Marmoset vocal communication: Behavior and neurobiology

There has been recent increasing interest in the use of marmosets, a New World primate species, as a model in biomedical research. One of the principal advantages of marmosets as a research model is their rich vocal repertoire and communicative vocal behaviors displayed both in the wild and in captivity. Studies of this species' vocal communication system have the potential to reveal the evolutionary underpinnings of human speech, and therefore are of interest to the neuroscience and biology research communities. Here a recent research into the behavioral and neurobiological basis of marmoset vocal communication was reviewed and they argued for their broader value as a neuroscientific model. They discuss potential avenues for future research including developmental neurobiology and the application of modern molecular tools to the study of primate communication. © 2016 Wiley Periodicals, Inc. Develop Neurobiol 77: 286–299, 2017

[1]  P. Goldman-Rakic,et al.  An auditory domain in primate prefrontal cortex , 2002, Nature Neuroscience.

[2]  J. D. Newman,et al.  Anatomical and physiological evidence for a relationship between the ‘cingular’ vocalization area and the auditory cortex in the squirrel monkey , 1980, Brain Research.

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

[4]  D. Kroodsma,et al.  Ecology and evolution of acoustic communication in birds , 1997 .

[5]  Xiaoqin Wang,et al.  Sensory-motor interaction in the primate auditory cortex during self-initiated vocalizations. , 2003, Journal of neurophysiology.

[6]  G. E. Alexander,et al.  Neural processing of vocalizations and artificial stimulin the medial geniculate body of squirrel monkey , 1980, Hearing Research.

[7]  Sabyasachi Roy,et al.  Vocal control by the common marmoset in the presence of interfering noise , 2011, Journal of Experimental Biology.

[8]  N. Logothetis,et al.  A voice region in the monkey brain , 2008, Nature Neuroscience.

[9]  G. Epple,et al.  Comparative studies on vocalization in marmoset monkeys (Hapalidae). , 1968, Folia primatologica; international journal of primatology.

[10]  Cory T. Miller,et al.  Sensory-motor interactions modulate a primate vocal behavior: antiphonal calling in common marmosets , 2005, Journal of Comparative Physiology A.

[11]  Xiaoqin Wang,et al.  Wireless multi-channel single unit recording in freely moving and vocalizing primates , 2012, Journal of Neuroscience Methods.

[12]  Xiaoqin Wang,et al.  Neural substrates of vocalization feedback monitoring in primate auditory cortex , 2008, Nature.

[13]  T. Yamamori,et al.  Comparative analyses of adeno-associated viral vector serotypes 1, 2, 5, 8 and 9 in marmoset, mouse and macaque cerebral cortex , 2015, Neuroscience Research.

[14]  Uwe Jürgens,et al.  Telemetrically recorded neuronal activity in the inferior colliculus and bordering tegmentum during vocal communication in squirrel monkeys (Saimiri sciureus) , 2004, Behavioural Brain Research.

[15]  David A. Leopold,et al.  The marmoset monkey as a model for visual neuroscience , 2015, Neuroscience Research.

[16]  P. Waser,et al.  Experimental playbacks show vocal mediation of intergroup avoidance in a forest monkey , 1975, Nature.

[17]  Sasaki Kazuo,et al.  Cortical field potentials preceding vocalization and influences of cerebellar hemispherectomy upon them in monkeys , 1995, Brain Research.

[18]  Michael I. Jordan,et al.  Sensorimotor adaptation in speech production. , 1998, Science.

[19]  K. Deisseroth Optogenetics: 10 years of microbial opsins in neuroscience , 2015, Nature Neuroscience.

[20]  J. Kaas,et al.  Architectonic identification of the core region in auditory cortex of macaques, chimpanzees, and humans , 2001, The Journal of comparative neurology.

[21]  David A. Leopold,et al.  Marmosets: A Neuroscientific Model of Human Social Behavior , 2016, Neuron.

[22]  Christoph Kayser,et al.  Modulation of Visual Responses in the Superior Temporal Sulcus by Audio-Visual Congruency , 2010, Front. Integr. Neurosci..

