Developmental Psychology Infant Categorization Study Presentation

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Paper presentation (Psych UA-34 Summer 2023)
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Nonhuman primate vocalizations support
categorization in very young human infants
Alissa L. Ferrya,b,1, Susan J. Hesposb, and Sandra R. Waxmanb
a
Cognitive Neuroscience Sector, Scuola Internazionale Superiore di Studi Avanzati, 34136 Trieste, Italy; and bDepartment of Psychology, Northwestern
University, Evanston, IL 60208
Edited* by Elizabeth S. Spelke, Harvard University, Cambridge, MA, and approved July 24, 2013 (received for review December 6, 2012)
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infancy developmental tuning language acquisition
conceptual development language and thought
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uman infants rapidly tune in to the signals of human language. At birth, they prefer listening to the vocalizations of
human and nonhuman primates over arti?cial sounds; within
months, as their listening preferences narrow, they become attuned to human speech, and to their own native language(s) in
particular (1–7).
Interestingly, the developmental path underlying infants’ rapid
tuning to the faces of communicative partners follows a similar
trajectory: Infants’ prowess in human face-processing derives
from a broader template that initially encompasses faces of both
humans and nonhuman primates before tuning speci?cally to
human faces (8–10). Moreover, these tuning effects are also
evident in infants’ cross-modal (auditory-visual) matching. Initially, human infants reveal a broad capacity to match speciesspeci?c vocalizations and faces (e.g., matching human vocalizations to human faces and nonhuman primate vocalizations to
nonhuman primate faces), but within the ?rst year of life, this
broad pattern of cross-modal matching narrows, as infants tune
speci?cally to the correspondences between human vocalizations
and faces (11–14). Perceptual tuning effects like these, ubiquitous throughout the animal kingdom (15, 16), are adaptive: They
ensure that infants direct their attention increasingly toward the
communicative signals of our species and toward the individuals
who will serve as their communicative and pedagogical partners.
www.pnas.org/cgi/doi/10.1073/pnas.1221166110
However, to learn language, infants must do more than tune in
to the sounds of their native language. They must also discover
how these sounds are linked to meaning. Remarkably, infants
make rapid headway toward establishing just such a link. For
infants as young as 3 mo of age, human language evokes more
than simple listening preferences: it also engages infants’ core
cognitive capacities. Listening to human vocalizations engenders
in young infants more in-depth processing of the objects in their
environment and supports their formation of object categories
(17). Categorization, a building block of cognition, is inherent in
a wide range of processes including conceptual organization and
reasoning (18–20). In infants, a precocious link between language and object categorization was documented using a simple
object categorization task. Infants ?rst viewed a series of distinct
images from one object category (e.g., dinosaurs). Each image
was presented in conjunction with either a segment of human
speech or a sequence of sine-wave tones, matched precisely to
the human speech segment in mean frequency, amplitude, duration, and pause lengths. At test, all infants viewed two test
images, presented in silence: a new member of the now-familiar
category (a dinosaur) and a member of a novel category (a ?sh).
Following the logic established for infant looking-time paradigms, if infants formed the object category (dinosaurs), they
were expected to distinguish the test images, expressing this
discrimination behaviorally with a reliable preference for either
the familiar or the novel image (21).
The results were straightforward. Infants hearing the tone
sequences failed to discriminate between the test images at any
age. In sharp contrast, infants hearing human speech successfully
formed the object category, expressing their distinction ?rst as
a familiarity preference (in 3-mo-old infants) and later as a
novelty preference (in 4- to 12-mo-old infants) (17, 22, 23). This
age-related shift is consistent with a systematic progression
documented in infancy research: familiarity preferences tend to
be expressed early (in very young infants and in older infants
before they have gained suf?cient familiarization), and novelty
preferences tend to be expressed later in development, or after
suf?cient familiarization (21, 24, 25). Although the precise
mechanism underlying this progression is not yet fully speci?ed,
advances in brain maturation, processing speed, and encoding
ef?ciency are implicated. These results documented that human
speech is not only a preferred signal, but also confers an adaptive
advantage: By 3 mo, infants are not only tuned to the communicative signals of their partners, but also to a principled and
surprisingly early link between these signals and the fundamental
cognitive process of categorization.
