Processing of sub- and supra-second intervals in the primate brain results from the calibration of neuronal oscillators via sensory, motor, and feedback processes

Frontiers in Psychology

Volumn 5, Issue AUG, 2014, Pages

  Gupta, Daya S ^a  

^a Camden County College   (United States)

Author keywords

Cerebellum; Interval timing; Neuronal clock; Parietal; Polysensory processing; Schizophrenia

Indexed keywords

EID: 84906343202     PISSN: None     EISSN: 16641078     Source Type: Journal    
DOI: 10.3389/fpsyg.2014.00816     Document Type: Article

References (87)

1. Akam, T., and Kullmann, D. M. (2010). Oscillations and filtering networks support flexible routing of information. Neuron 67, 308-320. doi: 10.1016/j.neuron.2010.06.019
2. Amino, Y., Kyuhou, S., Matsuzaki, R., and Gemba, H. (2001). Cerebello-thalamo-cortical projections to the posterior parietal cortex in the macaque monkey. Neurosci. Lett. 309, 29-32. doi: 10.1016/S0304-3940(01)02018-3
3. Andersen, R. A. (1997). Multimodal integration for the representation of space in the posterior parietal cortex. Philos. Trans. R. Soc. Lond. B Biol. Sci. 352, 1421-1428. doi: 10.1098/rstb.1997.0128
4. Becker, M. W., and Rasmussen, I. P. (2007). The rhythm aftereffect: support for time sensitive neurons with broad overlapping tuning curves. Brain Cogn. 64, 274-281. doi: 10.1016/j.bandc.2007.03.009
5. Borresen, J., and Lynch, S. (2012). Oscillatory threshold logic. PLoS ONE 7:e48498. doi: 10.1371/journal.pone.0048498
6. Bostan, A. C., Dum, R. P., and Strick, P. L. (2013). Cerebellar networks with the cerebral cortex and basal ganglia. Trends Cogn. Sci. 17, 241-254. doi: 10.1016/j.tics.2013.03.003
7. Bremmer, F., Schlack, A., Shah, N. J., Zafiris, O., Kubischik, M., Hoffmann, K.,et al. (2001). Polymodal motion processing in posterior parietal and premotor cortex: a human fMRI study strongly implies equivalencies between humans and monkeys. Neuron 29, 287-296. doi: 10.1016/S0896-6273(01)00198-2
8. Breukelaar, J. W., and Dalrymple-Alford, J. C. (1999). Effects of lesions to the cerebellar vermis and hemispheres on timing and counting in rats. Behav. Neurosci. 113, 78-90. doi: 10.1037/0735-7044.113.1.78
9. Bueti, D., Walsh, V., Frith, C., and Rees, G. (2008). Different brain circuits underlie motor and perceptual representations of temporal intervals. J. Cogn. Neurosci. 20, 204-214. doi: 10.1162/jocn.2008.20017
10. Buhusi, C. V., and Meck, W. H. (2005). What makes us tick? Functional and neural mechanisms of interval timing. Nat. Rev. Neurosci. 6, 755-765. doi: 10.1038/nrn1764
11. Buonomano, D. V., and Merzenich, M. M. (1995). Temporal information transformed into a spatial code by a neural network with realistic properties. Science 267, 1028-1030. doi: 10.1126/science.7863330
12. Buschman, T. J., Denovellis, E. L., Diogo, C., Bullock, D., and Miller, E. K. (2012). Synchronous oscillatory neural ensembles for rules in the prefrontal cortex. Neuron 76, 838-846. doi: 10.1016/j.neuron.2012.09.029
13. Bushara, K. O., Grafman, J., and Hallett, M. (2001). Neural correlates of auditory-visual stimulus onset asynchrony detection. J. Neurosci. 21, 300-304.
14. Buzsaki, G., and Wang, X. J. (2012). Mechanisms of gamma oscillations. Annu. Rev. Neurosci. 35, 203-225. doi: 10.1146/annurev-neuro-062111-150444
15. Clower, D. M., Dum, R. P., and Strick, P. L. (2005). Basal ganglia and cerebellar inputs to 'AIP'. Cereb. Cortex 15, 913-920. doi: 10.1093/cercor/bhh190
16. Cope, T. E., Grube, M., Mandal, A., Cooper, F. E., Brechany, U., Burn, D. J.,et al. (2014). Subthalamic deep brain stimulation in Parkinson's disease has no significant effect on perceptual timing in the hundreds of milliseconds range. Neuropsychologia 57, 29-37. doi: 10.1016/j.neuropsychologia.2014.02.021
17. Coull, J., and Nobre, A. (2008). Dissociating explicit timing from temporal expectation with fMRI. Curr. Opin. Neurobiol. 18, 137-144. doi: 10.1016/j.conb.2008.07.011
18. 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
19. Durstewitz, D. (2004). Neural representation of interval time. Neuroreport 15, 745-749. doi: 10.1097/00001756-200404090-00001
20. Eckhorn, R., Bauer, R., Jordan, W., Brosch, M., Kruse, W., Munk, M.,et al. (1988). Coherent oscillations: a mechanism of feature linking in the visual cortex? Multiple electrode and correlation analyses in the cat. Biol. Cybern. 60, 121-130. doi: 10.1007/BF00202899
21. Fernandez-Ruiz, A., and Herreras, O. (2013). Identifying the synaptic origin of ongoing neuronal oscillations through spatial discrimination of electric fields. F. Comput. Neurosci. 7:5. doi: 10.3389/fncom.2013.00005
22. Fries, P., Nikolic, D., and Singer, W. (2007). The gamma cycle. Trends Neurosci. 30, 309-316. doi: 10.1016/j.tins.2007.05.005
