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The dynamic integration

of cells continues
postnatally in the frontal
lobe of humans.

from their embryonic predecessors, making
a strong but circumstantial case for their
findings. More important, the authors were
able to support their histologic evidence with
T2 signal intensity in magnetic resonance
images of developing and postnatal human
brains, which allowed them to detect migratory streams of cells, providing an important
in vivo correlate for their conclusions. The
cross-correlation between high-resolution in
vitro analysis and lower-resolution in vivo
imaging is extremely promising. It suggests
that with modest improvements, noninvasive clinical studies will allow us to explore
the postnatal migration of cells within the
human brain.
What are the implications of these findings
for our understanding of brain development?
With a shift in focus from neurogenesis to
maturation, the authors raise the question
of what aspects of brain development we
have missed. The loss of markers of young
migrating neurons such as doublecortin by
6 months implies that shortly after birth the
residual migration of interneurons is complete. Nonetheless, it remains possible that
a postmigratory but immature interneuron
population is retained within the young
brain for months or perhaps years. If humans possess an “interneuron reserve,” its
potential to contribute to plasticity under
normal or pathophysiological conditions
may be considerable. Accumulated evidence
indicates that specific interneuron populations control critical-period plasticity within
the brain (11). Moreover, transplantation
studies pioneered by this same group have
indicated that the grafting of interneuron
precursors can reopen critical-period plasticity (12). The present data suggest that these
findings, rather than being epiphenomena,
may reflect the underlying biology of how
our brains are assembled. j
REFERENCES AND NOTES

1. R. E. Passingham, J. B. Smaers, Brain. Behav. Evol. 84, 156
(2014).
2. D. V. Hansen, J. H. Lui, P. R. L. Parker, A. R. Kriegstein,
Nature 464, 554 (2010).
3. M. F. Paredes et al., Science 354, aaf7073 (2016).
4. S. A. Anderson, D. D. Eisenstat, L. Shi, J. L. Rubenstein,
Science 278, 474 (1997).
5. C. Lois, J. M. García-Verdugo, A. Alvarez-Buylla, Science
271, 978 (1996).
6. K. Letinic, R. Zoncu, P. Rakic, Nature 417, 645 (2002).
7. D. V. Hansen et al., Nat. Neurosci. 16, 1576 (2013).
8. T. Ma et al., Nat. Neurosci. 16, 1588 (2013).
9. K. L. Spalding, R. D. Bhardwaj, B. A. Buchholz, H. Druid,
J. Frisén, Cell 122, 133 (2005).
10. A. Kepecs, G. Fishell, Nature 505, 318 (2014).
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12. D. G. Southwell et al., Science 327, 1145 (2010).
ACKNOWLEDGMENTS

We thank C. Mayer and R. Machold for critical reading and
insightful comments on the manuscript. Supported by the
Simons Foundation and NIH grants MH071679, MH111529,
NS074972, and NS081297 (G.F.), and by NIH grant
T32MH015174-39 (M.M.).
10.1126/science.aai9379
SCIENCE sciencemag.org

DEVELOPMENT

Apes know
what others
believe
Understanding false beliefs
is not unique to humans
By Frans B. M. de Waal

O

f all the human uniqueness claims
proposed over the years, theory of
mind enjoys perhaps the most prominent status. The term “theory of
mind” refers to the ability to know
what others know, that is, to attribute mental states such as intentions, goals,
and knowledge to others. It is widely held
to be unique to humans. Yet, given the results reported by Krupenye et al. on page
110 of this issue, this claim is starting to
wobble (1). The authors show that apes can
correctly anticipate where human actors
will look for a hidden item, even if the apes
know that the item is no longer there. Ironically, this finding brings us back to square
one, because apes played a major role in the
formulation of the theory of mind concept.
In the late 1960s, the primatologist Emil
Menzel often took a young chimpanzee by
the hand out into a large, grassy enclosure
to show her hidden food or a scary object,
such as a toy snake. After this, Menzel
brought the ape back to a waiting group
of juveniles and released them together.
Would the others pick up on her knowledge? The other apes proved eager to follow an ape who knew a food location, but
reluctant to stay with one who had seen a
snake (2). Ever since, the hiding and finding of items has been the main way of investigating what individuals know about
what others know. A more controlled ape
experiment gave the phenomenon its name
when Premack and Woodruff asked, “Does
the chimpanzee have a theory of mind?” (3).
Theory of mind soon became a staple of
developmental psychology. Many animal
studies followed as well, including on monkeys and birds (4). During all of the debates
about animal theory of mind, however,
one assumption seemed unassailable: that
nonhuman species have trouble with false
beliefs. This means that they fail to grasp

Living Links Center of the Yerkes National Primate Research
Center and Department of Psychology, Emory University,
Atlanta, GA 30322, USA. Email: dewaal@emory.edu
7 OCTOBER 2016 • VOL 354 ISSUE 6308