Author contributions: A.L.F., S.J.H., and S.R.W. designed research; A.L.F. and S.J.H. performed research; A.L.F. and S.J.H. analyzed data; and A.L.F., S.J.H., and S.R.W. wrote
the paper.
The authors declare no con?ict of interest.
*This Direct Submission article had a prearranged editor.
1
To whom correspondence should be addressed. E-mail: aferry@sissa.it.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.
1073/pnas.1221166110/-/DCSupplemental.
PNAS | September 17, 2013 | vol. 110 | no. 38 | 15231–15235
PSYCHOLOGICAL AND
COGNITIVE SCIENCES
Language is a signature of our species and our primary conduit for
conveying the contents of our minds. The power of language
derives not only from the exquisite detail of the signal itself but
also from its intricate link to human cognition. To acquire a
language, infants must identify which signals are part of their
language and discover how these signals are linked to meaning. At
birth, infants prefer listening to vocalizations of human and
nonhuman primates; within 3 mo, this initially broad listening
preference is tuned speci?cally to human vocalizations. Moreover,
even at this early developmental point, human vocalizations
evoke more than listening preferences alone: they engender in
infants a heightened focus on the objects in their visual environment and promote the formation of object categories, a fundamental cognitive capacity. Here, we illuminate the developmental
origin of this early link between human vocalizations and cognition.
We document that this link emerges from a broad biological template
that initially encompasses vocalizations of human and nonhuman
primates (but not backward speech) and that within 6 mo this link
to cognition is tuned speci?cally to human vocalizations. At 3 and
4 mo, nonhuman primate vocalizations promote object categorization, mirroring precisely the advantages conferred by human
vocalizations, but by 6 mo, nonhuman primate vocalizations no
longer exert this advantageous effect. This striking developmental
shift illuminates a path of specialization that supports infants as
they forge the foundational links between human language and
the core cognitive processes that will serve as the foundations
of meaning.
This evidence is intriguing, but it leaves open a key developmental question: What is the developmental origin of this link?
Is the link speci?c to human vocalizations from the start, or does
it derive from a broader template, perhaps one that initially also
encompasses the vocalizations of nonhuman primates? Here, we
address this question directly. To do so, we traced the effect of
introducing two new auditory signals—a nonhuman primate
vocalization and backward human speech—on infants’ object
categorization over the ?rst 6 mo of life.
Experiment 1: Nonhuman Primate Vocalization
If the link between human language and cognition emerges from
a broader template, then the vocalizations of nonhuman primates
may initially confer the same adaptive advantage as human
vocalizations.
Thirty-six infants participated, 12 at each of three ages (3, 4,
and 6 mo old). We adapted the categorization task described
earlier (17, 23), this time accompanying each of the familiarization images with a vocalization of a blue-eyed Madagascar
lemur (Eulemur macaco ?avifrons) (Fig. 1). By 3 mo, infants
discriminate vocalizations of humans from those of nonhuman
primates (1, 14). We selected a lemur vocalization because although it differs distinctly from human vocalizations, it nonetheless shares certain acoustic properties with infant-directed
speech. More speci?cally, the lemur vocalization that we selected falls naturally within the mean frequency range of infantdirected human speech and is comparable in duration to the
infant-directed speech segments that were presented to infants in
previous object categorization tasks (17, 22, 23; Audio File S1).
At test, infants viewed two images simultaneously: a new member of the familiar category (e.g., a new dinosaur) and a member
of a novel category (e.g., a ?sh), presented in silence. We recorded
infants’ looking time to each image.
At 3 and 4 mo, infants’ responses to the lemur vocalization
mirrored precisely their responses to human vocalizations (17),
reliably distinguishing the novel from familiar test images.
