Are non-human primates capable of rhythmic entrainment? Evidence for the gradual audiomotor evolution hypothesis

Frontiers in Neuroscience

Volumn , Issue 8 JAN, 2014, Pages

  Merchant, Hugo ^a   Honing, Henkjan ^b  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Interval timing; Macaques; Music origins; Rhythmic entrainment

Indexed keywords

ARTICLE; AUDITORY SYSTEM; BODY MOVEMENT; CLASSIFICATION; COGNITION; CONNECTOME; DANCING; DEPTH PERCEPTION; EVENT RELATED POTENTIAL; GRADUAL AUDIOMOTOR EVOLUTION; HUMAN; HUMAN VERSUS ANIMAL COMPARISON; INTERCEPTION; INTERVAL BASED TIMING; INTERVAL REPRODUCTION; LEARNING; MACACA; MACACA FUSCATA; MOTOR CORTICO BASAL GANGLIA THALAMO CORTICAL CIRCUIT; MOTOR SYSTEM; MUSIC; NONHUMAN; PSYCHOMOTOR DEVELOPMENT; RHESUS MONKEY; RHYTHM; RHYTHMIC ENTRAINMENT; SENSORIMOTOR FUNCTION; SENSORIMOTOR INTEGRATION; SPECIES DIFFERENCE; TIME; VOCAL LEARNING;

EID: 84896791193     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2013.00274     Document Type: Article

References (86)

1. Alexander, G. E., DeLong, M. R., and Strick, P. L. (1986). Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu. Rev. Neurosci. 9, 357-381. doi: 10.1146/annurev.ne.09.030186.002041.
2. Bartolo, R., Prado, L., and Merchant, H. (in press). Information processing in the primate basal ganglia during sensory guided and internally driven rhythmic tapping. J. Neurosci.
3. Bertelson, P., and Aschersleben, G. (2003). Temporal ventriloquism: crossmodal interaction on the time dimension: 1. evidence from auditory-visual temporal order judgment. Int. J. Psychophysiol. 50, 147-155.
4. Borgmann, S., and Jürgens, U. (1999). Lack of cortico-striatal projections from the primary auditory cortex in the squirrel monkey. Brain Res. 836, 225-228. doi: 10.1016/S0006-8993(99)01704-7.
5. Britten, K. H., Shadlen, M. N., Newsome, W. T., and Movshon, J. A. (1992). The analysis of visual motion: a comparison of neuronal and psychophysical performance. J. Neurosci. 12, 4745-4765.
6. Brodsky, W., Henik, A., Rubinstein, B. S., and Zorman, M. (2003). Auditory imagery from musical notation in expert musicians. Percept. Psychophys. 65, 602-612. doi: 10.3758/BF03194586.
7. Buneo, C. A., Jarvis, M. R., Batista, A. P., and Andersen, R. A. (2002). Direct visuomotor transformations for reaching. Nature 416, 632-636. doi: 10.1038/416632a.
8. Catani, M., and Jones, D. K. (2005). Perisylvian language networks of the human brain. Ann. Neurol. 57, 8-16. doi: 10.1002/ana.20319.
9. Cook, P., Rouse, A., Wilson, M., and Reichmuth, C. (2013). A california sea lion (Zalophus californianus) can keep the beat: motor entrainment to rhythmic auditory stimuli in a non vocal mimic. J. Comp. Psychol. 127, 412-427. doi: 10.1037/a0032345.
10. Coull, J. T., Cheng, R. K., and Meck, W. H. (2011). Neuroanatomical and neurochemical substrates of timing. Neuropsychopharmacology 36, 3-25. doi: 10.1038/npp.2010.113.
11. Dehaene, S., and Changeux, J. P. (1997). A hierarchical neuronal network for planning behavior. Proc. Natl. Acad. Sci. U.S.A. 94, 13293-13298. doi: 10.1073/pnas.94.24.13293.
12. Donnet, S., Bartolo, R., Fernandes, J. M., Cunha, J. P., Prado, L., and Merchant, H. (in press). Monkeys temporalize their movement pauses and not their movement kinematics during a synchronization-continuation rhythmic task. J. Neurophysiol.
13. Drake, C., Jones, M. R., and Baruch, C. (2000). The development of rhythmic attending in auditory sequences: attunement, referent period, focal attending. Cognition 77, 251-288. doi: 10.1016/S0010-0277(00)00106-2.
