Downloaded from http://rsbl.royalsocietypublishing.

org/ on December 11, 2016

engage in joint attention. This seminal finding and

the subsequent surge of behavioural research on the
topic led to a rejection of the long-held Piagetian
notion of infant egocentrism (Mundy & Newell
2007). Moreover, research on joint attention suggests
that infants ability to share a common point of reference develops before spoken language (Baldwin
1995), and that joint attention processes are important
precursors of the later development of higher-level
mental state attribution (Charman et al. 2001).
Despite the progress that has been made in understanding the behavioural emergence of joint attention
during infancy (e.g. Carpenter et al. 1998), almost
nothing is known about the brain substrate that supports joint attention in the developing child.
Investigating the neural basis of joint attention in
infants is important for several reasons, including the
possibility that behavioural tasks are insufficiently sensitive to reveal early abilities in infants. In adults, joint
attention relies on the recruitment of the medial
prefrontal cortex (Williams et al. 2005; Schilbach
et al. in press), a brain structure that has been more
generally implicated in social cognition and theory of
mind (Amodio & Frith 2006). Here, we examined
haemodynamic responses in five-month-old infants
prefrontal cortex during triadic social interactions
using near-infrared spectroscopy (NIRS) (see LloydFox et al. (2010) for a description of the method and
its use with infants).
Infants were presented with three different experimental conditions. In all conditions, the infant
watched an adults face in the middle of the screen
with an object either to the left or to the right side of
the face. In the joint attention condition, the adult
raised her eyebrows and smiled while holding eye contact with the infant, then shifted her eyes towards the
object, then shifted her eyes back to the infant and
finally turned her head towards the object. The ability
to jointly attend with another person requires the
infant to not only attend to the external object or
event but also to monitor (i) the other persons attention towards the same object or event and (ii) the
other persons attention in relation to the self.
Our two control conditions thus disrupted these two
critical aspects of joint attention. In the first control
condition, the no referent condition, the person
behaved exactly the same as in the joint attention condition, except that she looked and turned towards the
side where there was no object. In the second control
condition, the no eye contact condition, the person
looked at the object without establishing any eye contact with the infant (the person looked down with
her eyes closed before shifting her eyes towards the
object). We predicted that the brain region that is
specialized in dealing with triadic social interactions
should be selectively engaged during the joint attention
condition but not during the two control conditions,
because they lack the triangular nature required to
establish joint attention.

Biol. Lett. (2010) 6, 540543

doi:10.1098/rsbl.2009.1069
Published online 27 January 2010

Neurobiology

Selective prefrontal cortex

responses to joint attention
in early infancy
Tobias Grossmann* and Mark H. Johnson
Centre for Brain and Cognitive Development, Birkbeck,
University of London, London, UK
*Author for correspondence ([email protected]).

The process by which two people share attention

towards the same object or event is called joint
attention. Joint attention and the underlying triadic representations between self, other person
and object are thought to be unique to humans,
supporting teaching, cooperation and language
learning. Despite the progress that has been
made in understanding the behavioural importance of joint attention during early social
development, almost nothing is known about the
brain substrate that supports joint attention in
the developing infant. We examined responses
in five-month-old infants prefrontal cortex
during triadic social interactions using nearinfrared spectroscopy. The results demonstrate
that, even by the age of five months, infants are
sensitive to triadic interactions and, like adults,
they recruit a specific brain region localized in
left dorsal prefrontal cortex when engaged in
joint attention with another person. This suggests
that the human infant is neurobiologically
prepared for sharing attention with other
humans, which may provide the basis for a wide
variety of uniquely human social and cultural
learning processes.
Keywords: social cognition; prefrontal cortex;
infancy; joint attention

1. INTRODUCTION
Attending and responding to eye gaze is crucial for
human social interactions. Specifically, eye gaze plays
an important role in directing and coordinating attention during triadic interactions between self, other and
the environment. During a typical triadic interaction, a
person may establish eye contact with another person
and then direct that persons gaze to an object or
event. The psychological process by which two
people share attention towards the same object or
event is called joint attention. Joint attention and the
underlying
triadic
representations
(self other
person object) are thought to be unique to our
species, supporting teaching, cooperation and
language learning (Tomasello et al. 2005; Saxe 2006;
Csibra & Gergely 2009). Impairments in joint
attention are one of the earliest signs of autism
(Charman 2003).
More than 30 years ago, Scaife & Bruner (1975)
first observed that infants follow a persons gaze and