Infants exhibited familiarity preferences at 3 mo [t(11) = -3.427,
P = 0.006] and novelty preferences at 4 mo [t(11) = 2.693, P =
0.021] (Fig. 2). However, by 6 mo lemur vocalizations no longer
exerted this facilitative effect [mean = 0.52, SD = 0.07, t(11) =
1.039, P = 0.321] (Fig. 2). An ANOVA documented this significant effect of age [F(3,26) = 13.702, P < 0.001].
A series of supplementary analyses compared infants’ responses
to lemur vocalizations (reported here) and human speech [reported previously (17), using the same inclusion criteria]. First,
we compared 3- and 4-mo-olds’ responses to human speech and
lemur vocalizations directly. Infants responded identically to
Fig. 1. Experimental design. During the familiarization phase, each infant
viewed eight different exemplars, presented sequentially, in conjunction
with either the lemur vocalization (experiment 1) or backward speech (experiment 2). During the test phase, each infant viewed images from the
familiar and novel categories, presented simultaneously in silence.
15232 | www.pnas.org/cgi/doi/10.1073/pnas.1221166110
Fig. 2. Infants’ responses to lemur vocalizations (experiment 1) and backward speech (experiment 2). At 3 and 4 mo, infants hearing lemur vocalizations were not only more likely than chance, but also more likely than
those hearing backward speech, to discriminate between the novel and familiar test objects; at 6 mo, neither lemur vocalizations nor backward speech
supported object categorization. For the purpose of comparison, we also
show infants’ responses to human vocalizations (e.g., “Look at the modi!”)
and to pure sine-wave tone sequences [e.g., 400- or 800-Hz tones; matched
to the human vocalization stimuli for mean frequency, duration, and pause
length (17, 23)]. Error bars represent ±1 SEM. Signi?cant differences between preference score and chance performance (0.50) are marked by an
asterisk (P < 0.05).
these two conditions [F(1,42) = 0.004, P > 0.05]. Second, we
examined individual infants’ responses to these vocalizations.
The results were striking: 92% of the 3-mo-olds hearing lemur
vocalizations (and 90% of those hearing human speech) exhibited
familiarity preferences (P = 0.006, binomial comparison); 83% of
the 4-mo-olds hearing lemur vocalizations (and 83% hearing human speech) exhibited novelty preferences (P = 0.039). Third,
strong correlations between infants’ age and preference scores,
documented previously in infants’ responses to human speech
[r(20) = 0.61, P < 0.05], were echoed here in infants’ responses to
lemur vocalizations [r(22) = 0.60, P < 0.05] (Fig. 3A). Finally, to
gain insight into the shift from familiarity to novelty preferences
at 3 and 4 mo, we examined the performance of an additional
group of infants: 4-mo-olds who heard lemur vocalizations but
were excluded from the main analyses because they attended
insuf?ciently to the familiarization images. These infants, like
their 4-mo-old counterparts who heard human speech but who
also accrued minimal exposure to the familiarization images,
exhibited a signi?cant familiarity preference [t(10) = -1.935,
P = 0.041, one-tailed]. The ?nding that 4-mo-olds with minimal
exposure to the familiarization performed identically to their more
attentive 3-mo-old counterparts suggests that the systematic shift
from familiarity to novelty preference in this task may be mediated
by infants’ processing and encoding of the materials, rather than
by their maturational state. Together, these analyses highlight
the compelling parallels between 3- and 4-mo-olds’ responses to
human speech and lemur vocalizations.
These results reveal that the link between human language
and object categorization, evident at 3 mo of age, derives from
a broader template that initially encompasses vocalizations of
human and nonhuman primates and is rapidly tuned speci?cally
to human vocalizations. However, what is the best account of this
phenomenon? Is the facilitative effect conferred by lemur (and
human) vocalizations speci?c to primate vocalizations? Or is it
a consequence of the acoustic complexity of these vocalizations,
especially compared with sine-wave tones? After all, it is well
Ferry et al.