14. Fortes, A. F., Merchant, H., and Georgopoulos, A. P. (2004). Comparative and categorical spatial judgments in the monkey: "high" and "low." Anim. Cogn. 7, 101-108. doi: 10.1007/s10071-003-0195-6.
15. Fitch, W. T. (2009). Biology of music: another one bites the dust. Curr. Biol. 19, 403-404. doi: 10.1016/j.cub.2009.04.004.
16. Fritz, J., Mishkin, M., and Saunders, R. C. (2005). In search of an auditory engram. Proc. Natl. Acad. Sci. U.S.A. 102, 9359-9364. doi: 10.1073/pnas.0503998102.
17. Georgopoulos, A. P., Lurito, J. T., Petrides, M., Schwartz, A. B., and Massey, J. T. (1989). Mental rotation of the neuronal population vector. Science 243, 234-236. doi: 10.1126/science.2911737.
18. Georgopoulos, A. P., Schwartz, A. B., and Kettner, R. E. (1986). Neuronal population coding of movement direction. Science 233, 1416-1419. doi: 10.1126/science.3749885.
19. Gibbon, J., Malapani, C., Dale, C. L., and Gallistel, C. R. (1997). Toward a neurobiology of temporal cognition: advances and challenges. Curr. Opin. Neurobiol. 7, 170-184. doi: 10.1016/S0959-4388(97)80005-0.
20. Grafton, S. T., Hazeltine, E., and Ivry, R. (1995). Functional mapping of sequence learning in normal humans. J. Cogn. Neurosci. 7, 497-510. doi: 10.1162/jocn.1995.7.4.497.
21. Grahn, J. A., and Brett, M. (2007). Rhythm and beat perception in motor areas of the brain. J. Cogn. Neurosci. 19, 893-906. doi: 10.1162/jocn.2007.19.5.893.
22. Graybiel, A. M. (2008). Habits, rituals, and the evaluative brain. Annu. Rev. Neurosci. 31, 359-387. doi: 10.1146/annurev.neuro.29.051605.112851.
23. Grondin, S., Ivry, R. B., Franz, E., Perreault, L., and Metthe, L. (1996). Markers' influence on the duration discrimination of intermodal intervals. Percept. Psychophys. 58, 424-433. doi: 10.3758/BF03206818.
24. Grube, M., Cooper, F. E., Chinnery, P. F., and Griffiths, T. D. (2010). Dissociation of duration-based and beat-based auditory timing in cerebellar degeneration. Proc. Natl. Acad. Sci. U.S.A. 107, 11597-11601. doi: 10.1073/pnas.0910473107.
25. Guttman, S. E., Gilroy, L. A., and Blake, R. (2005). Hearing what the eyes see auditory encoding of visual temporal sequences. Psychol. Sci. 16, 228-235. doi: 10.1111/j.0956-7976.2005.00808.x.
26. Harrington, D. L., Zimbelman, J. L., Hinton, S. C., and Rao, S. M. (2010). Neural modulation of temporal encoding, maintenance, and decision processes. Cereb. Cortex 20, 1274-1285. doi: 10.1093/cercor/bhp194.
27. Hasegawa, A., Okanoya, K., Hasegawa, T., and Seki, Y. (2011). Rhythmic synchronization tapping to an audio-visual metronome in budgerigars. Sci. Rep. 1, 1-8. doi: 10.1038/srep00120.
28. Hattori, Y., Tomonaga, M., and Matsuzawa, T. (2013). Spontaneous synchronized tapping to an auditory rhythm in a chimpanzee. Sci. Rep. 3, 1566. doi: 10.1038/srep01566.
29. Hikosaka, O., Nakahara, H., Rand, M. K., Sakai, K., Lu, X., Nakamura, K., et al. (1999). Parallel neural networks for learning sequential procedures. Trends Neurosci. 22, 464-471. doi: 10.1016/S0166-2236(99)01439-3.
30. Hikosaka, O., Rand, M., Nakamura, K., Miyachi, S., Kitaguchi, K., Sakai, K., et al. (2002). Long-term retention of motor skill in macaque monkeys and humans. Exp. Brain Res. 147, 494-504. doi: 10.1007/s00221-002-1258-7.
31. Honing, H. (2012). Without it no music: beat induction as a fundamental musical trait. Ann. N.Y. Acad. Sci. 1252, 85-91. doi: 10.1111/j.1749-6632.2011.06402.x.
