Two organizing principles of vocal production: Implications for nonhuman and human primates

Vocal communication in nonhuman primates receives considerable research attention, with many investigators arguing for similarities between this calling and speech in humans. Data from development and neural organization show a central role of affect in monkey and ape sounds, however, suggesting that their calls are homologous to spontaneous human emotional vocalizations while having little relation to spoken language. Based on this evidence, we propose two principles that can be useful in evaluating the many and disparate empirical findings that bear on the nature of vocal production in nonhuman and human primates. One principle distinguishes production‐first from reception‐first vocal development, referring to the markedly different role of auditory‐motor experience in each case. The second highlights a phenomenon dubbed dual neural pathways, specifically that when a species with an existing vocal system evolves a new functionally distinct vocalization capability, it occurs through emergence of a second parallel neural pathway rather than through expansion of the extant circuitry. With these principles as a backdrop, we review evidence of acoustic modification of calling associated with background noise, conditioning effects, audience composition, and vocal convergence and divergence in nonhuman primates. Although each kind of evidence has been interpreted to show flexible cognitively mediated control over vocal production, we suggest that most are more consistent with affectively grounded mechanisms. The lone exception is production of simple, novel sounds in great apes, which is argued to reveal at least some degree of volitional vocal control. If also present in early hominins, the cortically based circuitry surmised to be associated with these rudimentary capabilities likely also provided the substrate for later emergence of the neural pathway allowing volitional production in modern humans. Am. J. Primatol. 73:530–544, 2011. © 2010 Wiley‐Liss, Inc.

[1]  H. de Vries,et al.  Male monkeys remember which group members have given alarm calls , 2006, Proceedings of the Royal Society B: Biological Sciences.

[2]  L. Fogassi,et al.  Audiovisual mirror neurons and action recognition , 2003, Experimental Brain Research.

[3]  Kurt Hammerschmidt,et al.  Constraints in primate vocal production , 2008 .

[4]  T. Fenzl,et al.  Dissimilarities in the vocal control over communication and echolocation calls in bats , 2007, Behavioural Brain Research.

[5]  R. Seyfarth,et al.  The Ontogeny of Vervet Monkey Alarm Calling Behavior: A Preliminary Report , 2010 .

[6]  D B Moody,et al.  Regulation of voice amplitude by the monkey. , 1975, The Journal of the Acoustical Society of America.

[7]  D. Rendall Acoustic correlates of caller identity and affect intensity in the vowel-like grunt vocalizations of baboons. , 2003, The Journal of the Acoustical Society of America.

[8]  S. Wich,et al.  Possible audience effect in thomas langurs (primates; presbytis thomasi): An experimental study on male loud calls in response to a tiger model , 2003, American journal of primatology.

[9]  D K Oller,et al.  Infant vocalizations and the early diagnosis of severe hearing impairment. , 1994, The Journal of pediatrics.

[10]  D. Todt,et al.  Acoustic communication in noise: regulation of call characteristics in a New World monkey , 2004, Journal of Experimental Biology.

[11]  J. Mitani,et al.  Social Factors Influence the Acoustic Variability in the Long‐distance Calls of Male Chimpanzees , 2010 .

[12]  R. Seyfarth,et al.  Vocal development in vervet monkeys , 1986, Animal Behaviour.

[13]  C. Larson,et al.  Neocortical and limbic lesion effects on primate phonation. , 1974, Brain research.

[14]  Robert M. Seyfarth,et al.  'Food' Calls Produced By Adult Female Rhesus (Macaca Mulatta) and Japanese (M. Fuscata) Macaques, Their Normally-Raised Offspring, and Offspring Cross-Fostered Between Species , 1992 .

[15]  Robert M. Seyfarth,et al.  Behavioral mechanisms underlying vocal communication in nonhuman primates , 1997 .

[16]  P. Marler,et al.  Vervet monkey alarm calls: Semantic communication in a free-ranging primate , 1980, Animal Behaviour.

[17]  S. Green,et al.  Dialects in Japanese monkeys: vocal learning and cultural transmission of locale-specific vocal behavior? , 2010, Zeitschrift fur Tierpsychologie.

[18]  R. Schusterman,et al.  3Vocal Learning in Mammals with Special Emphasis on Pinnipeds , 2008 .

[19]  Uwe Jürgens,et al.  The Influence of Hearing Impairment on Preverbal Emotional Vocalizations of Infants , 2004, Folia Phoniatrica et Logopaedica.

