Monkeys are perceptually tuned to facial expressions that exhibit a theta-like speech rhythm

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 5, 2013, Pages 1959-1963

  Ghazanfar, Asif A ^a   Morrill, Ryan J ^a   Kayser, Christoph ^b,c  

^a PRINCETON UNIVERSITY   (United States)

^b MAX PLANCK INSTITUTE FOR BIOLOGICAL CYBERNETICS   (Germany)

^c UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; COORDINATION; EYE MOVEMENT; FACIAL EXPRESSION; GESTURE; HAPLORHINI; HEAD MOVEMENT; HYPOTHESIS; MOVEMENT (PHYSIOLOGY); NONHUMAN; PRIORITY JOURNAL; RHYTHM; SPEECH;

ANIMALS; BIOLOGICAL EVOLUTION; FACIAL EXPRESSION; HUMANS; LIP; MACACA MULATTA; MOVEMENT; PERIODICITY; SPEECH; THETA RHYTHM; VOCALIZATION, ANIMAL;

EID: 84873201312     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1214956110     Document Type: Article

References (62)

1. Chandrasekaran C, Trubanova A, Stillittano S, Caplier A, Ghazanfar AA (2009) The natural statistics of audiovisual speech. PLOS Comput Biol 5(7):e1000436.
2. Greenberg S, Carvey H, Hitchcock L, Chang S (2003) Temporal properties of spontaneous speech: A syllable-centric perspective. J Phonetics 31(3-4):465-485. (Pubitemid 37495920)
3. Crystal TH, House AS (1982) Segmental durations in connected speech signals: Preliminary results. J Acoust Soc Am 72(3):705-716.
4. Malécot A, Johnston R, Kizziar P-A (1972) Syllabic rate and utterance length in French. Phonetica 26(4):235-251.
5. Drullman R, Festen JM, Plomp R (1994) Effect of reducing slow temporal modulations on speech reception. J Acoust Soc Am 95(5, Pt 1):2670-2680. (Pubitemid 24152861)
6. Saberi K, Perrott DR (1999) Cognitive restoration of reversed speech. Nature 398(6730):760-760.
7. Shannon RV, Zeng F-G, Kamath V, Wygonski J, Ekelid M (1995) Speech recognition with primarily temporal cues. Science 270(5234):303-304.
8. Smith ZM, Delgutte B, Oxenham AJ (2002) Chimaeric sounds reveal dichotomies in auditory perception. Nature 416(6876):87-90. (Pubitemid 34215405)
9. Elliott TM, Theunissen FE (2009) The modulation transfer function for speech intelligibility. PLOS Comput Biol 5(3):e1000302.
10. Vitkovitch M, Barber P (1996) Visible speech as a function of image quality: Effects of display parameters on lipreading ability. Appl Cogn Psychol 10(2):121-140. (Pubitemid 126482118)
11. Poeppel D (2003) The analysis of speech in different temporal integration windows: Cerebral lateralization as 'asymmetric sampling in time' Speech Commun 41(1):245-255.
12. Ghitza O (2011) Linking speech perception and neurophysiology: Speech decoding guided by cascaded oscillators locked to the input rhythm. Front Psychol 2:130.
13. Giraud AL, Poeppel D (2012) Cortical oscillations and speech processing: Emerging computational principles and operations. Nat Neurosci 15(4):511-517.
14. Ahissar E, et al. (2001) Speech comprehension is correlated with temporal response patterns recorded from auditory cortex. Proc Natl Acad Sci USA 98(23):13367-13372. (Pubitemid 33051369)
15. Luo H, Liu Z, Poeppel D (2010) Auditory cortex tracks both auditory and visual stimulus dynamics using low-frequency neuronal phase modulation. PLoS Biol 8(8):e1000445.
16. Luo H, Poeppel D (2007) Phase patterns of neuronal responses reliably discriminate speech in human auditory cortex. Neuron 54(6):1001-1010. (Pubitemid 46907508)
17. Ng BS, Logothetis NK, Kayser C (2012) EEG phase patterns reflect the selectivity of neural firing. Cereb Cortex, 10.1093/cercor/bhs031.
18. Ghitza O, Greenberg S (2009) On the possible role of brain rhythms in speech perception: Intelligibility of time-compressed speech with periodic and aperiodic insertions of silence. Phonetica 66(1-2):113-126.
