Auditory and visual modulation of temporal lobe neurons in voice-sensitive and association cortices

Journal of Neuroscience

Volumn 34, Issue 7, 2014, Pages 2524-2537

  Perrodin, Catherine ^a   Kayser, Christoph ^a,b   Logothetis, Nikos K ^a,c   Petkov, Christopher I ^a,d  

^a MAX PLANCK INSTITUTE FOR BIOLOGICAL CYBERNETICS   (Germany)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Audiovisual; Congruency; Face; Multisensory; Primate; Voice

Indexed keywords

AUDIOVISUAL; CONGRUENCY; FACE; MULTISENSORY; PRIMATE; VOICE;

ACOUSTIC STIMULATION; ANIMALS; AUDITORY PERCEPTION; BRAIN MAPPING; MACACA MULATTA; MAGNETIC RESONANCE IMAGING; MALE; NEURONS; PHOTIC STIMULATION; TEMPORAL LOBE; VISUAL PERCEPTION;

EID: 84893672565     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2805-13.2014     Document Type: Article

References (69)

1. Avillac M, Ben Hamed S, Duhamel JR (2007) Multisensory integration in the ventral intraparietal area of the macaque monkey. J Neurosci 27:1922-1932. CrossRef Medline
2. Barraclough NE, Xiao D, Baker CI, Oram MW, Perrett DI (2005) Integration of visual and auditory information by superior temporal sulcus neurons responsive to the sight of actions. J Cogn Neurosci 17:377-391. CrossRef Medline
3. Beauchamp MS, Argall BD, Bodurka J, Duyn JH, Martin A (2004a) Unraveling multisensory integration: patchy organization within human STS multisensory cortex. Nat Neurosci 7:1190-1192. CrossRef Medline
4. Beauchamp MS, Lee KE, Argall BD, Martin A (2004b) Integration of auditory and visual information about objects in superior temporal sulcus. Neuron 41:809-823. CrossRef Medline
5. Belin P, Zatorre RJ (2003) Adaptation to speaker's voice in right anterior temporal lobe. Neuroreport 14:2105-2109. CrossRef Medline
6. Belin P, Zatorre RJ, Lafaille P, Ahad P, Pike B (2000) Voice-selective areas in human auditory cortex. Nature 403:309-312. CrossRef Medline
7. Belin P, Zatorre RJ, Ahad P (2002) Human temporal-lobe response to vocal sounds. Brain Res Cogn Brain Res 13:17-26. CrossRef Medline
8. Benevento LA, Fallon J, Davis BJ, Rezak M (1977) Auditory-visual interaction in single cells in the cortex of the superior temporal sulcus and the orbital frontal cortex of the macaque monkey. Exp Neurol 57:849-872. CrossRef Medline
9. Benjamini YHY (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289-300.
10. Bizley JK, Nodal FR, Bajo VM, Nelken I, King AJ (2007) Physiological and anatomical evidence for multisensory interactions in auditory cortex. Cereb Cortex 17:2172-2189. CrossRef Medline
11. Blank H, Anwander A, von Kriegstein K (2011) Direct structural connections between voice-and face-recognition areas. J Neurosci 31:12906-12915. CrossRef Medline
12. Bruce C, Desimone R, Gross CG (1981) Visual properties of neurons in a polysensory area in superior temporal sulcus of the macaque. J Neurophysiol 46:369-384. Medline
13. Calvert GA, Campbell R, Brammer MJ (2000) Evidence from functional magnetic resonance imaging of cross-modal binding in the human heteromodal cortex. Curr Biol 10:649-657. CrossRef Medline
14. Campanella S, Belin P (2007) Integrating face and voice in person perception. Trends Cogn Sci 11:535-543. CrossRef Medline
15. Chen A, Deangelis GC, Angelaki DE (2013) Functional specializations of the ventral intraparietal area for multisensory heading discrimination. J Neurosci 33:3567-3581. CrossRef Medline
16. Cipolloni PB, Pandya DN (1989) Connectional analysis of the ipsilateral and contralateral afferent neurons of the superior temporal region in the rhesus monkey. J Comp Neurol 281:567-585. CrossRef Medline
17. Dahl CD, Logothetis NK, Kayser C (2009) Spatial organization of multisensory responses in temporal association cortex. J Neurosci 29:11924-11932. CrossRef Medline
18. Dahl CD, Logothetis NK, Kayser C (2010) Modulation of visual responses in the superior temporal sulcus by audio-visual congruency. Front Integr Neurosci 4:10. CrossRef Medline
19. Ellis HD, Jones DM, Mosdell N (1997) Intra-and inter-modal repetition priming of familiar faces and voices. Br J Psychol 88:143-156. CrossRef Medline
