Interhemispheric differences in auditory processing revealed by fMRI in awake rhesus monkeys

Cerebral Cortex

Volumn 22, Issue 4, 2012, Pages 838-853

  Joly, Olivier ^a   Ramus, Franck ^b   Pressnitzer, Daniel ^c   Vanduffel, Wim ^a,d,e   Orban, Guy A ^a  

^a KU LEUVEN UNIVERSITY OF LEUVEN   (Belgium)

^b PSL RESEARCH UNIVERSITY   (France)

^c ECOLE NORMALE SUPÉRIEURE   (France)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

auditory cortex; conspecifics; functional imaging; spectrotemporal complexity; vocalizations

Indexed keywords

CONTRAST MEDIUM;

ANIMAL EXPERIMENT; ARTICLE; AUDITORY CORTEX; AUDITORY STIMULATION; BRAIN REGION; CONTROLLED STUDY; EMOTION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEARING; HEMISPHERIC DOMINANCE; LEFT HEMISPHERE; MALE; NONHUMAN; PRIORITY JOURNAL; RHESUS MONKEY; RIGHT HEMISPHERE; SPEECH; VOCALIZATION; WAKEFULNESS;

EID: 84859023964     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhr150     Document Type: Article

References (84)

1. Avants B, Epstein C, Grossman M, Gee J. 2008. Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain. Med Image Anal. 12:26-41.
2. Averbeck BB, Romanski LM. 2006. Probabilistic encoding of vocalizations in macaque ventral lateral prefrontal cortex. J Neurosci. 26:11023-11033.
3. Baumgart F, Kaulisch T, Tempelmann C, Gaschler-Markefski B, Tegeler C, Schindler F, Stiller D, Scheich H. 1998. Electrodynamic headphones and woofers for application in magnetic resonance imaging scanners. Med Phys. 25:2068-2070.
4. Belin P, Fecteau S, Charest I, Nicastro N, Hauser MD, Armony JL. 2008. Human cerebral response to animal affective vocalizations. Proc Biol Sci. 275:473-481.
5. Belin P, Zatorre RJ, Lafaille P, Ahad P, Pike B. 2000. Voice-selective areas in human auditory cortex. Nature. 403:309-312.
6. Bendor D, Wang X. 2005. The neuronal representation of pitch in primate auditory cortex. Nature. 436:1161-1165.
7. Bradbury JW, Vehrencamp SL. 1998. Principles of animal communication. Oxford: Blackwell.
8. Chi T, Ru P, Shamma SA. 2005. Multiresolution spectrotemporal analysis of complex sounds. J Acoust Soc Am. 118:887-906.
9. Cowey A, Dewson JH. 1972. Effects of unilateral ablation of superior temporal cortex on auditory sequence discrimination in Macaca mulatta. Neuropsychologia. 10:279-289.
10. Dehaene-Lambertz G, Pallier C, Serniclaes W, Sprenger-Charolles L, Jobert A, Dehaene S. 2005. Neural correlates of switching from auditory to speech perception. Neuroimage. 24:21-33.
11. Depireux DA, Simon JZ, Klein DJ, Shamma SA. 2001. Spectro-temporal response field characterization with dynamic ripples in ferret primary auditory cortex. J Neurophysiol. 85:1220-1234.
12. Dewson JH, Cowey A, Weiskrantz L. 1970. Disruptions of auditory sequence discrimination by unilateral and bilateral cortical ablations of superior temporal gyrus in the monkey. Exp Neurol. 28:529-548.
13. Dewson JH, Pribram KH, Lynch JC. 1969. Effects of ablations of temporal cortex upon speech sound discrimination in the monkey. Exp Neurol. 24:579-591.
14. Dhanjal NS, Handunnetthi L, Patel MC, Wise RJS. 2008. Perceptual systems controlling speech production. J Neurosci. 28:9969-9975.
15. Ehret G. 1987. Left hemisphere advantage in the mouse brain for recognizing ultrasonic communication calls. Nature. 325:249-251.
16. Ekstrom LB, Roelfsema PR, Arsenault JT, Bonmassar G, Vanduffel W. 2008. Bottom-up dependent gating of frontal signals in early visual cortex. Science. 321:414-417.
17. Falchier A, Clavagnier S, Barone P, Kennedy H. 2002. Anatomical evidence of multimodal integration in primate striate cortex. J Neurosci. 22:5749-5759.