2. MATERIAL AND METHODS

(a) Participants
The final sample consisted of 15 five-month-old infants (eight girls)
aged between 136 and 159 days (M 149.1 days). An additional
eight five-month-olds were tested but not included in the final
sample because they had too many motion artefacts, resulting in

Electronic supplementary material is available at http://dx.doi.org/

10.1098/rsbl.2009.1069 or via http://rsbl.royalsocietypublishing.org.
Received 23 December 2009
Accepted 6 January 2010

540

This journal is q 2010 The Royal Society

Downloaded from http://rsbl.royalsocietypublishing.org/ on December 11, 2016

T. Grossmann & M. H. Johnson

Joint attention in infancy

right hemisphere

22

19

17

14

left hemisphere

24

23

21

20

12

11

10

9
7

18
16

541

15

4
2

13
FZ
24 F4 23
12 F3 11
8
21
9
20 10
19 18
6
7
17 16
3
4
15 5
1
14
13
2
22

0.1

oxy Hb (mM mm)

0
0.1

Figure 1. Prefrontal brain responses measured in five-month-old infants. This graph depicts mean oxygenated haemoglobin
concentration changes (+s.e.m.) during the joint attention, no referent and no eye contact conditions measured from 24
NIRS channels within dorsal, ventral and lateral ROIs. Black shaded box, joint attention; light grey shaded box, no referent;
white box, no eye contact; red, dorsal; yellow, lateral; blue, ventral.
too few usable trials for analysis (minimum number of four trials
per condition). Please note that an attrition rate at this level is
within the normal range for an infant NIRS study (Lloyd-Fox et al.
2010). All infants were born full-term (3742 weeks gestation)
and with normal birthweight (.2500 g). All parents gave informed
consent before the study.
(b) Stimuli and procedure
Animated photo-realistic face stimuli were generated using POSER 6.0
software (Curious Lab Inc., Santa Cruz, CA). Infants sat on their
parents lap while watching the stimuli on a computer monitor
within an acoustically shielded, dimly lit room. The faces presented
subtended a visual angle of 388  258, and each eye subtended 38 
58). The experimental sessions consisted of 9 s long trials. The three
experimental conditions were randomly distributed over the session
with no more than two trials of the same condition occurring in a
row. The inter-trial interval randomly varied between 8 and 12 s.
Non-social moving visual stimuli were presented during the
inter-trial interval to keep infants attention.
(c) Data acquisition and analysis
Cortical activations were measured using a Hitachi ETG-4000 NIRS
system. The multi-channel system uses two wavelengths at 695 and
830 nm. Two custom-built arrays consisting of nine optodes (five
sources, four detectors) in a 12-channel (sourcedetector pairs)
arrangement with an inter-optode separation of 25 mm were
placed over the frontal lobe on each hemisphere using an Easycap
(Falk Minow). The NIRS method relies on the optical determination
of changes in haemoglobin concentrations in cerebral cortex which
result from increased regional cerebral blood flow. NIRS data were
continuously sampled at 10 Hz. For analysis, after calculation of
the oxyHb concentration changes, pulse-related signal changes and
overall trends were eliminated by low-pass filtering (Butterworth,
fifth-order, lower cut-off 0.5 Hz). Movement artefacts were corrected
by an established procedure (Koch et al. 2006; Wartenburger et al.
2007), which allows marking of artefacts and then padding the contaminated data segments by linear interpolation. Cortical responses
were assessed by comparing average concentration changes
(oxyHb) within trials (15 s after stimulus onset) between the experimental conditions. For statistical analyses, three regions of interest
(ROIs: dorsal, ventral and lateral prefrontal cortex) were selected
on the basis of prefrontal cortex anatomy and a meta-analysis of
the adult functional magnetic resonance imaging (fMRI) work
Biol. Lett. (2010)

(Amodio & Frith 2006; see figure 1 for ROIs). An omnibus repeated
measures analysis of variance (ANOVA) was conducted with
within-subjects factors: ROI (3)  hemisphere (2)  condition (3).
Subsequently, planned comparisons were performed using repeated
measures ANOVAs for each ROI individually with within-subjects
factors: channel location (4)  hemisphere (2)  condition (3).

