Functional exibility of infant vocalization and the

emergence of language
D. Kimbrough Ollera,b,c,1, Eugene H. Budera,b, Heather L. Ramsdelld, Anne S. Warlaumonte, Lesya Chornaf,
and Roger Bakemang
a
School of Communication Sciences and Disorders, University of Memphis, Memphis, TN 38105; bInstitute for Intelligent Systems, University of Memphis,
Memphis, TN 38152; cThe Konrad Lorenz Institute for Evolution and Cognition Research, A-3422 Altenberg, Austria; dDepartment of Communication Sciences
and Disorders, Idaho State University, Pocatello, ID 83209; eCognitive and Information Sciences, University of California, Merced, CA 95343; fMathematics
Department, Milwaukee School of Engineering, Milwaukee, WI 53202; and gDepartment of Psychology, Georgia State University, Atlanta, GA 30303

Edited* by E. Anne Cutler, Max Planck Institute for Psycholinguistics, Heilig Landstichting, The Netherlands, and approved March 7, 2013 (received for review
January 8, 2013)

We report on the emergence of functional exibility in vocalizations guided by a common set of infrastructural principles, with similar
of human infants. This vastly underappreciated capability becomes foundational steps (such as canonical babbling, joint attention,
apparent when prelinguistic vocalizations express a full range of and so on) being required in both cases for subsequent language-
emotional contentpositive, neutral, and negative. The data show related advancement (1214).
that at least three types of infant vocalizations (squeals, vowel-like We continue to be inuenced by evo-devo logic and seek the
sounds, and growls) occur with this full range of expression by 34 deepest foundations in our communicative phylogenetic history
mo of age. In contrast, infant cry and laughter, which are species- and the earliest points of departure in evolution and development
specic signals apparently homologous to vocal calls in other pri- between humans and other animals, especially our closest pri-
mates, show functional stability, with cry overwhelmingly express- mate relatives. Our report focuses on a capability appearing
ing negative and laughter positive emotional states. Functional earlier in human development than any of those listed above, one
exibility is a sine qua non in spoken language, because all words that scarcely has been considered in work on origins of language.
or sentences can be produced as expressions of varying emotional
Functional exibility (15) is evidenced in infants when a single
states and because learning conventional meanings requires the
vocal category expresses positive, negative, and neutral emotional
states on different occasions. This vocal capability can be imple-
ability to produce sounds that are free of any predetermined func-
mented with any word or sentence in mature humans and is re-
tion. Functional exibility is a dening characteristic of language,
quired for language because learning of culturally specic word
and empirically it appears before syntax, word learning, and even
meanings logically requires production of sounds that have no
earlier-developing features presumed to be critical to language (e.g.,
species-universal functions or meanings. We must be able to use
joint attention, syllable imitation, and canonical babbling). The ap- any word or sentence with widely varying illocutionary forces (16),
pearance of functional exibility early in the rst year of human life a fact that implies the ability to express a positive state as seen in
is a critical step in the development of vocal language and may have joy or celebration, a negative state as in complaint, or an emo-
been a critical step in the evolution of human language, preceding tionally neutral state as can occur in factual description, all with
protosyntax and even primitive single words. Such exible affect the very same lexical or syntactic content. Thus, the sentence the
expression of vocalizations has not yet been reported for any non- airplane is arriving (or the single word airplane) can be used in
human primate but if found to occur would suggest deep roots for these and many other ways: (i) in celebration of the landing of
functional exibility of vocalization in our primate heritage. a ight, (ii) in complaint about the tardiness of a ight, or (iii) in
mere description of a landing. The syntax and semantic content
| |
evolution of language infant communication exibility in (or meaning) is the same in all three communicative acts, but the
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communication language development primate communication illocutionary content (or use) is vastly different. This sort of
exibility of use is not a dispensable side issue in language ca-
pability but rather is a fundamental requirement of all normal
R esearch on evolution and development of language has been
devoted primarily to syntax, the uniquely human capacity to
produce well-formed complex sentences (14). Additional work
human communication.
Functional exibility in vocalizations of infants as presented
has targeted the emergence of simpler communicative structures here implies that change in facial affect associated with any
and thus has shifted attention back in evolutionary time to an infant vocal category should correspond to reliably observable
earlier possible split of hominins from the primate background. and predictable change in (i) the corresponding infant com-
For example, research has considered the presumably earlier municative act (e.g., the illocutionary force complaint should
evolution of simple sentences or protosyntax (5). Other work be associated with utterances showing negative facial affect,
inuenced by recent trends in evolutionary developmental biology whereas exultation should be associated with utterances
(evo-devo) (6, 7) has focused on infrastructure for language, in- showing positive affect) and (ii) caregiver action in response to
voking capabilities logically more foundational even than proto- the infant social act (e.g., the perlocutionary effect of feeding
syntax and presumably moving the communicative differentiation an infant should occur with high likelihood when a negative
of hominins from other primates much farther back. For example, vocalization is interpreted by a caregiver as indicating hunger,
symbolic expression in single words beginning in modern human
development at about 12 mo is a precursor to even the simplest
syntax (8). Moving the evolutionary focus even farther back in Author contributions: D.K.O. and E.H.B. designed research; D.K.O., E.H.B., H.L.R., A.S.W.,
time, joint attentioninfant pointing with gaze alternation be- and L.C. performed research; D.K.O., E.H.B., L.C., and R.B. analyzed data; and D.K.O., E.H.B.,
H.L.R., A.S.W., and R.B. wrote the paper.
tween an object and an adult interactor, occurring before the end
of the rst yearis deemed a critical precursor to words (9). Conict of interest statement: The authors declare no conict of interest (such as dened
by PNAS policy).
Similarly, canonical babbling (onset at about 7 mo) is a crucial step
toward verbal vocabulary because development and imitation of *This Direct Submission article had a prearranged editor.