[23]  J. Rauschecker,et al.  Processing of complex sounds in the macaque nonprimary auditory cortex. , 1995, Science.

[24]  Judith M Burkart,et al.  Understanding visual access in common marmosets, Callithrix jacchus: perspective taking or behaviour reading? , 2007, Animal Behaviour.

[25]  Marc D. Hauser,et al.  The Neurophysiology of Functionally Meaningful Categories: Macaque Ventrolateral Prefrontal Cortex Plays a Critical Role in Spontaneous Categorization of Species-Specific Vocalizations , 2005, Journal of Cognitive Neuroscience.

[26]  S. Ribeiro,et al.  Activation of Frontal Neocortical Areas by Vocal Production in Marmosets , 2010, Front. Integr. Neurosci..

[27]  M. Emborg,et al.  Neurobehavioral development of common marmoset monkeys. , 2016, Developmental psychobiology.

[28]  S. King You talkin’ to me? Interactive playback is a powerful yet underused tool in animal communication research , 2015, Biology Letters.

[29]  P. Marler,et al.  Monkey responses to three different alarm calls: evidence of predator classification and semantic communication. , 1980, Science.

[30]  Asif A. Ghazanfar,et al.  Perinatally Influenced Autonomic System Fluctuations Drive Infant Vocal Sequences , 2016, Current Biology.

[31]  Steven J. Eliades,et al.  Journal of Neuroscience Methods Chronic Multi-electrode Neural Recording in Free-roaming Monkeys , 2022 .

[32]  B. Bezerra,et al.  Structure and Usage of the Vocal Repertoire of Callithrix jacchus , 2008, International Journal of Primatology.

[33]  Christoph E Schreiner,et al.  Plasticity in Primary Auditory Cortex of Monkeys with Altered Vocal Production , 2005, The Journal of Neuroscience.

[34]  M. Hauser,et al.  Functional referents and acoustic similarity: field playback experiments with rhesus monkeys , 1998, Animal Behaviour.

[35]  Cory T. Miller,et al.  The communicative content of the common marmoset phee call during antiphonal calling , 2010, American journal of primatology.

[36]  Xiaoqin Wang,et al.  Acoustic analysis of vocal development in a New World primate, the common marmoset (Callithrix jacchus). , 2006, The Journal of the Acoustical Society of America.

[37]  Cory T. Miller,et al.  Frontiers in Integrative Neuroscience Integrative Neuroscience , 2022 .

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

[39]  Cory T. Miller,et al.  Decisions to Communicate in Primate Ecological and Social Landscapes , 2016 .

[40]  C. Larson,et al.  Voice F0 responses to manipulations in pitch feedback. , 1998, The Journal of the Acoustical Society of America.

[41]  P. Goldman-Rakic,et al.  Auditory belt and parabelt projections to the prefrontal cortex in the Rhesus monkey , 1999, The Journal of comparative neurology.

[42]  Torben Dabelsteen,et al.  INTERACTIVE PLAYBACK: A FINELY TUNED RESPONSE , 1992 .

[43]  Cory T. Miller,et al.  Individual recognition during bouts of antiphonal calling in common marmosets , 2012, Journal of Comparative Physiology A.

[44]  L. Huber,et al.  Social influences on the development of foraging behavior in free‐living common marmosets (Callithrix jacchus) , 2006, American journal of primatology.

[45]  Artur Luczak,et al.  Multivariate receptive field mapping in marmoset auditory cortex , 2004, Journal of Neuroscience Methods.

[46]  Christoph Kayser,et al.  Voice Cells in the Primate Temporal Lobe , 2011, Current Biology.

[47]  Christopher DiMattina,et al.  Virtual vocalization stimuli for investigating neural representations of species-specific vocalizations. , 2006, Journal of neurophysiology.

[48]  Lindsay Aitkin,et al.  Audition and the auditory pathway of a vocal new world primate, the common marmoset , 1993, Progress in Neurobiology.

[49]  J. French,et al.  Vocal buffering of the stress response: exposure to conspecific vocalizations moderates urinary cortisol excretion in isolated marmosets , 2005, Hormones and Behavior.