20. Fitch WT, Fritz JB (2006) Rhesus macaques spontaneously perceive formants in conspecific vocalizations. J Acoust Soc Am 120:2132-2141. CrossRef Medline
21. Formisano E, De Martino F, Bonte M, Goebel R (2008) "Who" is saying "what?" Brain-based decoding of human voice and speech. Science 322: 970-973. CrossRef Medline
22. Fuster JM, Bodner M, Kroger JK (2000) Cross-modal and cross-temporal association in neurons of frontal cortex. Nature 405:347-351. CrossRef Medline
23. Galaburda AM, Pandya DN (1983) The intrinsic architectonic and connectional organization of the superior temporal region of the rhesus monkey. J Comp Neurol 221:169-184. CrossRef Medline
24. Ghazanfar AA, Schroeder CE (2006) Is neocortex essentially multisensory? Trends Cogn Sci 10:278-285. CrossRef Medline
25. Ghazanfar AA, Maier JX, Hoffman KL, Logothetis NK (2005) Multisensory integration of dynamic faces and voices in rhesus monkey auditory cortex. J Neurosci 25:5004-5012. CrossRef Medline
26. Ghazanfar AA, Turesson HK, Maier JX, van Dinther R, Patterson RD, Logothetis NK (2007) Vocal tract resonances as indexical cues in rhesus monkeys. Curr Biol 17:425-430. CrossRef Medline
27. 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. CrossRef Medline
28. Kaas JH, Hackett TA (1998) Subdivisions of auditory cortex and levels of processing in primates. Audiol Neurootol 3:73-85. CrossRef Medline
29. Kaas JH, Hackett TA (2000) Subdivisions of auditory cortex and processing streams in primates. Proc Natl Acad Sci U S A 97:11793-11799. CrossRef Medline
30. Kaposvari P, Csibri P, Csete G, Tompa T, Sary G (2011) Auditory modulation of the inferior temporal cortex neurons in rhesus monkey. Physiol Res 60 [Suppl 1]:S93-S99.
31. Kayser C, Logothetis NK (2007) Do early sensory cortices integrate crossmodal information? Brain Struct Funct 212:121-132. CrossRef Medline
32. Kayser C, Petkov CI, Augath M, Logothetis NK (2007) Functional imaging reveals visual modulation of specific fields in auditory cortex. J Neurosci 27:1824-1835. CrossRef Medline
33. Kayser C, Petkov CI, Logothetis NK (2008) Visual modulation of neurons in auditory cortex. Cereb Cortex 18:1560-1574. CrossRef Medline
34. Kikuchi Y, Horwitz B, Mishkin M (2010) Hierarchical auditory processing directed rostrally along the monkey's supratemporal plane. J Neurosci 30:13021-13030. CrossRef Medline
35. Lakatos P, Chen CM, O'Connell MN, Mills A, Schroeder CE (2007) Neuronal oscillations and multisensory interaction in primary auditory cortex. Neuron 53:279-292. CrossRef Medline
36. Lakatos P, O'Connell MN, Barczak A, Mills A, Javitt DC, Schroeder CE (2009) The leading sense: supramodal control of neurophysiological context by attention. Neuron 64:419-430. CrossRef Medline
37. Linden JF, Grunewald A, Andersen RA (1999) Responses to auditory stimuli in macaque lateral intraparietal area: II. Behavioral modulation. J Neurophysiol 82:343-358. Medline
38. Maunsell JH, Newsome WT (1987) Visual processing in monkey extrastriate cortex. Annu Rev Neurosci 10:363-401. CrossRef Medline
39. Mesgarani N, Chang EF (2012) Selective cortical representation of attended speaker in multi-talker speech perception. Nature 485:233-236. CrossRef Medline
40. Mitchell JF, Sundberg KA, Reynolds JH (2007) Differential attentiondependent response modulation across cell classes in macaque visual area V4. Neuron 55:131-141. CrossRef Medline
41. Müller VI, Habel U, Derntl B, Schneider F, Zilles K, Turetsky BI, Eickhoff SB (2011) Incongruence effects in cross-modal emotional integration. Neuroimage 54:2257-2266. CrossRef Medline
42. Pandya DN, Hallett M, Kmukherjee SK (1969) Intra-and interhemispheric connections of the neocortical auditory system in the rhesus monkey. Brain Res 14:49-65. CrossRef Medline
43. Perrodin C, Kayser C, Logothetis NK, Petkov CI (2011) Voice cells in the primate temporal lobe. Curr Biol 21:1408-1415. CrossRef Medline
44. Petkov CI, Kayser C, Augath M, Logothetis NK (2006) Functional imaging reveals numerous fields in the monkey auditory cortex. PLo S Biol 4:e215. CrossRef Medline
45. 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. CrossRef Medline
46. 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. CrossRef Medline