canonical syllables (e.g., baba) is required for extensive word Freely available online through the PNAS open access option.
learning (10, 11). Recent reasoning inuenced by evo-devo con- 1
To whom correspondence should be addressed. E-mail: koller@memphis.edu.
verges on the contention that the evolution of language in homi- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.
nins and the development of language in modern infants are 1073/pnas.1300337110/-/DCSupplemental.

63186323 | PNAS | April 16, 2013 | vol. 110 | no. 16 www.pnas.org/cgi/doi/10.1073/pnas.1300337110

and continuation of protoconversation should occur when an less related to our primate heritage and arguably more related to
infant vocalizes in a positive afliative manner). The distinction speech, emotional expression can change from utterance to
between illocution and perlocution, drawn from Austin (16) utterance. The evidence also shows that these changes in affect
and long used to advantage in descriptions of human infant correspond predictably to functional changes in classes of illo-
communication (8, 17, 18), corresponds to a sender/receiver dis- cutionary force and of perlocutionary effect of infant utterances.
tinction in literature on animal communication, where it is em- The protophones considered in the present research are squeals,
phasized that senders and receivers do not always have the same vowel-like sounds (hereafter vocants), and growls (SI Appendix,
interests (19). For details on our use of the terms illocution and Supporting Background, Characteristics of the protophones). These
perlocution and our reasoning about their relation to the sender/ protophones require phonation (i.e., voicing) with or without
receiver distinction, see SI Appendix, Supporting Background: Affect supraglottal articulation; hence they may or may not contain dis-
and context in the judgment of function in vocalizations. tinguishable consonants and vowels. Protophones occurring before
It has been argued that, on balance, both senders and receivers canonical babbling cannot be transcribed sensibly in the In-
must benet from signal transmission for stable signals to evolve ternational Phonetic Alphabet (48), because they generally do not
(20). In accord with this reasoning, illocutionary acts of senders on contain well-formed and distinguishable consonants and vowels.
balance must predict perlocutionary effects in receivers, and the Precanonical protophone description instead requires ethological
overall effect of signaling must be benecial to both parties. This categorization (similar to that used in assessing nonhuman vocal-
reasoning implies, as indicated above, that particular facial affect izations) with intuitive listening, categorizations that can be sup-
expressions through infant vocal categories should (if they have ported by acoustic analysis (SI Appendix, Supporting Fig. 1), and
consistent pragmatic functions) correspond to particular classes of statistical modeling (49). The protophone types appear to emerge
illocutionary forces and perlocutionary effects. An extensive lit- during active infant vocal exploration (12), and this exploration
erature in human caregiverinfant interaction (2127), especially may account for the fact that the categories are fuzzy, just as hand
in the eld of attachment (2832), suggests that precisely this sort and arm movements constitute fuzzy categories with substantially
of correspondence between perceived affect and functions of in- variable trajectories during infant development of reaching and
fant communications occurs in real parentinfant interaction. grasping (5052). Despite this fuzziness, key protophones (including
Infants express affect, and parents interpret that affect function- squeals, vocants, and growls) are reported spontaneously by parents
ally, responding with encouragement and/or continuation of and are consistently recognized by ethologically oriented research-
pleasurable interaction when an infant interacts with positive af- ers of infant vocalization (10, 5355).
fect but responding with physical attempts to change the situation The existence of functional exibility in human infant vocaliza-
by comforting or distracting and/or talking about a possible tion as well as its signicance as a foundation for language has