[50]  Doris Y. Tsao,et al.  A Cortical Region Consisting Entirely of Face-Selective Cells , 2006, Science.

[51]  Cory T. Miller,et al.  Responses of primate frontal cortex neurons during natural vocal communication. , 2015, Journal of neurophysiology.

[52]  Ramesh Rajan,et al.  Auditory cortex of the marmoset monkey – complex responses to tones and vocalizations under opiate anaesthesia in core and belt areas , 2013, The European journal of neuroscience.

[53]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[54]  A. Ghazanfar,et al.  Early development of turn-taking with parents shapes vocal acoustics in infant marmoset monkeys , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[55]  Judith M Burkart,et al.  Geometrical gaze following in common marmosets (Callithrix jacchus). , 2006, Journal of comparative psychology.

[56]  P. Holmes,et al.  The developmental dynamics of marmoset monkey vocal production , 2015, Science.

[57]  Doris Y. Tsao,et al.  Comparing face patch systems in macaques and humans , 2008, Proceedings of the National Academy of Sciences.

[58]  Xiaoqin Wang,et al.  Differential representation of species-specific primate vocalizations in the auditory cortices of marmoset and cat. , 2001, Journal of neurophysiology.

[59]  J. Newman,et al.  Context and gender‐specific differences in the acoustic structure of common marmoset (Callithrix jacchus) phee calls , 1993, American journal of primatology.

[60]  P. Grohrock,et al.  Dual-channel telemetry system for recording vocalization-correlated neuronal activity in freely moving squirrel monkeys , 1997, Journal of Neuroscience Methods.

[61]  J. Newman,et al.  Multiple coding of species-specific vocalizations in the auditory cortex of squirrel monkeys. , 1973, Brain research.

[62]  Xiaoqin Wang,et al.  Comparison of auditory-vocal interactions across multiple types of vocalizations in marmoset auditory cortex. , 2013, Journal of neurophysiology.

[63]  David A. Leopold,et al.  Brains, Genes, and Primates , 2015, Neuron.

[64]  Robert M. Seyfarth,et al.  Conceptual Semantics in a Nonhuman Primate , 1999 .

[65]  T. Geissmann,et al.  Calling in wild silvery gibbons (Hylobates moloch) in Java (Indonesia): behavior, phylogeny, and conservation , 2006, American journal of primatology.

[66]  P. Mohseni,et al.  Wireless multichannel biopotential recording using an integrated FM telemetry circuit , 2005, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[67]  Hisae Gemba,et al.  Cortical field potentials associated with audio-initiated vocalization in monkeys , 1999, Neuroscience Letters.

[68]  J. Kaas,et al.  Subdivisions of auditory cortex and processing streams in primates. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

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

[70]  Chia-Chun Hung,et al.  Functional Mapping of Face-Selective Regions in the Extrastriate Visual Cortex of the Marmoset , 2015, The Journal of Neuroscience.

[71]  Cory T. Miller,et al.  Antiphonal call timing in marmosets is behaviorally significant: interactive playback experiments , 2009, Journal of Comparative Physiology A.

[72]  Cory T. Miller,et al.  Vocal turn-taking in a non-human primate is learned during ontogeny , 2015, Proceedings of the Royal Society B: Biological Sciences.

[73]  Xiaoqin Wang,et al.  Motor planning for vocal production in common marmosets , 2009, Animal Behaviour.

[74]  Caralyn Kemp,et al.  Facial expressions in common marmosets (Callithrix jacchus) and their use by conspecifics , 2013, Animal Cognition.

[75]  L. Halsey,et al.  Vocalisations of wild common marmosets are influenced by diurnal and ontogenetic factors , 2009, Primates.

[76]  Xiaoqin Wang,et al.  Dynamics of auditory-vocal interaction in monkey auditory cortex. , 2005, Cerebral cortex.

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

[78]  Feng Rong,et al.  Sensorimotor Integration in Speech Processing: Computational Basis and Neural Organization , 2011, Neuron.

[79]  Xiaoqin Wang,et al.  Spectral integration in A1 of awake primates: neurons with single- and multipeaked tuning characteristics. , 2003, Journal of neurophysiology.