3. RESULTS
The omnibus ANOVA revealed a significant three-way
interaction between ROI, hemisphere and condition,
F4,56 3.201, p 0.019, partial h2 0.186. Planned
comparisons revealed a significant interaction between
condition and hemisphere (F2,28 6.944, p 0.004,
partial h2 0.332) for the dorsal prefrontal region.
The left dorsal prefrontal region was specifically sensitive to joint attention interactions. This region showed
the predicted pattern of an increased brain response
when the joint attention condition was compared
with the no referent condition (t14 1.795, p
0.047 one-tailed), and when the joint attention condition was compared with the no eye contact
condition (t14 2.125, p 0.026 one-tailed), whereas
in the right dorsal prefrontal region, there was no
difference between the joint attention and no referent
conditions (t1,14 0.002, p 0.494 one-tailed) and
the response was significantly decreased in the joint
attention when compared with the no eye contact condition (t1,14 21.969, p 0.034 one-tailed). As
shown in figure 1, within the left dorsal prefontal
region, comprising channels 9, 10, 11 and 12, all channels showed increased responses to joint attention
when compared with the other conditions. For channel
12 alone, this effect attained statistical significance
(F2,28 3.962, p 0.031, partial h2 0.281) (see
table S1 in the electronic supplementary material for

Downloaded from http://rsbl.royalsocietypublishing.org/ on December 11, 2016

542 T. Grossmann & M. H. Johnson Joint attention in infancy

statistical results of all channels). No main effects or
interactions were obtained in the planned comparisons
performed for the ventral and lateral prefrontal
regions.

4. DISCUSSION
These results show that, even by the age of five
months, infants are sensitive to triadic interactions
and, like adults, they recruit a specific prefrontal
region localized in left dorsal prefrontal cortex when
engaged in joint attention with another person
(Schilbach et al. in press). It is interesting to note that
the infant brain response was lateralized to the left
hemisphere, which is not only in line with the adult
fMRI work (Schilbach et al. in press) but also concurs
with findings showing that higher rates of resting glucose metabolism in left prefrontal regions measured
with positron emission tomography, and synchronized
brain activity measured from left frontal electrodes
during resting EEG, are positively correlated with childrens tendency to initiate joint attention bids in the
second year of life (Caplan et al. 1993; Mundy Card &
Fox 2000). The finding is also interesting in light of
work showing that adults with autism have atypical
brain structure (increased grey matter) in the same
left prefrontal regions that are functionally implicated
in joint attention in healthy adults (Waiter et al.
2004; Williams et al. 2005).
A critical distinction has been drawn between
responding to joint attention (RJA) and the actual
initiation of joint attention (IJA; Mundy & Newell
2007). In the current study, however, by focusing on
how infants respond to joint attention initiated by an
adult, we were not able to examine this potentially
important difference. Schilbach et al. (in press)
assessed the neurobiological basis of the distinction
between RJA and IJA in adults, and found that while
there are regions commonly involved in both kinds of
joint attention, such as the left medial dorsal prefontal
cortex, the ventral striatum appears to be specifically
engaged only when an adult initiates joint attention.
This specific involvement of the ventral striatum has
been argued to be the basis of the positive affective
experience associated with directing someone elses
gaze. While future neuroimaging work with infants
should address this important distinction between
RJA and IJA, it is unknown whether NIRS can detect
responses from brain structures located as deep as
the ventral striatum (Grossmann 2008).
In conclusion, using a novel paradigm and a
modern optical imaging technique well suited to studying freely behaving infants, we were able to
demonstrate that parts of the left dorsal prefrontal
cortex are selectively activated already very early in
the development of joint attention. This brings into
question claims that joint attention is an ability that
only emerges towards the end of the first year of life
(also termed the nine-month-revolution; Tomasello
1999). The current findings suggest that the human
infant is neurobiologically prepared for sharing attention with other humans, and this may provide the
basis of a wide variety of uniquely human social and
cultural learning processes.
Biol. Lett. (2010)

This work was supported by a Sir Henry Wellcome Postdoctoral

Fellowship awarded by the Wellcome Trust (082659/Z/07/Z)
to T.G., and the UK Medical Research Council (G0701484;
ID: 85031).