32. Honing, H. (2013). "The structure and interpretation of rhythm in music," in Psychology of Music, 3rd Edn., ed D. Deutsch (London: Academic Press), 369-404.
33. Honing, H., Ladinig, O., Winkler, I., and Háden, G. (2009). Is beat induction innate or learned? Probing emergent meter perception in adults and newborns using event-related brain potentials (ERP). Ann. N.Y. Acad. Sci. 1169, 93-96. doi: 10.1111/j.1749-6632.2009.04761.x.
34. Honing, H., Merchant, H., Háden, G., Prado, L. A., and Bartolo, R. (2012). Rhesus monkeys (Macaca mulatta) can detect rhythmic groups in music, but not the beat. PLoS ONE 7:e51369. doi: 10.1371/journal.pone.0051369.
35. Hubel, D. H., and Wiesel, T. N. (1968). Receptive fields and functional architecture of monkey striate cortex. J. Physiol. 195, 215-243.
36. Jäncke, L., Loose, R., Lutz, K., Specht, K., and Shah, N. J. (2000). Cortical activations during paced finger-tapping applying visual and auditory pacing stimuli. Brain Res. Cogn. Brain Res. 10, 51-66. doi: 10.1016/S0926-6410(00)00022-7.
37. Koechlin, E., and Jubault, T. (2006). Broca's area and the hierarchical organization of human behavior. Neuron 50, 963-974. doi: 10.1016/j.neuron.2006.05.017.
38. Kourtzi, Z., Tolias, A. S., Altmann, C. F., Augath, M., and Logothetis, N. K. (2003). Integration of local features into global shapes: monkey and human FMRI studies. Neuron 37, 333-346. doi: 10.1167/3.9.191.
39. Konoike, N., Mikami, A., and Miyachi, S. (2012). The influence of tempo upon the rhythmic motor control in macaque monkeys. Neurosci. Res. 74, 64-67. doi: 10.1016/j.neures.2012.06.002.
40. Large, E. W., and Jones, M. R. (1999). The dynamics of attending: how people track time-varying events. Psychol. Rev. 10, 119-159. doi: 10.1037/0033-295X.106.1.119.
41. Large, E. W. (2000). On synchronizing movements to music. Hum. Mov. Sci. 19, 527-566. doi: 10.1016/S0167-9457(00)00026-9.
42. Large, E. W., and Palmer, C. (2002). Perceiving temporal regularity in music. Cogn. Sci. 26, 1-37. doi: 10.1016/S0364-0213(01)00057-X.
43. Leaver, A., van Lare, J. E., Zielinski, B. A., Halpern, A., and Rauschecker, J. P. (2009). Brain activation during anticipation of sound sequences. J. Neurosci. 29, 2477-2485. doi: 10.1523/JNEUROSCI.4921-08.2009.
44. Matsuzaka, Y., and Tanji, J. (1996). Changing directions of forthcoming arm movements: neuronal activity in the presupplementary and supplementary motor area of monkey cerebral cortex. J. Neurophysiol. 76, 2327-2342.
45. Mendez, J. C., Prado, L., Mendoza, G., and Merchant, H. (2011). Temporal and spatial categorization in human and non-human primates. Front. Integr. Neurosci. 5:50. doi: 10.3389/fnint.2011.00050.
46. Merchant, H., Battaglia-Mayer, A., and Georgopoulos, A. P. (2003). Interception of real and apparent circularly moving targets: psychophysics in human subjects and monkeys. Exp. Brain Res. 152, 106-112. doi: 10.1007/s00221-003-1514-5.
47. Merchant, H., Fortes, A. F., and Georgopoulos, A. P. (2004). Short-term memory effects on the representation of two-dimensional space in the rhesus monkey. Anim. Cogn. 7, 133-143. doi: 10.1007/s10071-003-0201-z.
48. Merchant, H., Harrington, D., and Meck, W. H. (2013a). Neural basis of the perception and estimation of time. Ann. Rev. Neurosci. 36, 313-336. doi: 10.1146/annurev-neuro-062012-170349.
49. Merchant, H., Pérez, O., Zarco, W., and Gámez, J. (2013b). Interval tuning in the primate medial premotor cortex as a general timing mechanism. J. Neurosci. 33, 9082-9096. doi: 10.1523/JNEUROSCI.5513-12.2013.