change in the situation when an infant expresses negative affect. been largely ignored in the past because research on vocal de-
The caregiver also responds to the infant with her own emotional velopment has focused heavily on discerning meaning in infant
expressions and affect, and thus such interaction has been thought expression and thus on determining consistent rather than exible
to constitute a mutual emotional regulatory system (27, 33) with functions (especially expressions of emotional state) for the seem-
benets to both parties in health and well-being. ingly disorganized vocalizations of infancy (56, 57). There previ-
The exibility of affect expression and associated functions for ously has been no direct comparison illustrating the functional
linguistic units such as words stands in contrast with patterns
exibility of protophones versus the functional xedness of cry and
reported in some of the literature on nonhuman primate vocaliza-
laughter. This is a key gap because the demonstration of this dif-
tion where each vocal type or call has been portrayed as having
ference could illustrate straightforwardly the very early emergence
a consistent function (SI Appendix, Supporting Background). This
of a vocal capability present in and required for language and not
idea is rooted in the classical ethologists notion of xed signals
(34, 35), with each call seen as naturally selected to express a par- yet reported in other primates.
ticular emotional or arousal state, implying transmission of a corre- Results
sponding illocutionary force along with predictable perlocutionary
reactions from listeners. Given this view, one would not expect in- We analyzed longitudinal recordings of vocal interactions and play
dividual nonhuman primate calls to change valence from positive to for nine infants at three ages in the rst year. Acoustic analysts
neutral to negative on different occasions of use. located 6,995 utterances, which were then coded for vocal type
In recent years, however, research has suggested that animal (cry, laugh, squeal, vocant, and growl) based on audio presentation
calls may be more functionally exible than the classical ethologists only and for facial affect (positive, neutral, and negative) based on
imagined. For example, across development from infancy, chim- video only (SI Appendix, Supporting Methods and SI Appendix,
panzee grunts have been shown to occur in increasingly variable Supporting Table 1). Fig. 1 illustrates that all the protophones
contexts that may suggest variable functions (36, 37). Additional showed predominant neutrality in facial affect (mean = 64%),
sounds in chimpanzees and other primates later in life also have suggesting that, in protophones, infants possess the requirement of
been shown to be used in a variety of contexts (38). However, the language for exible detachment of vocalization from particular
research has not yet shown that such variations extend to the sort of emotions. Cries and laughs, in contrast, were rarely judged to be
functional exibility considered here, including variation in affect neutral in facial affect (mean = 4%). The gure also shows that
expression for a single call from positive to neutral to negative, nor cries were overwhelmingly deemed negative, whereas laughs were
has research illustrated that such variable affect in particular overwhelmingly deemed positive. In contrast, all the protophones
nonhuman primate calls corresponds to predictable variations in showed both considerable numbers of utterances with positive
illocutionary force or perlocutionary outcome. By providing a affect and considerable numbers with negative affect. For exam-
framework to evaluate quantitatively the possibility that functional ples of infant protophones illustrating functional exibility, see
vocal exibility occurs in infants, the present work may also provide SI Appendix, Supporting Methods and the audio/video examples
a basis for future research in nonhuman primates to quantify im- (Movies S1S19).
portant similarities or differences between humans and nonhu- Fig 2 illustrates that the distribution of protophone affect dif-
mans on this critical feature of linguistic communication and fered starkly from cry and laugh affect in six ways: Protophones
showed (i) more positivity than cry but (ii) less than laugh (Fig
PSYCHOLOGICAL AND