18. Ferrari PF, Gallese V, Rizzolatti G, Fogassi L. 2003. Mirror neurons responding to the observation of ingestive and communicative mouth actions in the monkey ventral premotor cortex. Eur J Neurosci. 17:1703-1714.
19. Fischer J, Teufel C, Drolet M, Patzelt A, Rübsamen R, von Cramon DY, Schubotz RI. 2009. Orienting asymmetries and lateralized processing of sounds in humans. BMC Neurosci. 10:14.
20. Gannon PJ, Kheck N, Hof PR. 2008. Leftward interhemispheric asymmetry of macaque monkey temporal lobe language area homolog is evident at the cytoarchitectural, but not gross anatomic level. Brain Res. 1199:62-73.
21. Georgieva S, Peeters R, Kolster H, Todd JT, Orban GA. 2009. The processing of three-dimensional shape from disparity in the human brain. J Neurosci. 29:727-742.
22. 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. 28:4457-4469.
23. 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. 31:1807-1817.
24. Ghazanfar AA, Miller CT. 2006. Language evolution: loquacious monkey brains? Curr Biol. 16:R879-R881.
25. Ghazanfar AA, Smith-Rohrberg D, Hauser MD. 2001. The role of temporal cues in rhesus monkey vocal recognition: orienting asymmetries to reversed calls. Brain Behav Evol. 58:163-172.
26. Gifford GW, Hauser MD, Cohen YE. 2003. Discrimination of functionally referential calls by laboratory-housed rhesus macaques: implications for neuroethological studies. Brain Behav Evol. 61:213-224.
27. Gil-da-Costa R, Braun A, Lopes M, Hauser MD, Carson RE, Herscovitch P, Martin A. 2004. Toward an evolutionary perspective on conceptual representation: species-specific calls activate visual and affective processing systems in the macaque. Proc Natl Acad Sci USA. 101:17516-17521.
28. Gil-da-Costa R, Hauser MD. 2006. Vervet monkeys and humans show brain asymmetries for processing conspecific vocalizations, but with opposite patterns of laterality. Proc Biol Sci. 273:2313-2318.
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. Grunewald A, Linden JF, Andersen RA. 1999. Responses to auditory stimuli in macaque lateral intraparietal area. I. Effects of training. J Neurophysiol. 82:330-342.
31. Hackett TA, Preuss TM, Kaas JH. 2001. Architectonic identification of the core region in auditory cortex of macaques, chimpanzees, and humans. J Comp Neurol. 441:197-222.
32. Hackett TA, Stepniewska I, Kaas JH. 1998. Subdivisions of auditory cortex and ipsilateral cortical connections of the parabelt auditory cortex in macaque monkeys. J Comp Neurol. 394:475-495.
33. Hackett TA, Stepniewska I, Kaas JH. 1999. Prefrontal connections of the parabelt auditory cortex in macaque monkeys. Brain Res. 817:45-58.
34. Harrington IA, Heffner RS, Heffner HE. 2001. An investigation of sensory deficits underlying the aphasia-like behavior of macaques with auditory cortex lesions. Neuroreport. 12:1217-1221.
35. Hauser MD. 1996. The evolution of communication. Cambridge (MA): The MIT Press.
36. Hauser MD, Andersson K. 1994. Left hemisphere dominance for processing vocalizations in adult, but not infant, rhesus monkeys: field experiments. Proc Natl Acad Sci USA. 91:3946-3948.
37. Heffner HE, Heffner RS. 1984. Temporal lobe lesions and perception of species-specific vocalizations by macaques. Science. 226:75-76.
38. Heffner HE, Heffner RS. 1986. Hearing loss in Japanese macaques following bilateral auditory cortex lesions. J Neurophysiol. 55:256-271.
39. Heffner HE, Heffner RS. 1989. Effect of restricted cortical lesions on absolute thresholds and aphasia-like deficits in Japanese macaques. Behav Neurosci. 103:158-169.
40. Jesteadt W, Wier CC, Green DM. 1977. Intensity discrimination as a function of frequency and sensation level. J Acoust Soc Am. 61:169-177.