[80]  Corrie R. Camalier,et al.  Coding of FM sweep trains and twitter calls in area CM of marmoset auditory cortex , 2008, Hearing Research.

[81]  H. Okano,et al.  Generation of transgenic non-human primates with germline transmission , 2009, Nature.

[82]  Andreas Nieder,et al.  Single neurons in monkey prefrontal cortex encode volitional initiation of vocalizations , 2013, Nature Communications.

[83]  John H. Reynolds,et al.  Active Vision in Marmosets: A Model System for Visual Neuroscience , 2014, The Journal of Neuroscience.

[84]  M. Mishkin,et al.  FOXP2 and the neuroanatomy of speech and language , 2005, Nature Reviews Neuroscience.

[85]  Hiroshi Kawasaki,et al.  Long-Term Two-Photon Calcium Imaging of Neuronal Populations with Subcellular Resolution in Adult Non-human Primates. , 2015, Cell reports.

[86]  C. Schreiner,et al.  Representation of spectral and temporal envelope of twitter vocalizations in common marmoset primary auditory cortex. , 2002, Journal of neurophysiology.

[87]  Monica Maranesi,et al.  Neurons Controlling Voluntary Vocalization in the Macaque Ventral Premotor Cortex , 2011, PloS one.

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

[89]  Cory T. Miller,et al.  Optogenetic manipulation of neural circuits in awake marmosets. , 2016, Journal of neurophysiology.

[90]  R. Seyfarth,et al.  Who, me? Can baboons infer the target of vocalizations? , 2006, Animal Behaviour.

[91]  Leo L. Lui,et al.  Responses of neurons in the marmoset primary auditory cortex to interaural level differences: comparison of pure tones and vocalizations , 2015, Front. Neurosci..

[92]  Chia-Jung Chang,et al.  A quantitative acoustic analysis of the vocal repertoire of the common marmoset (Callithrix jacchus). , 2015, The Journal of the Acoustical Society of America.

[93]  J. Rauschecker,et al.  Mechanisms and streams for processing of "what" and "where" in auditory cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[94]  C. Schreiner,et al.  Development of spectral and temporal response selectivity in the auditory cortex. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[95]  Bruno B Averbeck,et al.  Neural representation of vocalizations in the primate ventrolateral prefrontal cortex. , 2005, Journal of neurophysiology.

[96]  Bernard S. Lee Effects of delayed speech feedback , 1950 .

[97]  A. Ghazanfar,et al.  Coupled Oscillator Dynamics of Vocal Turn-Taking in Monkeys , 2013, Current Biology.

[98]  M M Merzenich,et al.  Representation of a species-specific vocalization in the primary auditory cortex of the common marmoset: temporal and spectral characteristics. , 1995, Journal of neurophysiology.

[99]  Henning U. Voss,et al.  High-field functional magnetic resonance imaging of vocalization processing in marmosets , 2014, Scientific Reports.

[100]  M. Sommer,et al.  Corollary discharge circuits in the primate brain , 2008, Current Opinion in Neurobiology.

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

[102]  J. Kaas,et al.  Microstimulation and architectonics of frontoparietal cortex in common marmosets (Callithrix jacchus) , 2008, The Journal of comparative neurology.

[103]  Xiaoqin Wang,et al.  Neural Correlates of the Lombard Effect in Primate Auditory Cortex , 2012, The Journal of Neuroscience.

[104]  D. Wolpert,et al.  Motor prediction , 2001, Current Biology.

[105]  D. Symmes,et al.  On the use of natural stimuli in neurophysiological studies of audition , 1981, Hearing Research.

[106]  A. Iriki,et al.  Human speech- and reading-related genes display partially overlapping expression patterns in the marmoset brain , 2014, Brain and Language.

[107]  Lisa A. de la Mothe,et al.  Thalamic connections of the auditory cortex in marmoset monkeys: Core and medial belt regions , 2006, The Journal of comparative neurology.

[108]  R. Seyfarth,et al.  The evolution of language from social cognition , 2014, Current Opinion in Neurobiology.