its development.
COGNITIVE SCIENCES

Considerable research has suggested that human infant cry 2A), (iii) more neutrality than either cry or (iv) laugh (Fig 2B),
and laughter are closely related in terms of form, function, and and (v) less negativity than cry but (vi) more than laugh (Fig 2C).
brain control mechanisms to species-specic calls of nonhuman These six patterns were seen at all ages and in all infants (SI
primates that may in fact be homologous with cry and laughter in Appendix, Supporting Figs. 6 and 7) and were supported statisti-
humans (3947). The evidence reported here, however, shows cally by highly signicant odds ratios (SI Appendix, Supporting
that in the protophones, the infant vocal types that seem to be Tables 2 and 3).

Oller et al. PNAS | April 16, 2013 | vol. 110 | no. 16 | 6319
 A phonation, and these more complex vocal patterns continued to
be expressed with a full range of facial affect.
Fig. 3 A and B demonstrate that facial affect expressed in
protophones corresponded predictably to illocutionary force
judgments based on simultaneous audio/video presentation.
Protophones categorized as showing pursuit of protoconversation
with the caregiver through comfortable vocal responsivity, imita-
tion, exultation, or initiation of interaction (the Converse group
of illocutionary functions) were strongly associated with positive
facial affect, whereas protophones interpreted as complaints or
pleas for help (the Complain illocutionary functions) corre-
B sponded systematically to negative facial affect. Fig. 3 C and D
similarly indicate that facial affect of protophones yielded
predictable perlocutionary outcomes also judged based on si-
multaneous audio/video presentation. Thus, positive affect
corresponded to caregiver encouragement of pleasurable vocal
Fig. 1. Frequency and proportion of occurrence of each vocal type. Data on interaction through imitation, celebration, smiling, and so on (the
nine infants in the rst year of life were collapsed across three observation Encourage perlocutionary group), whereas negative affect yiel-
periods. The emotional signals (cry and laughter) showed (A) proportions ded explicit spoken assessment by the caregiver of a possible
and (B) frequencies of occurrence with cries displaying overwhelmingly change in the physical situation or attempts to change the situation
negative and laughs positive facial affect. In contrast, the protophones or the interaction (the Change perlocutionary group). All the
(squeals, vocants, and growls), presumed to be precursors to speech, were all relations between affect and both illocutionary and perlocutionary
used exibly, showing primarily neutral facial affect and also presenting outcomes for Fig. 3 were supported by highly signicant odds ratios
numerous cases of both positive and negative affect. For description of the (P < 0.001), and all the protophones showed similar patterns of
vocal types, see SI Appendix, Supporting Background. Briey, squeals are relation between particular affect types and classes of both illo-
produced with very high pitch for the individual infant, vocants with mid- cutionary forces and perlocutionary effects. Additional data on
range pitch, and growls with harsh voice quality or low pitch. Positive,
affect and its relation to function are provided in SI Appendix,
negative, and neutral facial affect correspond roughly to smiling/grinning,
Results: The role of affect expression in the functional interpretation of
frowning/grimacing, and neither (see also SI Appendix, Supporting Methods:
Coding training and coding procedures for both vocal type and facial affect).
infant protophones and SI Appendix, Supporting Figs. 9 and 10.
Possible coder bias in the assessment of the relation between facial
affect and perlocutionary effect could be predicted if judgments of
As tabulated in Fig. 1, protophones occurred much more often perlocution were driven by attention to both video and audio of
than cry and laugh in our recordings, suggesting that vocalization both infant and parent. To determine if such bias could have been
even in the rst months of human life is not characterized pri- the source of the strong relation between facial affect and perlo-
cutionary effects, we compared results from two coders, one of
marily by predetermined emotional expression but rather by ex-
whom judged perlocutionary effects based on both audio and video
ploratory vocal freedom and exible expression, key foundations of the caregiver and infant, and the other of whom made judgments
for language. Moreover, the most commonly occurring vocal type based on caregiver utterances in audio alone, with no video and no
(vocant) was the one most commonly judged to be neutral in child voice included. Results from both coders (SI Appendix, Sup-
facial affect, suggesting again that these sounds reveal an emer- porting Fig. 10) showed, again with highly signicant odds ratios,
gent foundation for languagethe possibility that vocalizations that perlocutionary effect judgments corresponded as predicted to
can be detached from any particular emotional state. facial affect judgments.
The data for the 10- to 12-mo-olds showed that infants of- The consistency of the six patterns of difference in affect ex-
ten superimposed features of vocal quality corresponding to the pression across the protophones should not be taken to mean that
three protophones upon the more mature vocal patterns, in- systematic patterns of protophone affect expression were entirely
cluding canonical babbling; thus well-formed syllables were absent. Functional exibility, we reason, does not correspond to
produced in the oldest infants with squeal, vocant, or growl-like random action but rather to the potential for systematic, adaptive

