Humans mimicking animals: A cortical hierarchy for human vocal communication sounds

Journal of Neuroscience

Volumn 32, Issue 23, 2012, Pages 8084-8093

  Talkington, William J ^a   Rapuano, Kristina M ^a   Hitt, Laura A ^b   Frum, Chris A ^a   Lewis, James W ^a  

^a Center for Advanced Imaging   (United States)

^b WEST VIRGINIA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; AUDITORY RESPONSE; AUDITORY STIMULATION; AUDITORY THRESHOLD; BOLD SIGNAL; DOMINANCE BEHAVIOR; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; MALE; NORMAL HUMAN; PRIMARY AUDITORY CORTEX; PRIORITY JOURNAL; SPEECH DISCRIMINATION; SUPERIOR TEMPORAL SULCUS; TEMPORAL GYRUS; VOCALIZATION; VOICE;

ADULT; ANIMALS; AUDITORY PERCEPTION; CEREBRAL CORTEX; COMMUNICATION; ENTROPY; FEMALE; FUNCTIONAL LATERALITY; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MENTAL PROCESSES; OXYGEN; PSYCHOPHYSICS; SPEECH; VOCALIZATION, ANIMAL; YOUNG ADULT;

EID: 84861908557     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1118-12.2012     Document Type: Article

References (71)