50. Merchant, H., Zarco, W., Perez, O., Prado, L., and Bartolo, R. (2011). Measuring time with multiple neural chronometers during a synchronization-continuation task. Proc. Natl. Acad. Sci. U.S.A. 108, 19784-19789. doi: 10.1073/pnas.1112933108.
51. Merchant, H., Zarco, W., Prado, L., and Perez, O. (2009). Behavioral and neurophysiological aspects of target interception. Adv. Exp. Med. Biol. 629, 201-220. doi: 10.1007/978-0-387-77064-2_10.
52. Merchant, H., Zarco, W., and Prado, L. (2008). Do we have a common mechanism for measuring time in the hundreds of millisecond range? Evidence from multiple-interval timing tasks. J. Neurophysiol. 99, 939-949. doi: 10.1152/jn.01225.2007.
53. Merchant, H., and de Lafuente, V. (in press). "Introduction to the neurobiology of interval timing," in Neurobiology of Interval Timing, eds H. Merchant and V. de Lafuente (New York, NY: Springer Editorial System).
54. Mountcastle, V. B., Lynch, J. C., Georgopoulos, A. P., Sakata, H., and Acuna, C. (1975). Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space. J. Neurophysiol. 38, 871-908.
55. Murray, E. A., and Mishkin, M. (1984). Severe tactual as well as visual memory deficits follow combined removal of the amygdala and hippocampus in monkeys. J. Neurosci. 4, 2565-2580.
56. Nagasaka, Y., Chao, Z. C., Hasegawa, N., Notoya, T., and Fujii, N. (2013). Spontaneous synchronization of arm motion between Japanese macaques. Sci. Rep. 3, 1151. doi: 10.1038/srep01151.
57. Newsome, W. T., and Stein-Aviles, J. A. (1999). Nonhuman primate models of visually based cognition. ILAR J. 39, 78-91. doi: 10.1093/ilar.40.2.78.
58. Nichols, M. J., and Newsome, W. T. (1999). The neurobiology of cognition. Nature 402, C35-C38. doi: 10.1038/35011531.
59. Patel, A. D. (2006). Musical rhythm, linguistic rhythm, and human evolution. Music Percept. 24, 99-104. doi: 10.1525/mp.2006.24.1.99.
60. Patel, A. D., Iversen, J. R., Bregman, M. R., and Schulz, I. (2009). Experimental evidence for synchronization to a musical beat in a nonhuman animal. Curr. Biol. 19, 827-830. doi: 10.1016/j.cub.2009.03.038.
61. Perez, O., Kass, R., and Merchant, H. (2013). Trial time warping to discriminate stimulus-related from movement-related neural activity. J. Neurosci. Methods 212, 203-210. doi: 10.1016/j.jneumeth.2012.10.019.
62. Peterson, R., and Bartholomew, G. (1969). Airborne vocal communication in the California sea lion, Zalophus californianus. Anim. Behav. 17, 17-18. doi: 10.1016/0003-3472(69)90108-0.
63. Petkov, C. I., and Jarvis, E. D. (2012). Birds, primates, and spoken language origins: behavioral phenotypes and neurobiological substrates. Front. Evol. Neurosci. 4:12. doi: 10.3389/fnevo.2012.00012.
64. Petrides, M., and Pandya, D. N. (1988). Association fiber pathways to the frontal cortex from the superior temporal region in the rhesus monkey. J. Comp. Neurol. 273, 52-66. doi: 10.1002/cne.902730106.
65. Petrides, M., and Pandya, D. N. (2009). Distinct parietal and temporal pathways to the homologues of Broca's area in the monkey. PLoS Biol. 7:e1000170. doi: 10.1371/journal.pbio.1000170.
66. Rao, S. M., Harrington, D. L., Haaland, K. Y., Bobholz, J. A., Cox, R. W., and Binder, J. R. (1997). Distributed neural systems underlying the timing of movements. J. Neurosci. 17, 5528-5535.
67. Rauschecker, J. P., and Scott, S. K. (2009). Maps and streams in the auditory cortex: non-human primates illuminate human speech processing. Nat. Neurosci. 12, 718-724. doi: 10.1038/nn.2331.
68. Rauschecker, J. P. (2012). Ventral and dorsal streams in the evolution of speech and language. Front. Evol. Neurosci. 4:7. doi: 10.3389/fnevo.2012.00007.
69. Repp, B. H. (2005). Sensorimotor synchronization: a review of the tapping literature. Psychonom. Bull. Rev. 12, 969-992. doi: 10.3758/BF03206433.