Fig. 2. Quantitative illustration of the distinction in functional

exibility between protophones and cry/laugh. Key patterns for
protophones at all infant ages showed exibility, as is required in
speech, whereas cry and laugh showed consistent affect ex-
pression, as occurs in affectively charged vocalizations of other
primates. (A) Positivity in facial affect expression: Protophones
B C showed (i) far more positivity than cry but (ii) far less than laugh.
(B) Neutrality in facial affect expression: Protophones were (iii)
far more neutral than either cry or (iv) laugh. (C) Negativity in
facial affect expression: Protophones were (v) far less negative
than cry and were (vi) far more negative than laugh. Thus, the
results (supported strongly by odds ratios; see SI Appendix,
Supporting Results: Odds ratio analyses and SI Appendix, Sup-
porting Tables 23) illustrate that in the rst year, human infant
protophones show the kind of exibility in affect expression that
is required for speech; such exibility has not been reported as
yet in nonhuman primate vocalizations at any age.

6320 | www.pnas.org/cgi/doi/10.1073/pnas.1300337110 Oller et al.

Fig. 3. Effects of facial affect on illocutionary force and per-
locutionary effect of infant protophones. (A) Distribution of A C
protophones with varying facial affect across three illocu-
tionary groupings by proportion. (i) More than 80% of pro-
tophones with positive facial affect were coded as having
illocutionary forces supporting protoconversation with the
caregiver (e.g., initiating conversation, continuing conversa-
tion, expressing joy or exultation, imitating, and so on),
whereas (ii) protophones with neutral affect most often were
coded as indeterminate (e.g., they were not directed to the
caregiver, often being interpreted as vocal play), and (iii) those
with negative affect were coded 90% as complaints or pleas
for help. (B) Distribution of protophones with varying facial
affect across three illocutionary groupings by frequency of
occurrence. (C) Distribution of protophones with varying facial B D
affect across three perlocutionary groupings by proportion. (i)
The vast majority (88%) of protophones with positive facial
affect produced caregiver reactions encouraging proto-
conversation (e.g., calling to the infant, continuing conversa-
tion, praising, expressing joyful surprise, and so on), whereas
(ii) those with neutral affect yielded more than twice as many
encouragements as attempts to change the situation, along
with many responses coded as ambiguous, and (iii) 75% of
those with negative affect were responded to by explicit talk
about what might be wrong with the baby or by attempts to change the situation or interaction (picking the baby up, attempting to distract him/her,
soothing, and so on). (D) Distribution of protophones with varying facial affect across three perlocutionary groupings in frequency of occurrence. For details
see SI Appendix, Supporting Methods: Illocutionary force coding and perlocutionary force coding and SI Appendix, Supporting Results: The role of affect
expression in the functional interpretation of infant protophones, with SI Appendix Supporting Figs. 9 and 10.

