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Sensory-motor interactions modulate a primate vocal behavior: antiphonal calling in common marmosets

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Abstract

A fundamental issue in neuroscience pertains to how different cortical systems interact to generate behavior. One of the most direct ways to address this issue is to investigate how sensory information is encoded and used to produce a motor response. Antiphonal calling is a natural vocal behavior that involves individuals producing their species-specific long distance vocalization in response to hearing the same call and engages both the auditory and motor systems, as well as the cognitive neural systems involved in decision making and categorization. Here we present results from a series of behavioral experiments investigating the auditory–vocal interactions during antiphonal calling in the common marmoset (Callithrix jacchus). We manipulated sensory input by placing subjects in different social contexts and found that the auditory input had a significant effect on call timing and propensity to call. Playback experiments tested the significance of the timing of vocal production in antiphonal calling and showed that a short latency between antiphonal calls was necessary to maintain reciprocal vocal interactions. Overall, this study shows that sensory-motor interactions can be experimentally induced and manipulated in a natural primate vocal behavior. Antiphonal calling represents a promising model system to examine these issues in non-human primates at both the behavioral and neural levels.

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Abbreviations

CM:

Cagemate

HVC:

High vocal center

NCM:

Non-cagemate

NCM-OS:

Non-cagemate of the opposite sex

NCM-SS:

Non-cagemate of the same sex

References

  • Barbour D, Wang X (2003a) Auditory cortical responses elicited in awake primates by random spectrum stimuli. J Neuro 23:7194–7206

    Google Scholar 

  • Barbour D, Wang X (2003b) Contrast tuning in auditory cortex. Science 299

  • Bergman TJ, Beehner JC, Cheney DL, Seyfarth RM (2003) Hierarchical classification by rank and kinship in baboons. Science 302:1234–1236

    Article  PubMed  CAS  Google Scholar 

  • Carew TJ (2000) Behavioral neurobiology: the cellular organization of natural behavior. Sinauer Associates, New York

    Google Scholar 

  • Cheney DL, Seyfarth RM (1982) Recognition of individuals within and between groups of free ranging vervet monkeys. Am Zool 22:519–529

    Google Scholar 

  • Dabelsteen T, McGregor PK (1996) Dynamic acoustic communication and interactive playback. In: Kroodsma DE, Miller EH (eds), Ecology and evolution of acoustic commmunication in birds. Cornell University Press, Ithaca, pp 398–408

    Google Scholar 

  • Dave A, Yu AC, Margoliash D (1998) Behavioral state modulation of auditory activity in a vocal motor system. Science 282:2250–2254

    Article  PubMed  CAS  Google Scholar 

  • Eliades SJ, Wang X (2003) Sensory-motor interaction in the primate auditory cortex during self-initiated vocalizations. J Neurophysiol 89:2185–2207

    PubMed  Google Scholar 

  • Eliades SJ, Wang X (2005) Dynamics of auditory-vocal interaction in monkey auditory cortex. Cerebral Cortex (In Press)

  • Epple G, Belcher AM, Kuderling I, Zeller U, Scolnock L, Greenfield KL, Smith III AB (1993) Making sense out of scents: species differences in scent glands, scent-marking behavior and scent mark composition in the Callitrichidae. In: Rylands AB (ed) Marmosets and tamarins: systematics, behaviour and ecology. Oxford University Press, Oxford, pp 123–153

    Google Scholar 

  • Fee MS, Leonardo A (2001) Miniature motorized microdrive and commutator system for chronic neural recording in a small animal. J Neuro Methods 112:83–94

    Article  CAS  Google Scholar 

  • Freedman DJ, Anderson KC, Miller EK (2001) Categorical representation of visual stimuli in the primate prefrontal cortex. Science 291:312–316

    Article  PubMed  CAS  Google Scholar 

  • Ghazanfar AA, Hauser MD (2001) The auditory behaviour of primates: a neuroethological perspective. Curr Op Neuro 11:712–720

    Article  CAS  Google Scholar 

  • Ghazanfar AA, Flombaum JI, Miller CT, Hauser MD (2001) The units of peception in cotton-top tamarin (Saguinus oedipus) long calls. J Comp Physiol A 187:27–35

    Article  PubMed  CAS  Google Scholar 

  • Ghazanfar AA, Smith-Rohrberg D, Pollen A, Hauser MD (2002) Temporal cues in the antiphonal calling behaviour of cotton-top tamarins. Anim Behav 64:427–438