[20]  J. Eccles The emotional brain. , 1980, Bulletin et memoires de l'Academie royale de medecine de Belgique.

[21]  L. Barsalou,et al.  Embodiment in the acquisition and use of emotion knowledge , 2005 .

[22]  M. Knörnschild,et al.  Babbling behavior in the sac-winged bat (Saccopteryx bilineata) , 2006, Naturwissenschaften.

[23]  P. Lieberman On the nature and evolution of the neural bases of human language. , 2002, American journal of physical anthropology.

[24]  John D. Pierce,et al.  A review of attempts to condition operantly alloprimate vocalizations , 1985, Primates.

[25]  G. Rizzolatti,et al.  Action recognition in the premotor cortex. , 1996, Brain : a journal of neurology.

[26]  Martine Hausberger,et al.  Patterns of vocal sharing and social dynamics in a captive group of Campbell's monkeys (Cercopithecus campbelli campbelli). , 2004, Journal of comparative psychology.

[27]  David A. Leavens,et al.  Chimpanzees differentially produce novel vocalizations to capture the attention of a human , 2007, Animal Behaviour.

[28]  M. Horton,et al.  Cells in regenerating deer antler cartilage provide a microenvironment that supports osteoclast differentiation. , 2001, The Journal of experimental biology.

[29]  J. Mitani,et al.  Chorusing and Call Convergence in Chimpanzees: Tests of Three Hypotheses , 1998 .

[30]  C. Boesch,et al.  Wild Chimpanzees Produce Group‐Specific Calls: a Case for Vocal Learning? , 2004 .

[31]  R. Wrangham,et al.  Does learning affect the structure of vocalizations in chimpanzees? , 1999, Animal Behaviour.

[32]  R. Seyfarth,et al.  Vervet monkey alarm calls: Manipulation through shared information? , 1985 .

[33]  Joseph E LeDoux Emotion Circuits in the Brain , 2000 .

[34]  M J Owren,et al.  Vocalizations of rhesus (Macaca mulatta) and Japanese (M. fuscata) macaques cross-fostered between species show evidence of only limited modification. , 1993, Developmental psychobiology.

[35]  Eve V. Clark,et al.  Comprehension, Production, and Language Acquisition , 1983 .

[36]  P. Slater,et al.  Bird Song: Biological Themes and Variations , 1995 .

[37]  Klaus Zuberbühler,et al.  Chimpanzees modify recruitment screams as a function of audience composition , 2007, Proceedings of the National Academy of Sciences.

[38]  A. M. Elowson,et al.  `Babbling' and social context in infant monkeys: parallels to human infants , 1998, Trends in Cognitive Sciences.

[39]  P. Slater,et al.  The different roles of social learning in vocal communication , 2000, Animal Behaviour.

[40]  Erich D. Jarvis,et al.  Neural systems for vocal learning in birds and humans: a synopsis , 2007, Journal of Ornithology.

[41]  Michelle Y. Merrill,et al.  Orangutan Cultures and the Evolution of Material Culture , 2003, Science.

[42]  S. Savage-Rumbaugh How monkeys see the world , 1992, International Journal of Primatology.

[43]  D. Penfield Manipulating foraging group size : spider monkey food calls at fruiting trees , 2006 .

[44]  Gert Holstege,et al.  Chapter 1 The emotional motor system , 1996 .

[45]  P. Marler,et al.  Dialects in wild chimpanzees? , 1992, American journal of primatology.

[46]  Akihiro Katada,et al.  Lombard reflex during PAG-induced vocalization in decerebrate cats , 1997, Neuroscience Research.

[47]  Regulation of vocal output by chimpanzees finding food in the presence or absence of an audience , 2001 .

[48]  Brent A. Vogt,et al.  Structure and Connections of the Cingulate Vocalization Region in the Rhesus Monkey , 1988 .

[49]  M. Domjan The principles of learning and behavior, 4th ed. , 1998 .

[50]  D. Ploog,et al.  Effect of deafening on the vocal behavior of the squirrel monkey (Saimiri sciureus). , 1972, Folia primatologica; international journal of primatology.

[51]  T. J. Seller Midbrain vocalization centres in birds , 1981, Trends in Neurosciences.

[52]  Steffen R. Hage,et al.  Audio–vocal interaction in the pontine brainstem during self‐initiated vocalization in the squirrel monkey , 2006, The European journal of neuroscience.

