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. Garca-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. Frisn, Cell 122, 133 (2005).
10. A. Kepecs, G. Fishell, Nature 505, 318 (2014).
11. T. K. Hensch, M. P. Stryker, Science 272, 554 (1996).
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

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

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

knowledge of others if it deviates from what

they themselves know.
In children, the capacity for false beliefs
is tested in a hiding-and-rehiding scenario.
Children first see Sally, a doll, hide an item.
Once Sally exits the room, another doll
quickly rehides the item in a different place.
The children are then asked where Sally will
look upon return. Young children pick the
place where they themselves know the item
to be, but older children understand that
Sally does not share their knowledge (5). In
general, children pass this false-belief test
only after the age of four.
In 2007, an innovative experiment challenged the conclusion that younger children
fail to grasp false beliefs (6). Relying on eyetracking technology, scientists measured
where children look when the protagonist
returns to the scene. Children as young as
24 months correctly anticipated the agents
searching pattern even if they knew it to be
wrong. This experiment inspired Krupenye
et al.s ape study. The investigators had access to an unusually large number of apes of
three species: 19 chimpanzees, 14 bonobos,
and 7 orangutans. In the experiments, the
apes watch videotapes in which a human
actor interacts with another human actor
in a King Kong (KK) suit.
In one scenario, an ape sees KK steal an
object from a human actor and hide it under one of two boxes, say the one on the left.
KK then chases off the human and secretly
rehides the object under the box on the
40

right. After this, KK takes the object away

and leaves the scene. 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. Even though the ape knows that both
boxes are empty, he should expect the human to go to the left-hand box, where he last
saw the item being put. Eye-tracking shows
that the apes correctly anticipate the human
searching pattern, despite the discrepancy
with their own knowledge.
This nonverbal paradigm is a genuine
breakthrough, 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. Given the
importance attached to theory of mind in
developmental psychology and its possible
deficits in relation to autism spectrum disorder and schizophrenia, it is important to put
this capacity in a biological context. 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.
The results contain a lesson for those
who jump on negative outcomes regarding
animal mental capacities as proof of human
distinctiveness. As the old mantra goes, absence of evidence is not evidence of absence.
We should always keep an open mind about
the capacities of nonhuman species (7).

Whether other animals possess theory of

mind has been treated as an all-or-nothing
question. It may be more fruitful, however,
to break larger capacities into smaller elements, many of which may be shared
across species (8).
Theory of mind is probably part of a much
larger picture that includes empathy, social
connectedness, and the way bodies relate to
other bodies. It is no accident that the tests
conducted here focus on the body, i.e., subjects eyes following the physical movements
of actors. As such, the study by Krupenye et
al. 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. Reading others minds
is beyond anybodys capacity. All we can
doand what apes apparently do in similar
waysis read bodies. j
REFERENCES

1. C. Krupenye, F. Kano, S. Hirata, J. Call, M. Tomasello,

Science 354, 110 (2016).
2. E. W. Menzel, in Behavior of Nonhuman Primates, vol. 5,
A. M. Schrier, F. Stollnitz, Eds. (Academic Press, New York,
1974), pp. 83153.
3. D. Premack, G. Woodruff, Behav. Brain Sci. 4, 515 (1978).
4. J. M. Dally, N. J. Emery, N. S. Clayton, Science 312, 1662
(2006).
5. H. Wimmer, J. Perner, Cognition 13, 103 (1983).
6. V. Southgate, A. Senju, G. Csibra, Psychol. Sci. 18, 587
(2007).
7. F. B. M. de Waal, Are We Smart Enough to Know How Smart
Animals Are? (Norton, 2016).
8. F. B. M. de Waal, P. F. Ferrari, Trends Cogn. Sci. 14, 201
(2010).
10.1126/science.aai8851

sciencemag.org SCIENCE

7 OCTOBER 2016 VOL 354 ISSUE 6308

Published by AAAS

PHOTO: CYRIL RUOSO/MINDEN PICTURES/NATIONAL GEOGRAPHIC CREATIVE

Using eye-tracking technology, Krupenye et al. show that chimpanzees and other apes can grasp what others know, even when it differs from what they themselves know.

Apes know what others believe

Frans B. M. de Waal (October 6, 2016)
Science 354 (6308), 39-40. [doi: 10.1126/science.aai8851]

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