    Article  Google Scholar 

  • Grace JA, Amin N, Singh NC, Theunissen FE (2003) Selectivity for conspecific song in the zebra finch auditory forebrain. J Neurophysiol 89:472–487

    Article  PubMed  Google Scholar 

  • Hahnloser RHR, Kozhevnikov AA, Fee MS (2002) An ultra-sparse code underlies the generation of neural sequences in a songbird. Nature 419:65–70

    Article  PubMed  CAS  Google Scholar 

  • Hauser MD (1996) The evolution of communication. MIT Press, Cambridge

    Google Scholar 

  • Hessler N, Doupe AJ (2000) Social context modulates singing-related neural activity in the songbird forebrain. Nat Neuro 2:209–211

    Article  Google Scholar 

  • Jarvis ED, Scharff C, Grossman M, Ramos JA, Nottebohm F (1998) For whom the bird sings: context-dependent gene expression. Neuron 21:775–788

    Article  PubMed  CAS  Google Scholar 

  • Leonardo A, Fee MS (2005) Ensemble coding of vocal control in birdsong. J Neuro 25:652–661

    Article  CAS  Google Scholar 

  • Liberman AM (1996) Speech: a special code. MIT press, Cambridge

    Google Scholar 

  • Lu T, Liang L, Wang X (2001a) Temporal and rate representations in time varying signals in the auditory cortex of awake primates. Nat Neuro 4:1131–1138

    Article  CAS  Google Scholar 

  • Lu T, Liang L, Wang X (2001b) Neural representation of temporally asymmetric stimuli in the auditory cortex of awake primates. J Neurophysiol 85:2364–2380

    PubMed  CAS  Google Scholar 

  • Luo M, Fee MS, Katz LC (2003) Encoding phermonal signals in the accessory olfactory bulb of behaving mice. Science 299:1196–1201

    Article  PubMed  CAS  Google Scholar 

  • Marler P, Slabbekoorn H (2004) Nature’s music: the science of birdsong. Elsevier/Academic Press, Amsterdam

    Google Scholar 

  • Miller CT, Hauser MD (2004) Multiple acoustic features underlie vocal signal recognition in tamarins: antiphonal calling experiments. J Comp Physiol A 190:7–19

    Article  CAS  Google Scholar 

  • Miller CT, Dibble E, Hauser MD (2001a) Amodal completion of acoustic signals by a nonhuman primate. Nat Neuro 4:783–784

    Article  CAS  Google Scholar 

  • Miller CT, Miller J, Costa RGD, Hauser MD (2001b) Selective phontaxis by cotton-top tamarins (Saguinus oeidpus). Behaviour 138:811–826

    Article  Google Scholar 

  • Miller CT, Scarl JS, Hauser MD (2004) Sensory biases underlie sex differences in tamarin long call structure. Anim Beh 68:713–720

    Article  Google Scholar 

  • Miller CT, Iguina C, Hauser MD (2005) Processing vocal signal for recognition during antiphonal calling. Anim Beh 69:1387–1398

    Article  Google Scholar 

  • Miller EK, Nieder A, Freedman DJ, Wallis JD (2003) Neural correlates of categories and concepts. Curr Op Neurobiol 13:198–203

    Article  PubMed  CAS  Google Scholar 

  • Newman JD, Wollberg Z (1973) Multiple coding of species-specific vocalizations in the auditory cortex of squirrel monkeys. Brain Res 54:287–304

    Article  PubMed  CAS  Google Scholar 

  • Nieder A, Freedman DJ, Miller EK (2002) Representation of quantity of visual items in the primate prefrontal cortex. Science 297:1708–1711

    Article  PubMed  CAS  Google Scholar 

  • Norcross JL, Newman JD (1993) Context and gender specific differences in the acoustic structure of common marmoset (Callithrix jacchus) phee calls. Am J Prim 30:37–54

    Article  Google Scholar 

  • Norcross JL, Newman JD (1997) Social context affects phee call production by nonreproductive common marmosets (Callithrix jacchus). Am J Prim 43:135–146

    Article  CAS  Google Scholar 

  • Norcross JL, Newman JD, Fitch WT (1994) Responses to natural and synthetic phee calls by common marmosets. Am J Prim 33:15–29

    Article  Google Scholar 

  • Nottebohm F, Stokes TM, Leonard CM (1976) Central control of song in the canary, Serinus canarius. J Comp Neurol 165:457–468

    Article  PubMed  CAS  Google Scholar 

  • Rauschecker JP, Tian B, Hauser M (1995) Processing of complex sounds in the macaque nonprimary auditory cortex. Science 268:111–114