patterning, as is required in speech. The three protophones, al- positivity in facial affect, and squeals also showed more than
though far more affectively exible than cry and laugh, each dis- expected negativity. Thus, squeals and growls were more likely
played consistent patterns in affect expression. Fig. 4 compares the than vocants to be used in expressing extremes of emotion, even
observed positive, neutral, and negative counts for each proto- though all three protophone types were used in substantial num-
phone with counts expected by an independence model assuming bers to express both positivity and negativity.
identical distribution of facial affect types across protophones. The Despite the systematicity of affect expression in protophones
independence model failed to t; 2(4, n = 6,535) = 148, P < 0.001. for data aggregated across infants (Fig. 4), contingency-table
Adjusted residuals, approximating a unit normal distribution, analysis revealed that the patterns varied by individual. Fig. 5
revealed that the observed frequencies often differed by several illustrates nine unique patterns, thus revealing an additional
SDs from the frequencies expected by the independence model, kind of functional exibilitysystematic individual variation
and the deviations differed notably across protophones. For ex- in affect expression for protophones. Cry and laugh, on the
ample, vocants were 9.1 SD more likely than expected to be facially other hand, showed no such individual variation: all infants
neutral, whereas squeals were 10.0 SD less likely than expected to displayed strong positivity in laugh and negativity in cry (SI
be neutral. Both squeals and growls showed more than expected Appendix, Supporting Results: Additional contingency table analyses,

Fig. 4. Observed and expected counts for each facial affect

type, separately by protophone. Comparison of observed and A
expected counts, aggregated across observations of nine
infants during the rst year of life, illustrates that functional
exibility does not indicate lack of differentiation but instead
indicates systematic exibility in affect expression by infants
across the three protophones, the presumed precursors to
speech. Darker right-hand bars indicate observed counts of
positive, neutral, and negative facial affect for each proto-
phone. Lighter left-hand bars indicate counts expected if facial
affect were independent of protophone type. Insets with
a light gray background show adjusted residual values (some B C
positive, some negative) corresponding to counts signicantly
greater than or less than expected (P < 0.05). (A) Compared
with the counts generated by the independence model,
vocants were signicantly more likely to be neutral (9.1 SD
more than expected) and were signicantly less likely to be
either positive or negative. (B) In contrast, squeals were more
likely than expected to be both positive and negative and
were less likely to be neutral, and (C) growls were more likely
to be positive than expected by chance. These outcomes il-
PSYCHOLOGICAL AND
COGNITIVE SCIENCES

lustrate that although protophones manifest functional exi-

bility (all were predominantly neutral, and all also showed substantial numbers of cases of positive and negative expression), they were used affectively in
systematically different ways with respect to each other. We reason that the ability to produce the same vocalization with differing affective character is
a necessary foundation for language, but a random distribution of facial affect with respect to vocalizations would constitute a restriction on the very
exibility that is needed for adaptation of vocal expression to specic contexts and communicative needs. Thus, the systematic patterns in the data
are consistent with the idea that infants control affective expression in protophones rather than producing facial affect in random association with the
protophones.