Fig. 3. Correlations between age (in days) and preference score for infants
hearing (A) lemur vocalizations and (B) backward speech. For the purpose of
comparison, we also show the correlations for the human vocalization and
sine-wave tone conditions (17). Signi?cant correlations are marked by an
asterisk (P < 0.05).
documented that infants’ attention and arousal are enhanced in
the context of complex acoustic stimuli (26, 27).
Experiment 2: Backward Human Speech
To adjudicate between these alternatives, we presented another
group of 36 infants (12 per age group) with backward speech in
the context of the same object categorization task described
earlier. In fact, we presented the same segment of human speech
from ref. 17, but played it backward (Audio File S2). This segment
provides an ideal point of comparison, for although backward
speech is identical to forward speech in perceptual complexity, it
violates fundamental acoustic properties of forward speech, is
processed in different brain regions than forward speech from
birth, and is impossible to produce with a mammalian vocal tract
(3, 28). We reasoned as follows: If the cognitive advantage conferred by lemur (and human) vocalizations is a general consequence of young infants’ heightened attention in the context of
complex acoustic stimuli, then 3- and 4-mo-old infants hearing
backward speech should also successfully form object categories.
However, this was not the case (Fig. 2). Instead, infants hearing
backward speech failed to form object categories, performing
at chance levels at each age: 3 mo [t(11) = 0.504, P = 0.624], 4 mo
[t(11) = -0.212, P = 0.836], and 6 mo [t(11) = 0.280, P = 0.280].
An ANOVA comparing infants’ responses at each age to lemur
vocalizations (experiment 1) and backward speech (experiment
2) revealed a signi?cant interaction [F(5,66) = 5.021, P = 0.009]:
although infants’ responses to these two signals differed at 3
and 4 mo, by 6 mo, infants’ responses to these signals were
indistinguishable.
Finally, a supplementary series of analyses revealed that
infants’ responses to backward speech (reported here) mirrored
their responses to sine-wave tone sequences [reported previously
(17), using the same inclusion criteria]. An ANOVA revealed no
main effects or interactions between infants’ responses to these
signals (all P > 0.05). Moreover, as was the case for tone
Ferry et al.
General Discussion
The current work reveals that tuning processes not only guide
human infants to the communicative signals of our species, but
also support the very ?rst links between these signals and the
core cognitive capacities that will ultimately constitute the foundations of meaning. We document that a link between human
language and object categorization, evident at 3 mo of age, derives
from a broader template that initially encompasses vocalizations
of human and nonhuman primates and is rapidly tuned speci?cally
to human vocalizations. This work sheds light on a path of developmental specialization that supports infants’ ?rst steps toward
establishing the links between human language and cognition that
are the hallmark of the human mind and the primary conduit for
the cultural transmission of knowledge.
This work provides unique insight into the processes that undergird infant language development, concept development, and
the links between them. First, we document that in human infants,
the fundamental process of developmental narrowing extends
well beyond purely perceptual discriminations and preferences
(1, 5–7). Perceptual narrowing is well underway within the ?rst
months of life. For example, neonates’ listening preferences,
which include both human and nonhuman primate vocalizations,
give way to a strong preference for human over nonhuman
vocalizations by 3 mo (1, 5). However, despite their clearly-tuned
preference for human vocalizations, nonhuman primate vocalizations conferred precisely the same conceptual advantages at
3 and 4 mo as human vocalizations, an advantage that by 6 mo
was tuned speci?cally to human vocalizations. This constitutes
evidence that the power of developmental tuning reaches beyond perceptual capacities alone to support the establishment
of foundational cross-modal links between human language and
the core cognitive processes that will serve as the foundations
of meaning.