Published by AAAS

39

Downloaded from http://science.sciencemag.org/ on October 9, 2016

are already generated before birth. Cortical
interneurons are renowned for their diversity, which has been shown to relate to their
region of origin (10). The Arc populations
identified appear to run the gamut of different interneuron subtypes, which in rodents
are known to arise from distinct ventral telencephalic progenitor zones. The source and
precise timing of the origin of migrating Arc
cells, and how they are assembled in the cortex, remain open questions.
Studies on human brain development
are technically difficult and typically rely
on piecemeal data. The heroic effort needed
to histologically examine and track virally
labeled Arc cells using the meager human
samples available should not be underestimated. By overcoming the inherent difficulties involved in such studies, Paredes et al.
have begun to scratch the surface of how
this novel mode of circuit integration could
influence human brain development. Despite
the sparseness of their data, both indirect
and direct lines of evidence support their
conclusions. With striking symmetry, Arc
cells migrate in a manner indistinguishable

not only because it avoids an undue reliance on language skills required to understand narrative and questions in theory of mind testing in children but also because it highlights the mental continuity between great apes and humans. Csibra. where he last saw the item being put. 18. 2016 knowledge of others if it deviates from what they themselves know. Eds. In the experiments. In general.1126/science. B. 14. S. 1662 (2006). to break larger capacities into smaller elements. 587 (2007). F. Krupenye et al. Clayton. It is no accident that the tests conducted here focus on the body. M. As the old mantra goes. A. the study by Krupenye et al. Senju. F. de Waal. Are We Smart Enough to Know How Smart Animals Are? (Norton. Given the importance attached to theory of mind in developmental psychology and its possible deficits in relation to autism spectrum disorder and schizophrenia. Sci. 10. This experiment inspired Krupenye et al. Trends Cogn. an ape sees KK steal an object from a human actor and hide it under one of two boxes. the capacity for false beliefs is tested in a hiding-and-rehiding scenario. Children as young as 24 months correctly anticipated the agent’s searching pattern even if they knew it to be wrong. The investigators had access to an unusually large number of apes of three species: 19 chimpanzees. Wimmer. F. 83–153. 4. in Behavior of Nonhuman Primates. Children first see Sally. show that chimpanzees and other apes can grasp what others know. F. 2016). 201 (2010).sciencemag. S. j REFERENCES 1. N..e. Kano. 8. H. absence of evidence is not evidence of absence. another doll quickly rehides the item in a different place. Theory of mind is probably part of a much larger picture that includes empathy. . N. Relying on eyetracking technology. Whether other animals possess theory of mind has been treated as an all-or-nothing question. J. Behav. 1974). KK takes the object away and leaves the scene. Emery. 5. V. and the way bodies relate to other bodies. J. The results contain a lesson for those who jump on negative outcomes regarding animal mental capacities as proof of human distinctiveness. KK then chases off the human and secretly rehides the object under the box on the 40 right. de Waal. Menzel. D. Young children pick the place where they themselves know the item to be. This nonverbal paradigm is a genuine breakthrough. In children.’s ape study. say the one on the left. Southgate. despite the discrepancy with their own knowledge. All we can do—and what apes apparently do in similar ways—is read bodies. Eye-tracking shows that the apes correctly anticipate the human searching pattern. many of which may be shared across species (8). Sci. Perner. M. The human actor now returns to search for the object while an infrared eye-tracker measures precisely which parts of the video the ape subject pays attention to.Downloaded from http://science. 3. Woodruff.org/ on October 9. Krupenye. scientists measured where children look when the protagonist returns to the scene. but older children understand that Sally does not share their knowledge (5). Dally. Ferrari. New York. the apes watch videotapes in which a human actor interacts with another human actor in a King Kong (KK) suit. M. G. We should always keep an open mind about the capacities of nonhuman species (7). 6. 4. may help us move away from the prevailing assumption that theory of mind relies on a cognitive simulation of what is going on in the heads of others. 110 (2016). In one scenario. After this. Even though the ape knows that both boxes are empty. W. 2. and 7 orangutans. G. A. social connectedness. he should expect the human to go to the left-hand box. Science 354. J. As such. It likely evolved in the complex societies that mark the Hominidae (humans and apes) to offer individuals the benefit of better anticipating the behavior of others. Premack. pp.org SCIENCE 7 OCTOBER 2016 • VOL 354 ISSUE 6308 Published by AAAS PHOTO: CYRIL RUOSO/MINDEN PICTURES/NATIONAL GEOGRAPHIC CREATIVE Using eye-tracking technology. Stollnitz. Psychol. Brain Sci. however. E. Science 312. It may be more fruitful. Schrier. M. it is important to put this capacity in a biological context. hide an item. 5. subjects’ eyes following the physical movements of actors. a doll.aai8851 sciencemag. 103 (1983). vol. J. 515 (1978). The children are then asked where Sally will look upon return. i. P. F. Tomasello. M. an innovative experiment challenged the conclusion that younger children fail to grasp false beliefs (6). Call. In 2007. Hirata. (Academic Press. 7. 14 bonobos. B. children pass this false-belief test only after the age of four. Once Sally exits the room. Reading others’ minds is beyond anybody’s capacity. Cognition 13. C. even when it differs from what they themselves know.

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