Oller et al. PNAS | April 16, 2013 | vol. 110 | no. 16 | 6321
 and perhaps of individual variation. Facial affect agreement for
the reliability coders observing only video showed = 0.73 with
respect to the master coding.
Observer agreement regarding the six patterns of functional
exibility differentiating protophones from cry and laugh was
conrmed by an analysis of the same sort displayed in Fig. 2. All
six patterns applied both to reliability coders and to the master
coding, with protophones showing massively greater exibility of
facial affect than cry and laugh (SI Appendix, Supporting Fig. 8),
patterns again strongly supported by statistically signicant
odds ratios.

Discussion
All the results converge on stark differentiation of the functional
exibility of protophones from the xedness of cry and laughter
Fig. 5. Individual differences in facial affect expression through the pro-
by age 34 mo in human infants (SI Appendix, Supporting Fig. 7).
tophones. Log-linear analysis of 3 3 tables for frequency of occurrence of The evidence suggests that the early protophones have a special
protophones by facial affect (see text and SI Appendix, Supporting Results: role in language development and evolution because they are the
Log-linear analyses) revealed signicant differences among the nine infants. rst sounds to be free of specic xed functions and thus reveal
At the same time, log-linear analysis of 2 3 tables for cry and laugh the opening of a door to the exibility required for language.
revealed no such individual differences (because cries were negative and Because vocal exibility is a logical requirement for even the
laughs positive for all infants who produced them; see SI Appendix, Sup- most rudimentary speech development, the evolution of language
porting Table 4). This gure provides a quantitative illustration of individual may have required the evolution of vocal exibility such as seen in
differences in patterns of functional exibility across infants for the proto- these human infants at a very early stage among hominins. An
phones based on Contingency Table Analysis. Each square represents one of intriguing question is whether the evolution of such vocal exi-
the nine infants. Cells within squares represent associations of protophones bility was one of the rst steps in communicative differentiation of
with facial affect types. Darker cells indicate positive adjusted residuals the hominin line from that of other primates, especially our
(observed counts greater than expected); a plus indicates an adjusted re- closest relatives, chimpanzees and bonobos. Research often has
sidual greater than +1.96. Lighter cells indicate negative adjusted residuals
tended to emphasize limitations in exibility of vocal communi-
(observed counts less than expected); a minus indicates an adjusted residual
cation in nonhumans and thus to suggest that the type of func-
less than 1.96. The gure indicates that each of the nine infants showed
a unique pattern of adjusted residuals. These signicant individual differ-
tional exibility reported here for human infants may be absent or
ences suggest that the functional exibility of infants is not the result of an
present only to a more limited extent in nonhumans. However,
innate tendency specifying use of protophones in terms of affect (as appears the precise studies that would need to be done for quantitative
to occur with cry and laugh) but rather that infants possess an inclination to comparison of nonhuman primate vocal exibility with the kind
explore vocalization in protophones and to be expressive with them, each of exibility indicated by the present results for human infants
infant thus developing a personalized path toward a capacity for speech (see have not yet been conducted. Usually primatologists assess
also SI Appendix, Supporting Results: Additional contingency table analyses). function by reasoning from contexts of use. Nonhuman primates
often use a particular call in substantially varying contexts (37,
38), but such variation still may be consistent with a generalized
especially SI Appendix, Supporting Table 4). Log-linear analysis function that transcends the different contexts (58, p. 185). A
conrmed statistically signicant individual differences for pro- key goal is to determine the generalized function or functions that
tophones but not for cry and laugh (SI Appendix, Supporting each call may serve, both in terms of illocution and perlocution.
Results: Log-linear analyses, and SI Appendix, Supporting Tables However, direct functional assessment will be difcult to apply
57), illustrating again the affect exibility of protophones in consistently across species because of major differences in life-
sharp contrast with the affect rigidity of cry and laugh. styles. An approach focusing on affect expression may offer
Perspective on protophones occurring in different contexts is a useful rst step toward optimal cross-species comparisons.
supplied in SI Appendix, Supporting Results: Robustness of func- Thus, far, we do not know whether or to what extent nonhuman
tional exibility of protophones across contexts, where SI Appendix, primate vocalizations may show reversals of valence in affect ex-
Supporting Fig. 11 illustrates that vocalizations occurring both pression (and corresponding reversals of function) on different
during and not during gaze toward another person showed occasions, i.e., the sorts of reversals we have documented here for
a strong pattern of variation in affect, similar to that reported in the human infant. A recent review emphasizes that little effort has
Fig. 1. Similarly SI Appendix, Supporting Fig. 12 provides illus- been devoted to multimodal description of vocal communication in
trations that infants used variable facial affect with all the proto- nonhuman primates (59), and consequently the emotional valence
phones in each of ve situational contexts, including one in which of vocalizations often has been assessed (to the extent that it has
infants were not engaged in interaction but instead were vocalizing been assessed at all) in terms of external context rather than in
while playing alone in the same room with the parent. Thus, all the terms of a combination of vocal patterns, facial affect, and other
protophones occurred with variable facial affect in all the contexts, behavioral expressions of the sender. To conduct comparative
suggesting considerable robustness of functional exibility across studies patterned after the present one, the optimal approach would
interactive contexts. seem to require a scale of emotional valence applicable, mutatis
To assess observer agreement, two reliability coders judged 21% mutandis, to nonhuman primates as well as human infants. Signi-
of the data for both facial affect and vocal type. They followed the cant groundwork has been laid recently with the development of
same protocol as in the master coding that was used in our data a facial affect coding system for chimpanzee (60, 61) modeled after
analysis (SI Appendix, Supporting Methods: Observer agreement the Ekman scheme for human facial expression (62). An optimal
levels for both vocal type and facial affect). Agreement between the approach also may require consideration of additional expressive
reliability coders and the master based on audio-only judgments modalities, including for example gesture, posture, and piloerection
showed = 0.60 for protophone category (squeal, vocant, or to assign comparable labels of emotional valence across species.
growl) and = 0.91 for cry and laugh. The much higher agreement If future research shows that nonhuman primates (especially
for cry and laugh provides an additional indication of their rel- apes) are incapable of vocal functional exibility or (as seems also
ative innateness and immutability, whereas the lower agreement possible) are signicantly less capable than human infants, we shall
for protophones is consistent with their interpretation as emer- have isolated a key communicative differentiation that may have
gent categories resulting from active exploration of vocalization been one of the rst on the route that led to language in hominins