[53]  D. Barash Human Ethology , 1973 .

[54]  K. Scherer,et al.  Appraisal processes in emotion: Theory, methods, research. , 2001 .

[55]  C. Larson,et al.  Vocalization in rhesus monkeys: conditionability. , 1973, Brain research.

[56]  W. Grodd,et al.  Neural correlates of laughter and humour. , 2003, Brain : a journal of neurology.

[57]  HIDEKI SUGIURA,et al.  Matching of acoustic features during the vocal exchange of coo calls by Japanese macaques , 1998, Animal Behaviour.

[58]  G. Rizzolatti,et al.  A unifying view of the basis of social cognition , 2004, Trends in Cognitive Sciences.

[59]  N. Caine,et al.  Factors affecting the rates of food calls given by red-bellied tamarins , 1995, Animal Behaviour.

[60]  Charles T. Snowdon,et al.  Quality, Quantity, Distribution and Audience Effects on Food Calling in Cotton—Top Tamarins , 2000 .

[61]  J. Wingfield,et al.  Intraventricular Infusion of Arginine Vasotocin induces Singing in a Female Songbird , 1997, Journal of neuroendocrinology.

[62]  Joseph E LeDoux Emotion circuits in the brain. , 2009, Annual review of neuroscience.

[63]  R. Hinde,et al.  VOCAL COMMUNICATION BY THE RHESUS MOJSXEY (MACACA MULATTA) , 2009 .

[64]  D. Ploog,et al.  Ontogeny of squirrel monkey calls under normal conditions and under acoustic isolation. , 1973, Behaviour.

[65]  P. Slater,et al.  Call usage learning in gray seals (Halichoerus grypus). , 2004, Journal of comparative psychology.

[66]  G. Holstege,et al.  The emotional motor system. , 1992, European journal of morphology.

[67]  H. Lane,et al.  The Lombard Sign and the Role of Hearing in Speech , 1971 .

[68]  D Margoliash,et al.  Functional organization of forebrain pathways for song production and perception. , 1997, Journal of neurobiology.

[69]  S. Wich,et al.  Innovation in wild Bornean orangutans (Pongo pygmaeus wurmbii) , 2006 .

[70]  The Zoological Society of London , 1896, Nature.

[71]  U. Jürgens,et al.  The neural control of vocalization in mammals: a review. , 2009, Journal of voice : official journal of the Voice Foundation.

[72]  F. Waal,et al.  The Communicative Repertoire of Captive Bonobos (Pan Paniscus), Compared To That of Chimpanzees , 1988 .

[73]  M. Owren,et al.  An acoustic analysis of laughter produced by congenitally deaf and normally hearing college students. , 2008, The Journal of the Acoustical Society of America.

[74]  J. Itani Vocal communication of the wild Japanese monkey , 1963, Primates.

[75]  M. Owren,et al.  Variations in fundamental frequency peak position in Japanese macaque (Macaca fuscata) coo calls. , 1994, Journal of comparative psychology.

[76]  D. Vicario,et al.  Brain pathways for learned and unlearned vocalizations differ in zebra finches , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[77]  C. Snowdon,et al.  Environmental correlates of vocal communication of wild pygmy marmosets, Cebuella pygmaea , 2002, Animal Behaviour.

[78]  D. Sutton,et al.  Vocal and nonvocal discriminative performance in monkeys , 1981, Brain and Language.

[79]  U. Jürgens Neural pathways underlying vocal control , 2002, Neuroscience & Biobehavioral Reviews.

[80]  Elisabeth Scheiner,et al.  Acoustic analyses of developmental changes and emotional expression in the preverbal vocalizations of infants. , 2002, Journal of voice : official journal of the Voice Foundation.

[81]  James D. McCawley,et al.  The Human Language , 1995 .

[82]  M. Domjan The principles of learning and behavior , 1982 .

[83]  A. Arcadi,et al.  Phrase structure of wild chimpanzee pant hoots: Patterns of production and interpopulation variability , 1996, American journal of primatology.

[84]  S. Wich,et al.  A description of the orangutan's vocal and sound repertoire, with a focus on geographic variation , 2008 .

[85]  William D. Hopkins,et al.  Left Hemisphere Specialization for Oro-Facial Movements of Learned Vocal Signals by Captive Chimpanzees , 2008, PloS one.

[86]  Terrence W. Deacon,et al.  The neural circuitry underlying primate calls and human language , 1989 .