70. Repp, B. H., and Penel, A. (2002). Auditory dominance in temporal processing: new evidence from synchronization with simultaneous visual and auditory sequences. J. Exp. Psychol. Hum. Percept. Perform. 28, 1085-1099. doi: 10.1037//0096-1523.28.5.1085.
71. Rilling, J. K., Glasser, M. F., Preuss, T. M., Ma, X., Zhao, T., Hu, X., et al. (2008). The evolution of the arcuate fasciculus revealed with comparative DTI. Nat. Neurosci. 11, 426-428. doi: 10.1038/nn2072.
72. Romo, R., Hernandez, A., Zainos, A., Brody, C. D., and Lemus, L. (2000). Sensing without touching: psychophysical performance based on cortical microstimulation. Neuron 26, 273-278. doi: 10.1016/S0896-6273(00)81156-3.
73. Schachner, A., Brady, T. F., Pepperberg, I. M., and Hauser, M. D. (2009). Spontaneous motor entrainment to music in multiple vocal mimicking species. Curr. Biol. 19, 831-836. doi: 10.1016/j.cub.2009.03.061.
74. Schubotz, R. I., and von Cramon, D. Y. (2001). Interval and ordinal properties of sequences are associated with distinct premotor areas. Cereb. Cortex 11, 210-222. doi: 10.1093/cercor/11.3.210.
75. Schulze, K., Vargha-Khadem, F., and Mishkin, M. (2012). Test of a motor theory of long-term auditory memory. Proc. Natl. Acad. Sci. U.S.A. 109, 7121-7125. doi: 10.1073/pnas.1204717109.
76. Selezneva, E., Deike, S., Knyazeva, S., Scheich, H., Brechmann, A., and Brosch, M. (2013). Rhythm sensitivity in macaque monkeys. Front. Syst. Neurosci. 7:49. doi: 10.3389/fnsys.2013.00049.
77. Tanji, J. (2001). Sequential organization of multiple movements: involvement of cortical motor areas. Annu. Rev. Neurosci. 24, 631-651. doi: 10.1146/annurev.neuro.24.1.631.
78. Tanji, J., and Kurata, K. (1985). Contrasting neuronal activity in supplementary and precentral motor cortex of monkeys. I. Responses to instructions determining motor responses to forthcoming signals of different modalities. J. Neurophysiol. 53, 129-141.
79. Teki, S., Grube, M., Kumar, S., and Griffiths, T. D. (2011). Distinct neural substrates of duration-based and beat-based auditory timing. J. Neurosci. 31, 3805-3812. doi: 10.1523/JNEUROSCI.5561-10.2011.
80. Thiebaut de Schotten, M., Dell'Acqua, F., Valabregue, R., and Catani, M. (2012). Monkey to human comparative anatomy of the frontal lobe association tracts. Cortex 48, 82-96. doi: 10.1016/j.cortex.2011.10.001.
81. Vanduffel, W., Fize, D., Peuskens, H., Denys, K., Sunaert, S., Todd, J. T., et al. (2002). Extracting 3D from motion: differences in human and monkey intraparietal cortex. Science 298, 413-415. doi: 10.1126/science.1073574.
82. Wallin, N. L., Merker, B., and Brown, S. (2000). The Origins of Music. Cambridge: MIT Press.
83. Wiener, M., Turkeltaub, P., and Coslett, H. H. (2010). The image of time: a voxel-wise meta-analysis. Neuroimage 49, 1728-1740. doi: 10.1016/j.neuroimage.2009.09.064.
84. Winkler, I., Háden, G., Ladinig, O., Sziller, I., and Honing, H. (2009). Newborn infants detect the beat in music. Proc. Natl. Acad. Sci. U.S.A. 106, 2468-2471. doi: 10.1073/pnas.0809035106.
85. Yeterian, E. H., and Pandya, D. N. (1998). Corticostriatal connections of the superior temporal region in rhesus monkeys. J. Comp. Neurol. 399, 384-402. doi: 10.1002/(SICI)1096-9861(19980928)399:3<384::AID-CNE7>3.0.CO;2-X.
86. Zarco, W., Merchant, H., Prado, L., and Mendez, J. C. (2009). Subsecond timing in primates: comparison of interval production between human subjects and rhesus monkeys. J. Neurophysiol. 102, 3191-3202. doi: 10.1152/jn.00066.2009.