Second, we identify very detailed parallels in young infants’
responses to human and nonhuman vocalizations. Despite their
preference for human vocalizations (1) and the vast differences
in their prior exposure to these stimuli, infants hearing human
and nonhuman vocalizations revealed the same, precisely timed
shift from familiarity preferences (at 3 mo) to novelty preferences (at 4 mo) (Figs. 2 and 3). This parallel, striking in itself,
also sets limits on the role of prior exposure in infants’ processing
speed, encoding ef?ciency and their expression of familiarity or
novelty preferences (21, 24, 25).
Third, these ?ndings offer insight into the mechanisms underlying infants’ initially broad link between language and object
categorization (17). Certainly, experience with human language
is instrumental in infants’ ?rst months of life (1, 5, 7, 29). Infants
may quickly learn that human language heralds interesting visible events or brings with it rewarding affective experiences.
Associations like these would likely engender in infants heightened attention in the context of human vocalizations. However,
we document here that lemur vocalizations—an entirely unfamiliar signal—engender the same facilitative effect as human
vocalizations at 3 and 4 mo. We therefore conclude that the
starting point for human infants’ link between language and core
cognitive processes cannot be derived from learning alone.
These ?ndings also open several avenues for additional research. First, it will be important to discover the boundary conditions on the signals that initially engage infants’ cognitive
processes, including object categorization. Is this link suf?ciently
broad to include naturalistic vocalizations beyond those of our
closest genealogical cousins, or is it restricted to primates, whose
vocalizations may be perceptually just close enough to our own
to serve as early candidates for the platform on which human
PNAS | September 17, 2013 | vol. 110 | no. 38 | 15233
PSYCHOLOGICAL AND
COGNITIVE SCIENCES
sequences, there was no correlation between infants’ age and
preference scores for backward speech [r(22) = -0.18, P > 0.05]
(Fig. 3B).
language is launched? Does the initial link encompass communicative signals from other modalities (e.g., signed languages), or
does it privilege vocalizations from the start (30, 31)? Additional
research will also be required to ascertain whether the tuning
process that we have documented here has begun even earlier, in
infants younger than 3 mo of age. It will also be important to
investigate whether and how infants’ exposure to multiple languages in?uences the course of this developmental progression
(32, 33).
Another key question concerns the boundary conditions on
the kinds of cognitive capacities that are initially engaged by
human and nonhuman vocalizations. The evidence reported here
documents an advantageous effect of human and nonhuman
primate vocalizations on one fundamental cognitive process:
object categorization. Do vocalizations initially support other
cognitive processes (e.g., object individuation), or does the link
to cognition initially privilege object categorization? Finally,
additional work will help to reveal whether and how the striking
developmental effects documented here are gated by experience, maturation, or an interaction between these twin engines
of development.
Methods
Participants. Seventy-two healthy, full-term infants from predominantly
college-educated, white families living in the Greater Chicago Area participated. All procedures were approved by the Northwestern University Institutional Review Board and informed consent was obtained from the
parents of all infants. There were 36 infants per experiment divided into 12
infants per age: 3-mo-olds (2 mo, 11 d to 3 mo, 20 d; mean = 3 mo, 2 d), 4-moolds (3 mo, 25 d to 4 mo, 16 d; mean = 4 mo, 6 d), and 6-mo-olds (5 mo, 18 d
to 6 mo, 24 d; mean = 6 mo, 3 d). Infants who devoted insuf?cient attention
(less than 50% overall) to familiarization images (43, distributed evenly across
conditions and sex) were analyzed separately. Additional infants were excluded for fussiness (10) and parental interference (4). Excluded infants did
not differ in either age or sex from included infants; this exclusion rate is
consistent with prior work (17, 23).
Parents were asked whether their infant was exposed to any language(s)
other than English and the percentage of time another language was spoken
to the infant. Approximately 70% of the infants were raised in a monolingual
environment. The remaining infants, who were exposed to more than one
language (at least 20% of the time), were evenly distributed across ages and
experiments, and performed comparably to those exposed only to English.
Infants with bilingual exposure had a variety of linguistic backgrounds including exposure to Spanish (~50%) and a variety of other languages. This
variation in language exposure prevented us from identifying effects of
monolingual versus bilingual exposure in this experiment.
images varied in color; within each test pair, images were matched in color.