[87]  Charles T. Snowdon,et al.  Pygmy marmosets, Cebuella pygmaea, modify vocal structure in response to changed social environment , 1994, Animal Behaviour.

[88]  Peter L. Tyack,et al.  Social influences on vocal development: Vocal learning in cetaceans , 1997 .

[89]  Serge A. Wich,et al.  A case of spontaneous acquisition of a human sound by an orangutan , 2008, Primates.

[90]  J. Lancaster Primate Behavior and the Emergence of Human Culture , 1975 .

[91]  C. Snowdon,et al.  Dialects in pygmy marmosets? Population variation in call structure , 2009, American journal of primatology.

[92]  S. Savage-Rumbaugh,et al.  Vocal Production by a Language-Competent Pan paniscus , 2003, International Journal of Primatology.

[93]  K. Hammerschmidt,et al.  VOCAL DEVELOPMENT IN SQUIRREL MONKEYS , 2001 .

[94]  R. W. Mitchell,et al.  Simon says: The development of imitation in an enculturated orangutan. , 1996 .

[95]  G. Rizzolatti,et al.  Hearing Sounds, Understanding Actions: Action Representation in Mirror Neurons , 2002, Science.

[96]  G. Striedter,et al.  The vocal control pathways in budgerigars differ from those in songbirds , 1994, The Journal of comparative neurology.

[97]  J. Wild,et al.  Neural pathways for the control of birdsong production. , 1997, Journal of neurobiology.

[98]  D. Sutton,et al.  Primate phonation: Anterior cingulate lesion effects on response rate and acoustical structure , 1981, American journal of primatology.

[99]  S. Wich,et al.  Tool use in wild orang-utans modifies sound production: a functionally deceptive innovation? , 2009, Proceedings of the Royal Society B: Biological Sciences.

[100]  Gareth Jones,et al.  The evolution of echolocation in bats. , 2006, Trends in ecology & evolution.

[101]  C. Hayes,et al.  The ape in our house , 1951 .

[102]  C. Darwin The Expression of the Emotions in Man and Animals , .

[103]  Eckart Altenmüller,et al.  Evolution of Emotional Communication: From Sounds in Nonhuman Mammals to Speech and Music in Man , 2013 .

[104]  J. Mitani,et al.  Geographic variation in the calls of wild chimpanzees: A reassessment , 1999, American journal of primatology.

[105]  N. Masataka,et al.  Locale‐specific Vocal Behaviour of the Tamarin (Saguinus I. labiatus) , 2010 .

[106]  E. Adkins-Regan,et al.  Sexual differentiation of brain and behavior in the zebra finch: critical periods for effects of early estrogen treatment. , 1994, Journal of neurobiology.

[107]  D. Oller The emergence of the speech capacity , 2000 .

[108]  K. Scherer,et al.  Acoustic profiles in vocal emotion expression. , 1996, Journal of personality and social psychology.

[109]  Marvin B. Shapiro,et al.  Development of the Isolation Peep in laboratory-bred squirrel monkeys , 1980, Animal Behaviour.

[110]  D. Rendall,et al.  Vocalizations as tools for influencing the affect and behavior of others , 2010 .

[111]  Chris J. Clement,et al.  Babbling and the lack of auditory speech perception: a matter of coordination? , 2001 .

[112]  Silhouettes elicit alarm calls from captive vervet monkeys (Cercopithecus aethiops). , 1992, Journal of comparative psychology.

[113]  G. Rizzolatti,et al.  ß Federation of European Neuroscience Societies Mirror , 2003 .

[114]  D K Oller,et al.  The role of audition in infant babbling. , 1988, Child development.

[115]  J. Mitani,et al.  Contexts and social correlates of long-distance calling by male chimpanzees , 1993, Animal Behaviour.

[116]  Amy S. Pollick,et al.  Audience effects on food calls in captive brown capuchin monkeys, Cebus apella , 2005, Animal Behaviour.

[117]  Marc D. Hauser,et al.  Chimpanzees (Pan troglodytes) modify grouping and vocal behaviour in response to location-specific risk , 2007 .

[118]  Joel Waldfogel,et al.  Introduction , 2010, Inf. Econ. Policy.

[119]  Charles T. Snowdon,et al.  Pygmy Marmosets modify call structure when paired , 1999 .

[120]  S. Green,et al.  Variation of Vocal Pattern with Social Situation in the Japanese Monkey (Macaca fuscata): A Field Study * , 1975 .