and patch size in the chimpanzee species Pan paniscus and Pan troglodytes. — Behaviour 105: 148-163.
WhiteN.M.McDonaldR.J. (2002). Multiple parallel memory systems in the brain of the rat. — Neurobiol. Learn. Mem. 77: 125-184.
WobberV.HareB. (2011). Psychological health of orphan bonobos and chimpanzees in African sanctuaries. — PLoS One 6: e17147.
WobberV.WranghamR.HareB. (2010). Bonobos exhibit delayed development of social behavior and cognition relative to chimpanzees. — Curr. Biol. 20: 226-230.
WobberV.HerrmannE.HareB.WranghamR.TomaselloM. (2013). Differences in the early cognitive development of children and great apes. — Dev. Psychobiol.in press DOI:10.1002/dev.21125.
Figures
-
View in gallery
Setup for place-response task (Study 1). In each session, apes first completed 12 learning trials in which one of two locations (both overturned bowls) was consistently baited. In the final probe trial, the apes’ starting position was rotated 180° so they faced the locations from a flipped perspective. Their responses therefore indicated if they had encoded the baited location from a viewer-dependent (egocentric) framework or a spatial (allocentric) framework. On all trials the caretaker centered the bonobo at their starting position, and the experimenter stood in the opposite position across the midline of the testing area.
-
View in gallery
Results from place-response task (Study 1). (a) Bonobos’ mean proportion choices for the correct location in learning trials, and for the allocentric location in probe trials. (b) Relationship between overall allocentric probe choices and the subject’s age. Error bars indicate standard error. ∗, ∗∗∗.
-
View in gallery
Setup for relations task (Study 2). Apes first completed a learning phase in which one location (always either the left or right side) was consistently baited. After apes met a learning criterion indicating they consistently chose the correct side, they moved 180° into a new room for the test phase. In the last 10 trials, apes faced an identical table from a flipped perspective to assess if they had encoded the baited location from a viewer-dependent (egocentric) framework or a spatial (allocentric) framework. The experimenter sat centered behind the table at both locations.
-
View in gallery
Results from the relations task (Study 2). (a) Bonobos’ mean proportion choices in the test phase for the allocentric option, the egocentric option, and the middle option. (b) Breakdown of egocentric choices in test phase by the subjects’ sex. Error bars indicate standard error. ∗, ∗∗∗.
Setup for place-response task (Study 1). In each session, apes first completed 12 learning trials in which one of two locations (both overturned bowls) was consistently baited. In the final probe trial, the apes’ starting position was rotated 180° so they faced the locations from a flipped perspective. Their responses therefore indicated if they had encoded the baited location from a viewer-dependent (egocentric) framework or a spatial (allocentric) framework. On all trials the caretaker centered the bonobo at their starting position, and the experimenter stood in the opposite position across the midline of the testing area.
Results from place-response task (Study 1). (a) Bonobos’ mean proportion choices for the correct location in learning trials, and for the allocentric location in probe trials. (b) Relationship between overall allocentric probe choices and the subject’s age. Error bars indicate standard error. ∗, ∗∗∗.
Setup for relations task (Study 2). Apes first completed a learning phase in which one location (always either the left or right side) was consistently baited. After apes met a learning criterion indicating they consistently chose the correct side, they moved 180° into a new room for the test phase. In the last 10 trials, apes faced an identical table from a flipped perspective to assess if they had encoded the baited location from a viewer-dependent (egocentric) framework or a spatial (allocentric) framework. The experimenter sat centered behind the table at both locations.
Results from the relations task (Study 2). (a) Bonobos’ mean proportion choices in the test phase for the allocentric option, the egocentric option, and the middle option. (b) Breakdown of egocentric choices in test phase by the subjects’ sex. Error bars indicate standard error. ∗, ∗∗∗.
Information
Content Metrics
| All Time | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 8 | 8 | 3 |
| Full Text Views | 58 | 58 | 43 |
| PDF Downloads | 3 | 3 | 1 |
| EPUB Downloads | 0 | 0 | 0 |