    Article  PubMed  CAS  Google Scholar 

  • Rendall D, Rodman PS, Edmond RE (1996) Vocal recognition of individuals and kin in free-ranging rhesus monkeys. Anim Beh 51:1007–1015

    Article  Google Scholar 

  • Romanski LM, Goldman-Rakic PS (2001) An auditory domain in primate prefrontal. Nat Neuro 5:15–16

    Article  CAS  Google Scholar 

  • Romanski LM, Averbeck BB, Diltz M (2004) Neural representation of vocalizations in the primate ventrolateral prefrontal cortex. J Neurophysiol 93:734–747

    Article  PubMed  Google Scholar 

  • Romo R, Salinas E (2003) Flutter discrimination: neural codes, perception and decision making. Nat Rev Neuro 4:203–221

    Article  PubMed  CAS  Google Scholar 

  • Romo R, Brody CD, Hernandez A, Lemus L (1999) Neuronal correlates of parametric working memory in the prefrontal cortex. Nature 399:470–473

    Article  PubMed  CAS  Google Scholar 

  • Romo R, Hernandez A, Zainos A (2004) Neuronal correlates of a perceptual decision in ventral premotor. Neuron 41:165–173

    Article  PubMed  CAS  Google Scholar 

  • Schmidt MF, Konishi M (1998) Gating of auditory responses in the vocal control system of awake songbirds. Nat Neuro 1:513–518

    Article  CAS  Google Scholar 

  • Schwartz JH (2001) Call monitoring and interactive playback systems in the study of acoustic interactions among male anurans. In: Ryan MJ (eds) Anuran communication. Smithsonian Institution Press, Washington

    Google Scholar 

  • Sen K, Theunissen FE, Doupe AJ (2001) Feature analysis of natural sounds in the songbird auditory cortex. J Neurophysiol 86:1145–1458

    Google Scholar 

  • Smith TE, Tomlinson AJ, Mlotkiewcz JZ, Abbott DH (2001) Female marmoset monkeys (Callithrix jacchus) can be identified from chemical composition of their scent marks. Chem Sens 26:449–458

    Article  CAS  Google Scholar 

  • Spiro JE, Dalva MB, Mooney R (1999) Long-range inhibition within the zebra finch song nucleus RA can coordinate the firing of multiple projection neurons. J Neurophysiol 81:3007–3020

    PubMed  CAS  Google Scholar 

  • Wang X (2000) On cortical coding of vocal communication sounds in primates. Proc Nat Acad Sci 97:11843–11849

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Kadia SC (2001) Differential representation of species-specific primate vocalizations in the auditory cortices of marmoset and cat. J Neurophysiol 86:2616–2620

    PubMed  CAS  Google Scholar 

  • Wang X, Merzenich MM, Beitel R, Schreiner CE (1995) Representations of species-specific vocalizations in the primary auditory cortex of the common marmoset: temporal and spectral characteristics. J Neurophysiol 74:2685–2706

    PubMed  CAS  Google Scholar 

  • Weiss DJ, Garibaldi BT, Hauser MD (2001) The production and perception of long calls by cotton-top tamarins (Saguinus oedipus): acoustic analyses and playback experiments. J Comp Psych 11:258–271

    Article  Google Scholar 

  • Winter P, Funkenstein HH (1973) The effect of species-specific vocalizations on the discharge of auditory cortical cells in the awake squirrel monkey. Exp Brain Res 18:489–504

    Article  PubMed  CAS  Google Scholar 

  • Yu AC, Margoliash D (1996) Temporal hierarchical control of singing in birds. Science 273:1871–1874

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank Audrey DiMauro, Kate Mandel, Kate Rydstrom, Ambica Tumkur, and Ray Wang for their help in running these experiments. This research was supported by NIH grants F32 DC007022 (CTM) and R01 DC 005808 (XW). These experiments comply with the ‘Principles of Animal Care’, Publication No. 86–23, revised 1985, of the National Institutes of Health. All experimental protocols were approved by the Johns Hopkins University Animal Use and Care Committee.

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Correspondence to Cory T. Miller.

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Miller, C.T., Wang, X. Sensory-motor interactions modulate a primate vocal behavior: antiphonal calling in common marmosets. J Comp Physiol A 192, 27–38 (2006). https://doi.org/10.1007/s00359-005-0043-z

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  • DOI: https://doi.org/10.1007/s00359-005-0043-z

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