6322 | www.pnas.org/cgi/doi/10.1073/pnas.1300337110 Oller et al.

after the split from the groups that would become chimpanzees and Denitions of vocal types and facial affect types in the study; (vii) positive,
bonobos. If, on the other hand, the research determines that there neutral, and negative affect as a proxy for function; (viii) illocutionary force
is substantial functional exibility in at least some of the calls coding; (ix) perlocutionary force coding; and (x) observer agreement levels
of nonhuman primates, we shall have helped to cast further for both vocal type and facial affect.
light on the evolution of language and its grounding in the
primate lineage. ACKNOWLEDGMENTS. We thank Yuna Jhang and Beau Franklin for help
with coding. The research for this paper was funded by Grants R01 DC006099
Methods and DC011027from the National Institute on Deafness and Other Communi-
cation Disorders and by the Plough Foundation, which supports D.K.O.s Chair
All procedures were approved by the University of Memphis Institutional
of Excellence at the University of Memphis. Theoretical work underlying
Review Board. Details of methods are found in the SI Appendix. Topics this article was funded in part by the Konrad Lorenz Institute for Evolution
covered are (i) infants and recordings; (ii) selection of data for the present and Cognition Research, where D.K.O. is an external faculty member. A.S.W.
study; (iii) coding software; (iv) utterance location for coding; (v) coding was supported by a U.S. Dept. of Energy Computational Science Graduate
training and coding procedures for both vocal type and facial affect; (vi) Fellowship, DE-FG02-97ER25308.

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