47. Rauschecker JP, Tian B, Pons T, Mishkin M (1997) Serial and parallel processing in rhesus monkey auditory cortex. J Comp Neurol 382:89-103. CrossRef Medline
48. Romanski LM (2007) Representation and integration of auditory and visual stimuli in the primate ventral lateral prefrontal cortex. Cereb Cortex 17 [Suppl 1]:i61-i69.
49. Romanski LM, Giguere M, Bates JF, Goldman-Rakic PS (1997) Topographic organization of medial pulvinar connections with the prefrontal cortex in the rhesus monkey. J Comp Neurol 379:313-332. CrossRef Medline
50. Romanski LM, Bates JF, Goldman-Rakic PS (1999a) Auditory belt and parabelt projections to the prefrontal cortex in the rhesus monkey. J Comp Neurol 403:141-157. CrossRef Medline
51. Romanski LM, Tian B, Fritz J, Mishkin M, Goldman-Rakic PS, Rauschecker JP (1999b) Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex. Nat Neurosci 2:1131-1136. CrossRef Medline
52. Romanski LM, Averbeck BB, Diltz M (2005) Neural representation of vocalizations in the primate ventrolateral prefrontal cortex. J Neurophysiol 93:734-747. CrossRef Medline
53. Ross LA, Saint-Amour D, Leavitt VM, Javitt DC, Foxe JJ (2007) Do you see what I am saying? Exploring visual enhancement of speech comprehension in noisy environments. Cereb Cortex 17:1147-1153. CrossRef Medline
54. Schroeder CE, Foxe J (2005) Multisensory contributions to low-level, 'unisensory' processing. Curr Opin Neurobiol 15:454-458. CrossRef Medline
55. Schroeder CE, Foxe JJ (2002) The timing and laminar profile of converging inputs to multisensory areas of the macaque neocortex. Brain Res Cogn Brain Res 14:187-198. CrossRef Medline
56. Schroeder CE, Smiley J, Fu KG, McGinnis T, O'Connell MN, Hackett TA (2003) Anatomical mechanisms and functional implications of multisensory convergence in early cortical processing. Int J Psychophysiol 50: 5-17. CrossRef Medline
57. Seltzer B, Pandya DN (1994) Parietal, temporal, and occipital projections to cortex of the superior temporal sulcus in the rhesus monkey: a retrograde tracer study. J Comp Neurol 343:445-463. CrossRef Medline
58. Sergent J, Ohta S, MacDonald B (1992) Functional neuroanatomy of face and object processing: a positron emission tomography study. Brain 115: 15-36. CrossRef Medline
59. Sokal RR, Rohlf FJ (1995) Biometry. New York: W.H. Freeman.
60. Stanford TR, Quessy S, Stein BE (2005) Evaluating the operations underlying multisensory integration in the cat superior colliculus. J Neurosci 25:6499-6508. CrossRef Medline
61. Stein BE, Stanford TR (2008) Multisensory integration: current issues from the perspective of the single neuron. Nat Rev Neurosci 9:255-266. CrossRef Medline
62. 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. CrossRef Medline
63. Tsao DY, Moeller S, Freiwald WA (2008) Comparing face patch systems in macaques and humans. Proc Natl Acad Sci U S A 105:19514-19519. CrossRef Medline
64. von Kriegstein K, Giraud AL (2004) Distinct functional substrates along the right superior temporal sulcus for the processing of voices. Neuroimage 22:948-955. CrossRef Medline
65. von Kriegstein K, Eger E, Kleinschmidt A, Giraud AL (2003) Modulation of neural responses to speech by directing attention to voices or verbal content. Brain Res Cogn Brain Res 17:48-55. CrossRef Medline
66. von Kriegstein K, Kleinschmidt A, Sterzer P, Giraud AL (2005) Interaction of face and voice areas during speaker recognition. J Cogn Neurosci 17: 367-376. CrossRef Medline
67. Werner S, Noppeney U (2010a) Distinct functional contributions of primary sensory and association areas to audiovisual integration in object categorization. J Neurosci 30:2662-2675. CrossRef Medline
68. Werner S, Noppeney U (2010b) Superadditive responses in superior temporal sulcus predict audiovisual benefits in object categorization. Cereb Cortex 20:1829-1842. CrossRef Medline
69. Zion Golumbic EM, Ding N, Bickel S, Lakatos P, Schevon CA, McKhann GM, Goodman RR, Emerson R, Mehta AD, Simon JZ, Poeppel D, Schroeder CE (2013) Mechanisms underlying selective neuronal tracking of attended speech at a "cocktail party. " Neuron 77:980-991. CrossRef