41. Joly O, Vanduffel W, Orban GA. 2009. The monkey ventral premotor cortex processes 3D shape from disparity. Neuroimage. 47:262-272.
42. Kaas JH, Hackett TA. 2000. Subdivisions of auditory cortex and processing streams in primates. Proc Natl Acad Sci USA. 97:11793-11799.
43. Kayser C, Logothetis NK. 2009. Directed interactions between auditory and superior temporal cortices and their role in sensory integration. Front Integr Neurosci. 3:7.
44. Klein A, Andersson J, Ardekani BA, Ashburner J, Avants B, Chiang MC, Christensen GE, Collins DL, Gee J, Hellier P, et al. 2009. Evaluation of 14 nonlinear deformation algorithms applied to human brain MRI registration. Neuroimage. 46:786-802
45. Kohler E, Keysers C, Umiltà MA, Fogassi L, Gallese V, Rizzolatti G. 2002. Hearing sounds, understanding actions: action representation in mirror neurons. Science. 297:846-848.
46. Kovacs S, Peeters R, Smits M, De Ridder D, Van Hecke P, Sunaert S. 2006. Activation of cortical and subcortical auditory structures at 3 T by means of a functional magnetic resonance imaging paradigm suitable for clinical use. Invest Radiol. 41:87-96.
47. Leite FP, Tsao D, Vanduffel W, Fize D, Sasaki Y, Wald LL, Dale AM, Kwong KK, Orban GA, Rosen BR, et al. 2002. Repeated fMRI using iron oxide contrast agent in awake, behaving macaques at 3 Tesla. Neuroimage. 16:283-294.
48. May B, Moody D, Stebbins W. 1988. The significant features of Japanese macaque coo sounds: a psychophysical study. Anim Behav. 36:1432-1444.
49. May B, Moody D, Stebbins W. 1989. Categorical perception of conspecific communication sounds by Japanese macaques, Macaca fuscata. J Acoust Soc Am. 85:837.
50. Mazzoni P, Bracewell RM, Barash S, Andersen RA. 1996. Spatially tuned auditory responses in area lip of macaques performing delayed memory saccades to acoustic targets. J Neurophysiol. 75:1233-1241.
51. McLaren DG, Kosmatka KJ, Oakes TR, Kroenke CD, Kohama SG, Matochik JA, Ingram DK, Johnson SC. 2009. A population-average MRI-based atlas collection of the rhesus macaque. Neuroimage. 45:52-59.
52. Narain C, Scott SK, Wise RJS, Rosen S, Leff A, Iversen SD, Matthews PM. 2003. Defining a left-lateralized response specific to intelligible speech using fMRI. Cereb Cortex. 13:1362-1368.
53. Nelissen K, Vanduffel W, Orban GA. 2006. Charting the lower superior temporal region, a new motion-sensitive region in monkey superior temporal sulcus. J Neurosci. 26:5929-5947.
54. Patterson RD, Allerhand MH, Giguère C. 1995. Time-domain modeling of peripheral auditory processing: a modular architecture and a software platform. J Acoust Soc Am. 98:1890-1894.
55. Petersen MR, Beecher MD, Zoloth SR, Moody DB, Stebbins WC. 1978. Neural lateralization of species-specific vocalizations by Japanese macaques (Macaca fuscata). Science. 202:324-327.
56. Petkov CI, Kayser C, Augath M, Logothetis NK. 2006. Functional imaging reveals numerous fields in the monkey auditory cortex. PLoS Biol. 4:e215.
57. 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.
58. Poeppel D, Guillemin A, Thompson J, Fritz J, Bavelier D, Braun AR. 2004. Auditory lexical decision, categorical perception, and FM direction discrimination differentially engage left and right auditory cortex. Neuropsychologia. 42:183-200.
59. 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.
60. Poremba A, Saunders RC, Crane AM, Cook M, Sokoloff L, Mishkin M. 2003. Functional mapping of the primate auditory system. Science. 299:568-572.
61. Rauschecker JP. 1998. Parallel processing in the auditory cortex of primates. Audiol Neurootol. 3(2-3):86-103.