19. MacNeilage PF (1998) The frame/content theory of evolution of speech production. Behav Brain Sci 21(4):499-511; discussion 511-546.
20. Hinde RA, Rowell TE (1962) Communication by posture and facial expressions in the rhesus monkey (Macaca mulatta). Proc Zool Soc Lond 138(1):1-21.
21. Redican WK (1975) Facial expressions in nonhuman primates. Primate Behavior: Developments in Field and Laboratory Research, ed Rosenblum LA (Academic Press, New York), pp 103-194.
22. Van Hooff JARAM (1962) Facial expressions of higher primates. Symp Zoolog Soc Lond 8:97-125.
23. Parr LA, Cohen M, de Waal F (2005) Influence of social context on the use of blended and graded facial displays in chimpanzees. Int J Primatol 26(1):73-103. (Pubitemid 40383620)
24. Ghazanfar AA, Takahashi DY, Mathur N, Fitch WT (2012) Cineradiography of monkey lip-smacking reveals putative precursors of speech dynamics. Curr Biol 22(13):1176-1182.
25. Ferrari PF, Paukner A, Ionica C, Suomi SJ (2009) Reciprocal face-to-face communication between rhesus macaque mothers and their newborn infants. Curr Biol 19(20):1768-1772.
26. Ferrari PF, et al. (2006) Neonatal imitation in rhesus macaques. PLoS Biol 4(9):e302.
27. De Marco A, Visalberghi E (2007) Facial displays in young tufted Capuchin monkeys (Cebus apella): Appearance, meaning, context and target. Folia Primatol (Basel) 78(2):118-137.
28. Ghazanfar AA, Chandrasekaran C, Morrill RJ (2010) Dynamic, rhythmic facial expressions and the superior temporal sulcus of macaque monkeys: Implications for the evolution of audiovisual speech. Eur J Neurosci 31(10):1807-1817.
29. Morrill RJ, Paukner A, Ferrari PF, Ghazanfar AA (2012) Monkey lipsmacking develops like the human speech rhythm. Dev Sci 15(4):557-568.
30. Chandrasekaran C, Ghazanfar AA (2009) Different neural frequency bands integrate faces and voices differently in the superior temporal sulcus. J Neurophysiol 101(2):773-788.
31. Ghazanfar AA, Chandrasekaran C, Logothetis NK (2008) Interactions between the superior temporal sulcus and auditory cortex mediate dynamic face/voice integration in rhesus monkeys. J Neurosci 28(17):4457-4469.
32. Ghazanfar AA, Maier JX, Hoffman KL, Logothetis NK (2005) Multisensory integration of dynamic faces and voices in rhesus monkey auditory cortex. J Neurosci 25(20):5004-5012. (Pubitemid 40712843)
33. Bruce C, Desimone R, Gross CG (1981) Visual properties of neurons in a polysensory area in superior temporal sulcus of the macaque. J Neurophysiol 46(2):369-384. (Pubitemid 11087648)
34. Lakatos P, et al. (2005) An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex. J Neurophysiol 94(3):1904-1911. (Pubitemid 41192862)
35. Kayser C, Montemurro MA, Logothetis NK, Panzeri S (2009) Spike-phase coding boosts and stabilizes information carried by spatial and temporal spike patterns. Neuron 61(4):597-608.
36. Chandrasekaran C, Lemus L, Trubanova A, Gondan M, Ghazanfar AA (2011) Monkeys and humans share a common computation for face/voice integration. PLOS Comput Biol 7(9):e1002165.
37. Steckenfinger SA, Ghazanfar AA (2009) Monkey visual behavior falls into the uncanny valley. Proc Natl Acad Sci USA 106(43):18362-18366.
38. Lewkowicz DJ (1985) Developmental changes in infants' response to temporal frequency. Dev Psychobiol 21(2):858-865.
39. Zangenehpour S, Ghazanfar AA, Lewkowicz DJ, Zatorre RJ (2009) Heterochrony and cross-species intersensory matching by infant vervet monkeys. PLoS ONE 4(1):e4302.