Amodio, D. & Frith, C. D. 2006 Meeting of minds: the

medial prefrontal cortex and social cognition. Nat. Rev.
Neurosci. 7, 268277. (doi:10.1038/nrn1884)
Baldwin, D. A. 1995 Understanding the link between
joint attention and language. In Joint attention: its origins
and role in development (eds C. Moore & P. J. Dunham),
pp. 131 158. Hillsdale, NJ: Erlbaum.
Caplan, R., Chugani, H., Messa, C., Guthrie, D., Sigman,
M., Traversay, J. & Mundy, P. 1993 Hemispherectomy
for early onset intractable seizures: presurgical cerebral
glucose metabolism and postsurgical nonverbal communication patterns. Dev. Med. Child Neurol. 35,
574 581.
Carpenter, M., Nagell, K. & Tomasello, M. 1998 Social cognition, joint attention, and communicative competence
from 9 to 15 months of age. Monographs of the Society
for Research in Child Development, no. 63. (doi:10.
2307/1166214)
Charman, T. 2003 Why is joint attention a pivotal skill in
autism? Phil. Trans. R. Soc. Lond. B 358, 315 324.
(doi:10.1098/rstb.2002.1199)
Charman, T., Baron-Cohen, S., Swettenham, J., Baird, G.,
Cox, A. & Drew, A. 2001 Testing joint attention, imitation, and play as infancy precursors to language and
theory of mind. Cogn. Dev. 4, 481498.
Csibra, G. & Gergely, G. 2009 Natural pedagogy.
Trends Cogn. Sci. 13, 148153. (doi:10.1016/j.tics.2009.
01.005)
Grossmann, T. 2008 Shedding light on infant brain function:
the use of near-infrared spectroscopy (NIRS) in the study
of face perception. Acta Paediatr. 97, 11561158. (doi:10.
1111/j.1651-2227.2008.00938.x)
Koch, S. P., Steinbrink, J., Villringer, A. & Obrig, H. 2006
Synchronization between background activity and visually
evoked potential is not mirrored by focal hyperoxygenation: implications for the interpretation of vascular brain
imaging. J. Neurosci. 26, 49404948. (doi:10.1523/
JNEUROSCI.3989-05.2006)
Lloyd-Fox, S., Blasi, A. & Elwell, C. E. 2010 Illuminating
the developing brain: the past, present, and future of
near infrared spectroscopy. Neurosci. Biobehav. Rev. 34,
269 284.
Mundy, P. & Newell, L. 2007 Attention, joint attention, and
social cognition. Curr. Dir. Psychol. Sci. 16, 269 274.
(doi:10.1111/j.1467-8721.2007.00518.x)
Mundy, P., Card, J. & Fox, N. 2000 Fourteen-month cortical
activity and different joint attention skills. Dev. Psychobiol.
36, 325 338. (doi:10.1002/(SICI)1098-2302(200005)
36:4,325::AID-DEV7.3.0.CO;2-F)
Saxe, R. 2006 Uniquely human social cognition. Curr.
Opin. Neurobiol. 16, 235239. (doi:10.1016/j.conb.
2006.03.001)
Scaife, M. & Bruner, J. 1975 The capacity for joint visual
attention in the infant. Nature 253, 265 266. (doi:10.
1038/253265a0)
Schilbach, L., Wilms, M., Eickhoff, S. B., Romanzetti, S.,
Tepest, R., Bente, G., Shah, N. J., Fink, G. R. &
Vogeley, K. In press. Minds made for sharing: initiating
joint attention recruits reward-related neurocircuitry.
J. Cogn. Neurosci.
Tomasello, M. 1999 The cultural origins of human cognition.
Cambridge, MA: MIT Press.

Downloaded from http://rsbl.royalsocietypublishing.org/ on December 11, 2016

Joint attention in infancy

Tomasello, M., Carpenter, M., Call, J., Behne, T. & Moll, H.
2005 Understanding and sharing intentions: the origins of
cultural cognition. Behav. Brain Sci. 28, 675735.
(doi:10.1017/S0140525X05000129)
Waiter, G. D., Williams, J. H. G., Murray, A. D., Gilchrist, A.,
Perrett, D. I. & Whiten, A. 2004 A voxel based investigation
of brain structure in male adolescents with autistic spectrum disorder. NeuroImage 22, 619625. (doi:10.1016/j.
neuroimage.2004.02.029)

Biol. Lett. (2010)

T. Grossmann & M. H. Johnson

543

Wartenburger, I., Steinbrink, J., Telkemeyer, S., Friedrich,

M., Friederici, A. D. & Obrig, H. 2007 The processing
of prosody: evidence of interhemispheric specialization
at the age of four. Neuroimage 34, 416 425. (doi:10.
1016/j.neuroimage.2006.09.009)
Williams, J. H. G., Waiter, G. D., Perra, O., Perrett, D. &
Whiten, A. 2005 An fMRI study of joint attention
experience. NeuroImage 25, 133 140. (doi:10.1016/j.
neuroimage.2004.10.047)