1. Abrams DA, Nicol T, Zecker S, Kraus N (2009) Abnormal cortical processing of the syllable rate of speech in poor readers. J Neurosci 29:7686-7693.
2. Aeschlimann M, Knebel JF, Murray MM, Clarke S (2008) Emotional preeminence of human vocalizations. Brain Topogr 20:239-248.
3. Alain C (2007) Breaking the wave: effects of attention and learning on concurrent sound perception. Hear Res 229:225-236.
4. Argall BD, Saad ZS, Beauchamp MS (2006) Simplified intersubject averaging on the cortical surface using SUMA. Hum Brain Mapp 27:14-27.
5. Austin JL (1975) How to do things with words, Ed 2. Cambridge, MA: Harvard UP.
6. Belin P, Zatorre RJ, Lafaille P, Ahad P, Pike B (2000) Voice-selective areas in human auditory cortex. Nature 403:309-312.
7. Belin P, Zatorre RJ, Ahad P (2002) Human temporal-lobe response to vocal sounds. Cogn Brain Res 13:17-26.
8. Binder JR, Frost JA, Hammeke TA, Bellgowan PS, Springer JA, Kaufman JN, Possing ET (2000) Human temporal lobe activation by speech and nonspeech sounds. Cereb Cortex 10:512-528.
9. Blasi A, Mercure E, Lloyd-Fox S, Thomson A, Brammer M, Sauter D, Deeley Q, Barker GJ, Renvall V, Deoni S, Gasston D, Williams SC, Johnson MH, Simmons A, MurphyDG (2011) Early specialization for voice and emotion processing in the infant brain. Curr Biol 21:1220-1224.
10. Boersma P (1993) Accurate short-term analysis of the fundamental frequency and the harmonics-to-noise ratio of a sampled sound. Proc Inst Phon Sci 15:97-110.
11. Chevillet M, Riesenhuber M, Rauschecker JP (2011) Functional correlates of the anterolateral processing hierarchy in human auditory cortex. J Neurosci 31:9345-9352.
12. Chung MK, Robbins SM, Dalton KM, Davidson RJ, Alexander AL, Evans AC (2005) Cortical thickness analysis in autism with heat kernel smoothing. Neuroimage 25:1256-1265.
13. Cooper RP, Aslin RN (1990) Preference for infant-directed speech in the first month after birth. Child Dev 61:1584-1595.
14. Cox RW (1996) AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 29:162-173.
15. Cronbach LJ (1951) Coefficient alpha and the internal structure of tests. Psychometrika 16:297-334.
16. Dale AM, Fischl B, Sereno MI (1999) Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 9:179-194.
17. Davis MH, Johnsrude IS (2003) Hierarchical processing in spoken language comprehension. J Neurosci 23:3423-3431.
18. Decasper AJ, Lecanuet JP, Busnel MC, Granierdeferre C, Maugeais R (1994) Fetal reactions to recurrent maternal speech. Infant Behav Dev 17:159-164.
19. Edmister WB, Talavage TM, Ledden PJ, Weisskoff RM (1999) Improved auditory cortex imaging using clustered volume acquisitions. Hum Brain Mapp 7:89-97.
20. Ethofer T, Anders S, Erb M, Herbert C, Wiethoff S, Kissler J, Grodd W, Wildgruber D (2006) Cerebral pathways in processing of affective prosody: a dynamic causal modeling study. Neuroimage 30:580-587.
21. Fecteau S, Armony JL, Joanette Y, Belin P (2004) Is voice processing speciesspecific in human auditory cortex? An fMRI study. Neuroimage 23:840-848.
22. Fernald A (1989) Intonation and communicative intent in mothers' speech to infants: is the melody the message? Child Dev 60:1497-1510.
23. Fischl B, Sereno MI, Dale AM (1999) Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. Neuroimage 9:195-207.
24. Fitch WT, Neubauer J, Herzel H (2002) Calls out of chaos: the adaptive significance of nonlinear phenomena in mammalian vocal production. Anim Behav 63:407-418.
25. Friederici AD, Alter K (2004) Lateralization of auditory language functions: a dynamic dual pathway model. Brain Lang 89:267-276.
26. Friederici AD, Kotz SA, Scott SK, Obleser J (2010) Disentangling syntax and intelligibility in auditory language comprehension. Hum Brain Mapp 31:448-457.
27. Gannon PJ, Holloway RL, Broadfield DC, Braun AR (1998) Asymmetry of chimpanzee planum temporale: humanlike pattern of Wernicke's brain language area homolog. Science 279:220-222.
28. Gervais H, Belin P, Boddaert N, Leboyer M, Coez A, Sfaello I, Barthélémy C, Brunelle F, Samson Y, Zilbovicius M (2004) Abnormal cortical voice processing in autism. Nat Neurosci 7:801-802.
29. Gil-da-Costa R, Martin A, Lopes MA, Muñoz M, Fritz JB, Braun AR (2006) Species-specific calls activate homologs of Broca's and Wernicke's areas in the macaque. Nat Neurosci 9:1064-1070.
30. Glover GH, Law CS (2001) Spiral-in/out BOLD fMRI for increased SNR and reduced susceptibility artifacts. Magn Reson Med 46:515-522.
31. Grossmann T, Oberecker R, Koch SP, Friederici AD (2010) The developmental origins of voice processing in the human brain. Neuron 65:852-858.
32. Hall DA, Haggard MP, Akeroyd MA, Palmer AR, Summerfield AQ, Elliott MR, Gurney EM, Bowtell RW (1999) "Sparse" temporal sampling in auditory fMRI. Hum Brain Mapp 7:213-223.
33. Hauber ME, Cassey P, Woolley SM, Theunissen FE (2007) Neurophysiological response selectivity for conspecific songs over synthetic sounds in the auditory forebrain of non-singing female songbirds. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 193:765-774.
34. Hickok G, PoeppelD (2007) The cortical organization of speech processing. Nat Rev Neurosci 8:393-402.
35. Hill J, Dierker D, Neil J, Inder T, Knutsen A, Harwell J, Coalson T, Van Essen D (2010) Asurface-based analysis of hemispheric asymmetries and folding of cerebral cortex in term-born human infants. J Neurosci 30:2268-2276.
36. Hopkins WD, Marino L, Rilling JK, MacGregor LA (1998) Planum temporale asymmetries in great apes as revealed by magnetic resonance imaging (MRI). Neuroreport 9:2913-2918.