62. Rauschecker JP, Scott SK. 2009. Maps and streams in the auditory cortex: nonhuman primates illuminate human speech processing. Nat Neurosci. 12:718-724.
63. Rauschecker JP, Tian B. 2000. Mechanisms and streams for processing of "what" and "where" in auditory cortex. Proc Natl Acad Sci USA. 97:11800-11806.
64. Rauschecker JP, Tian B, Hauser M. 1995. Processing of complex sounds in the macaque nonprimary auditory cortex. Science. 268:111-114.
65. Remedios R, Logothetis NK, Kayser C. 2009. An auditory region in the primate insular cortex responding preferentially to vocal communication sounds. J Neurosci. 29:1034-1045.
66. Romanski LM, Averbeck BB. 2009. The primate cortical auditory system and neural representation of conspecific vocalizations. Annu Rev Neurosci. 32:315-346.
67. Romanski LM, Averbeck BB, Diltz M. 2005. Neural representation of vocalizations in the primate ventrolateral prefrontal cortex. J Neurophysiol. 93:734-747.
68. Romanski LM, Tian B, Fritz J, Mishkin M, Goldman-Rakic PS, Rauschecker JP. 1999. Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex. Nat Neurosci. 2:1131-1136.
69. Ruggero MA, Temchin AN. 2005. Unexceptional sharpness of frequency tuning in the human cochlea. Proc Natl Acad Sci USA. 102:18614-18619.
70. Russ BE, Ackelson AL, Baker AE, Cohen YE. 2008. Coding of auditorystimulus identity in the auditory non-spatial processing stream. J Neurophysiol. 99:87-95.
71. Saleem K, Logothetis N. 2006. A combined MRI and histology Atlas of the Rhesus monkey brain. San Diego (CA): Academic Press.
72. Samson F, Zeffiro TA, Toussaint A, Belin P. 2011. Stimulus complexity and categorical effects in human auditory cortex: an activation likelihood estimation meta-analysis. Front. Psychology. 1:241.
73. Schroeder CE, Lakatos P, Kajikawa Y, Partan S, Puce A. 2008. Neuronal oscillations and visual amplification of speech. Trends Cogn Sci. 12:106-113.
74. Scott SK, Blank CC, Rosen S, Wise RJ. 2000. Identification of a pathway for intelligible speech in the left temporal lobe. Brain. 123(Pt 12):2400-2406.
75. Serafin JV, Moody DB, Stebbins WC. 1982. Frequency selectivity of the monkey's auditory system: psychophysical tuning curves. J Acoust Soc Am. 71:1513-1518.
76. Spitsyna G, Warren JE, Scott SK, Turkheimer FE, Wise RJS. 2006. Converging language streams in the human temporal lobe. J Neurosci. 26:7328-7336.
77. Steinschneider M, Schroeder CE, Arezzo JC, Vaughan HG. 1994. Speechevoked activity in primary auditory cortex: effects of voice onset time. Electroencephalogr Clin Neurophysiol. 92:30-43.
78. Sugihara T, Diltz MD, Averbeck BB, Romanski LM. 2006. Integration of auditory and visual communication information in the primate ventrolateral prefrontal cortex. J Neurosci. 26:11138-11147.
79. Teufel C, Ghazanfar AA, Fischer J. 2010. On the relationship between lateralized brain function and orienting asymmetries. Behav Neurosci. 124:437-445.
80. Tian B, Rauschecker JP. 2004. Processing of frequency-modulated sounds in the lateral auditory belt cortex of the rhesus monkey. J Neurophysiol. 92:2993-3013.
81. Tian B, Reser D, Durham A, Kustov A, Rauschecker JP. 2001. Functional specialization in rhesus monkey auditory cortex. Science. 292:290-293.
82. Vanduffel W, Fize D, Mandeville JB, Nelissen K, Hecke PV, Rosen BR, Tootell RB, Orban GA. 2001. Visual motion processing investigated using contrast agent-enhanced fMRI in awake behaving monkeys. Neuron. 32:565-577.
83. Wetzel W, Wagner T, Ohl FW, Scheich H. 1998. Categorical discrimination of direction in frequency-modulated tones by mongolian gerbils. Behav Brain Res. 91:29-39.
84. Wilke M, Lidzba K. 2007. LI-tool: a new toolbox to assess lateralization in functional MR-data. J Neurosci Methods. 163:128-136.