40. Karmel BZ, Lester ML, McCarvill SL, Brown P, Hofmann MJ (1977) Correlation of infants' brain and behavior response to temporal changes in visual stimulation. Psychophysiology 14(2):134-142. (Pubitemid 8057598)
41. Ghazanfar AA, Logothetis NK (2003) Neuroperception: Facial expressions linked to monkey calls. Nature 423(6943):937-938. (Pubitemid 36806899)
42. Ghazanfar AA, et al. (2007) Vocal-tract resonances as indexical cues in rhesus monkeys. Curr Biol 17(5):425-430.
43. Jordan KE, Brannon EM, Logothetis NK, Ghazanfar AA (2005) Monkeys match the number of voices they hear to the number of faces they see. Curr Biol 15(11):1034-1038. (Pubitemid 40772151)
44. Maier JX, Neuhoff JG, Logothetis NK, Ghazanfar AA (2004) Multisensory integration of looming signals by rhesus monkeys. Neuron 43(2):177-181. (Pubitemid 38942958)
45. Giraud AL, et al. (2007) Endogenous cortical rhythms determine cerebral specialization for speech perception and production. Neuron 56(6):1127-1134.
46. Ghitza O (2012) On the role of theta-driven syllabic parsing in decoding speech: Intelligibility of speech with a manipulated modulation spectrum. Front Psychol 3:1-12.
47. Kayser C, Logothetis NK, Panzeri S (2010) Visual enhancement of the information representation in auditory cortex. Curr Biol 20(1):19-24.
48. Buzsáki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304(5679):1926-1929.
49. Karmel BZ, Maisel EB (1975) A neuronal activity model of infant visual attention. Infant Perception: From Sensation to Cognition. Part I: Basic Visual Processes, eds Cohen LB, Salapatek P (Academic Press, New York), pp 77-131.
50. Arcadi AC, Robert D, Boesch C (1998) Buttress drumming by wild chimpanzees: Temporal patterning. Phrase integration into loud calls, and preliminary evidence for individual distinctiveness. Primates 39(4):505-518. (Pubitemid 29118697)
51. Kalan AK, Rainey HJ (2009) Hand-clapping as a communicative gesture by wild female swamp gorillas. Primates 50(3):273-275.
52. Mehlman PT (1996) Branch shaking and related displays in wild Barbary macaques. Evolution and Ecology of Macaque Societies, eds Fa JE, Lindburg DG (Cambridge Univ. Press, Cambridge, UK), pp 503-526. (Pubitemid 27003829)
53. Remedios R, Logothetis NK, Kayser C (2009) Monkey drumming reveals common networks for perceiving vocal and nonvocal communication sounds. Proc Natl Acad Sci USA 106(42):18010-18015.
54. Hiiemae KM, Palmer JB (2003) Tongue movements in feeding and speech. Crit Rev Oral Biol Med 14(6):413-429. (Pubitemid 44567528)
55. Hiiemae KM, et al. (2002) Hyoid and tongue surface movements in speaking and eating. Arch Oral Biol 47(1):11-27. (Pubitemid 34052666)
56. Moore CA, Smith A, Ringel RL (1988) Task-specific organization of activity in human jaw muscles. J Speech Hear Res 31(4):670-680. (Pubitemid 19006882)
57. Ostry DJ, Munhall KG (1994) Control of jaw orientation and position in mastication and speech. J Neurophysiol 71(4):1528-1545. (Pubitemid 24121848)
58. Matsuo K, Palmer JB (2010) Kinematic linkage of the tongue, jaw, and hyoid during eating and speech. Arch Oral Biol 55(4):325-331.
59. Locke JL (2008) Lipsmacking and babbling: Syllables, sociality, and survival. The Syllable in Speech Production, eds Davis BL, Zajdo K (Lawrence Erlbaum Associates, New York), pp 111-129.
60. Moore CA, Ruark JL (1996) Does speech emerge from earlier appearing oral motor behaviors? J Speech Hear Res 39(5):1034-1047.
61. Steeve RW (2010) Babbling and chewing: Jaw kinematics from 8 to 22 months. J Phonetics 38(3):445-458.
62. Steeve RW, Moore CA, Green JR, Reilly KJ, Ruark McMurtrey J (2008) Babbling, chewing, and sucking: Oromandibular coordination at 9 months. J Speech Lang Hear Res 51(6):1390-1404.