37. Jones SE, Mahmoud SY, Phillips MD (2011) A practical clinical method to quantify language lateralization in fMRI using whole-brain analysis. Neuroimage 54:2937-2949.
38. Kotz SA, Meyer M, Paulmann S (2006) Lateralization of emotional prosody in the brain: an overview and synopsis on the impact of study design. Prog Brain Res 156:285-294.
39. Kuhl PK (2007) Is speech learning 'gated' by the social brain? Dev Sci 10:110-120.
40. Kuhl PK (2010) Brain mechanisms in early language acquisition. Neuron 67:713-727.
41. Lass NJ, Eastham SK, Wright TL, Hinzman AR, Mills KJ, Hefferin AL (1983) Listeners' identification of human-imitated animal sounds. Percept Mot Skills 57:995-998.
42. Leech R, Holt LL, Devlin JT, Dick F (2009) Expertise with artificial nonspeech sounds recruits speech-sensitive cortical regions. J Neurosci 29:5234-5239.
43. Leroy F, Glasel H, Dubois J, Hertz-Pannier L, Thirion B, Mangin JF, Dehaene-Lambertz G (2011) Early maturation of the linguistic dorsal pathway in human infants. J Neurosci 31:1500-1506.
44. Lewis JW, Wightman FL, Brefczynski JA, Phinney RE, Binder JR, DeYoe EA (2004) Human brain regions involved in recognizing environmental sounds. Cereb Cortex 14:1008-1021.
45. Lewis JW, Brefczynski JA, Phinney RE, Janik JJ, DeYoe EA (2005) Distinct cortical pathways for processing tool versus animal sounds. J Neurosci 25:5148-5158.
46. Lewis JW, Talkington WJ, Walker NA, Spirou GA, Jajosky A, Frum C, Brefczynski-Lewis JA (2009) Human cortical organization for processing vocalizations indicates representation of harmonic structure as a signal attribute. J Neurosci 29:2283-2296.
47. Lewis JW, Talkington WJ, Tallaksen KC, Frum CA (2012) Auditory object salience: human cortical processing of non-biological action sounds and their acoustic signal attributes. Front Syst Neurosci 6:1-15. doi:10.3389/fnsys.2012.00027.
48. Liebenthal E, Desai R, Ellingson MM, Ramachandran B, Desai A, Binder JR (2010) Specialization along the left superior temporal sulcus for auditory categorization. Cereb Cortex 20:2958-2970.
49. Mastropieri D, Turkewitz G (1999) Prenatal experience and neonatal responsiveness to vocal expressions of emotion. Dev Psychobiol 35:204-214.
50. Morosan P, Rademacher J, Schleicher A, Amunts K, Schormann T, Zilles K (2001) Human primary auditory cortex: cytoarchitectonic subdivisions and mapping into a spatial reference system. Neuroimage 13:684-701.
51. Nunnally JC (1978) Psychometric theory. New York: McGraw-Hill.
52. Obleser J, Eisner F, Kotz SA (2008) Bilateral speech comprehension reflects differential sensitivity to spectral and temporal features. J Neurosci 28:8116-8123.
53. Petkov CI, Kayser C, Steudel T, Whittingstall K, Augath M, Logothetis NK (2008) A voice region in the monkey brain. Nat Neurosci 11:367-374.
54. Poremba A, Malloy M, Saunders RC, Carson RE, Herscovitch P, Mishkin M (2004) Species-specific calls evoke asymmetric activity in the monkey's temporal poles. Nature 427:448-451.
55. Rademacher J, Morosan P, Schormann T, Schleicher A, Werner C, Freund HJ, Zilles K (2001) Probabilistic mapping and volume measurement of human primary auditory cortex. Neuroimage 13:669-683.
56. Reddy RK, Ramachandra V, Kumar N, Singh NC (2009) Categorization of environmental sounds. Biol Cybern 100:299-306.
57. Riede T, Herzel H, Hammerschmidt K, Brunnberg L, Tembrock G (2001) The harmonic-to-noise ratio applied to dog barks. J Acoust Soc Am 110:2191-2197.
58. Rilling JK, Glasser MF, Preuss TM, Ma X, Zhao T, Hu X, Behrens TE (2008) The evolution of the arcuate fasciculus revealed with comparative DTI. Nat Neurosci 11:426-428.
59. Robins DL, Hunyadi E, Schultz RT (2009) Superior temporal activation in response to dynamic audio-visual emotional cues. Brain Cogn 69:269-278.
60. Ross ED, Monnot M (2008) Neurology of affective prosody and its functional-anatomic organization in right hemisphere. Brain Lang 104:51-74.
61. Saad ZS, Chen G, Reynolds RC, Christidis PP, Hammett KR, Bellgowan PSF, Cox RW (2006) Functional Imaging Analysis Contest (FIAC) analysis according to AFNI and SUMA. Hum Brain Mapp 27:417-424.
62. Scott SK, Blank CC, Rosen S, Wise RJ (2000) Identification of a pathway for intelligible speech in the left temporal lobe. Brain 123:2400-2406.
63. Shafer VL, Sussman E (2011) Predicting the future: ERP markers of language risk in infancy. Clin Neurophysiol 122:213-214.
64. Smith SM, Nichols TE (2009) Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage 44:83-98.
65. Taglialatela JP, Russell JL, Schaeffer JA, Hopkins WD (2009) Visualizing vocal perception in the chimpanzee brain. Cereb Cortex 19: 1151-1157.
66. Tian B, Reser D, Durham A, Kustov A, Rauschecker JP (2001) Functional specialization in rhesus monkey auditory cortex. Science 292:290-293.
67. Van Essen DC, Drury HA, Dickson J, Harwell J, Hanlon D, Anderson CH (2001) An integrated software suite for surface-based analyses of cerebral cortex. J Am Med Inform Assoc 8:443-459.
68. Wang X (2000) On cortical coding of vocal communication sounds in primates. Proc Natl Acad Sci U S A 97:11843-11849.
69. 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.
70. Wilson B, Petkov CI (2011) Communication and the primate brain: insights from neuroimaging studies in humans, chimpanzees and macaques. Hum Biol 83:175-189.
71. Zatorre RJ, Belin P (2001) Spectral and temporal processing in human auditory cortex. Cereb Cortex 11:946-953.