Images (~15 cm2) were projected onto a white screen ~75 cm from the
infant’s eyes.
Auditory. A vocalization of a blue-eyed Madagascar lemur (E. macaco ?avifrons) and a segment of backward speech [a labeling phrase from ref. 17,
played in reverse], each ~2.2 s, were played from a hidden speaker, located
56 cm below the center of the screen. (Audio Files S1 and S2).
Procedure. Infants were seated on a parent’s lap, facing a wooden puppet
stage (located 93 cm above the ?oor; the front opening was 61 cm high ×
106 cm wide). The visual images were projected onto a screen resting on the
stage ?oor. The left and right positions of the projected images were separated by 11 cm. Parents were instructed not to in?uence their infant’s attention. Infant behavior was recorded by a video camera (hidden 12 cm
below the screen). During the task, two trained coders, blind to condition
assignment, recorded infants’ visual attention; reliability between these
coders was 90%.
Familiarization trials. Visual stimuli (either dinosaurs or ?sh) were presented on
alternating sides of the screen (20 s each). Auditory stimuli (either lemur
vocalization or backward speech) were presented as each image appeared
and repeated 8 s later.
Test trials. Each test pair appeared side-by-side, in silence, and remained visible
until the infant accumulated 10 s of looking at the test images. [Note: Three
infants in each experiment, who looked exclusively at one test image for
10 s, were presented with a second test trial with new images. In accordance
with previous implementations of this paradigm (17), the analyses reported
here include these infants’ performance on the second test trial; the same
pattern of results emerges, whether or not these infants are included.]
Across infants, left/right positions of the ?rst familiarization image and the
test images were counterbalanced.
Coding. Infants’ looking time at test served as our dependent measure. For
each infant, we calculated a preference score (looking time at novel image/
looking time at both images). Test trials were coded of?ine using frame-byframe software (34). Reliability between two trained observers, blind to
condition, was 91%.
Infants’ looking time during familiarization (coded online) revealed no
differences across age or experimental condition (P > 0.05). This provides
assurances that any differences between experiments cannot be attributed
to differences in attention to the stimuli during familiarization.
Stimuli. Visual. Line-drawn images of dinosaurs and ?sh formed two eightitem familiarization sets and two test pairs. Within each familiarization set,
ACKNOWLEDGMENTS. We are indebted to the parents and infants for
participating; to E. Brannon and the Duke University Primate Center for providing the lemur vocalization; to members of the S.J.H. laboratory for assistance in data collection; to S. Arunachalam, K. Byers-Heinlein, B. Ferguson,
D. Gentner, M. Havy, J. R. Hochmann, and E. Leddon for discussion; and to
the Prearranged Editor for suggestions. This work was supported by National
Science Foundation (NSF) Grant 0950376 (to S.R.W.), NSF Grant 0114948
(to S.J.H.), and European Research Council 269502, which supported A.L.F.
while this manuscript was under review.
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2. Kuhl PK (2004) Early language acquisition: Cracking the speech code. Nat Rev Neurosci 5(11):831–843.
3. Mehler J, et al. (1988) A precursor of language acquisition in young infants. Cognition
29(2):143–178.
4. Shultz S, Vouloumanos A (2010) Three-month-olds prefer speech to other naturally
occurring signals. Lang Learn Dev 6(4):241–257.
5. Vouloumanos A, Werker JF (2004) Tuned to the signal: The privileged status of speech
for young infants. Dev Sci 7(3):270–276.
6. Werker JF, Tees RC (1984) Cross-language speech perception: Evidence for perceptual
reorganization during the ?rst year of life. Infant Behav Dev 7(1):49–63.
7. Werker JF, Yeung HH, Yoshida KA (2012) How do infants become experts at nativespeech perception? Curr Dir Psychol Sci 21(4):221–226.
8. Di Giorgio

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