23. Gavornik, J. P., and Shouval, H. Z. A. (2011). network of spiking neurons that can represent interval timing: mean field analysis. J. Comput. Neurosci. 30, 501-513. doi: 10.1007/s10827-010-0275-y
24. Gil, Z., Connors, B. W., and Amitai, Y. (1999). Efficacy of thalamocortical and intracortical synaptic connections: quanta, innervation, and reliability. Neuron 23, 385-397. doi: 10.1016/S0896-6273(00)80788-6
25. Gooch, C. M., Wiener, M., Wencil, E. B., and Coslett, H. B. (2010). Interval timing disruptions in subjects with cerebellar lesions. Neuropsychologia 48, 1022-1031. doi: 10.1016/j.neuropsychologia.2009.11.028
26. Grace, A. A., and Onn, S. P. (1989). Morphology and electrophysiological properties of immunocytochemically identified rat dopamine neurons recorded in vitro. J. Neurosci. 9, 3463-3481.
27. Gray, C. M., and Viana Di Prisco, G. (1997). Stimulus-dependent neuronal oscillations and local synchronization in striate cortex of the alert cat. J. Neurosci. 17, 3239-3253.
28. Harrington, D. L., Castillo, G. N., Fong, C. H., and Reed, J. D. (2011). Neural underpinnings of distortions in the experience of time across senses. Front. Integr. Neurosci. 5:32. doi: 10.3389/fnint.2011.00032
29. Harrington, D. L., Haaland, K. Y., and Knight, R. T. (1998). Cortical networks underlying mechanisms of time perception. J. Neurosci. 18, 1085-1095.
30. Ivry, R. B., and Schlerf, J. E. (2008). Dedicated and intrinsic models of time perception. Trends Cogn. Sci. 12, 273-280. doi: 10.1016/j.tics.2008.04.002
31. Ivry, R. B., and Spencer, R. M. (2004). The neural representation of time. Curr. Opin. Neurobiol. 14, 225-232. doi: 10.1016/j.conb.2004.03.013
32. Jaeger, D., Gilman, S., and Aldridge, J. W. (1995). Neuronal activity in the striatum and pallidum of primates related to the execution of externally cued reaching movements. Brain Res. 694, 111-127. doi: 10.1016/0006-8993(95)00780-T
33. Jahnsen, H. (1986). Electrophysiological characteristics of neurones in the guinea-pig deep cerebellar nuclei in vitro. J. Physiol. 372, 129-147.
34. Jantzen, K. J., Steinberg, F. L., and Kelso, J. A. (2004). Brain networks underlying human timing behavior are influenced by prior context. Proc. Natl. Acad. Sci. U.S.A. 101, 6815-6820. doi: 10.1073/pnas.0401300101
35. Joliot, M., Ribary, U., and Llinas, R. (1994). Human oscillatory brain activity near 40 Hz coexists with cognitive temporal binding. Proc. Natl. Acad. Sci. U.S.A. 91, 11748-11751. doi: 10.1073/pnas.91.24.11748
36. Kaas, J. H., Gharbawie, O. A., and Stepniewska, I. (2011). The organization and evolution of dorsal stream multisensory motor pathways in primates. Front. Neuroanat. 5:34. doi: 10.3389/fnana.2011.00034
37. Kahana, M. J. (2006). The cognitive correlates of human brain oscillations. J. Neurosci. 26, 1669-1672. doi: 10.1523/JNEUROSCI.3737-05c.2006
38. Kang, Y., and Kitai, S. T. (1993). A whole cell patch-clamp study on the pacemaker potential in dopaminergic neurons of rat substantia nigra compacta. Neurosci. Res. 18, 209-221. doi: 10.1016/0168-0102(93)90056-V
39. Karmarkar, U. R., and Buonomano, D. V. (2007). Timing in the absence of clocks: encoding time in neural network states. Neuron 53, 427-438. doi: 10. 1016/j.neuron.2007.01.006
40. Lebedev, M. A., O'doherty, J. E., and Nicolelis, M. A. (2008). Decoding of temporal intervals from cortical ensemble activity. J. Neurophysiol. 99, 166-186. doi: 10.1152/jn.00734.2007
41. Leon, M. I., and Shadlen, M. N. (2003). Representation of time by neurons in the posterior parietal cortex of the macaque. Neuron 38, 317-327. doi: 10.1016/S0896-6273(03)00185-5
42. Lewis, P. A., and Miall, R. C. (2003). Brain activation patterns during measurement of sub- and supra-second intervals. Neuropsychologia 41, 1583-1592. doi: 10.1016/S0028-3932(03)00118-0
43. Llinas, R. R. (1988). The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. Science 242, 1654-1664. doi: 10.1126/science.3059497
44. Llinas, R. R., Grace, A. A., and Yarom, Y. (1991). In vitro neurons in mammalian cortical layer 4 exhibit intrinsic oscillatory activity in the 10- to 50-Hz frequency range. Proc. Natl. Acad. Sci. U.S.A. 88, 897-901. doi: 10.1073/pnas.88.3.897
45. Maass, W., Natschlager, T., and Markram, H. (2002). Real-time computing without stable states: a new framework for neural computation based on perturbations. Neural Comput. 14, 2531-2560. doi: 10.1162/089976602760407955
46. Macaluso, E., and Driver, J. (2001). Spatial attention and crossmodal interactions between vision and touch. Neuropsychologia 39, 1304-1316. doi: 10.1016/S0028-3932(01)00119-1
47. Magill, P. J., Sharott, A., Bolam, J. P., and Brown, P. (2004). Brain state-dependency of coherent oscillatory activity in the cerebral cortex and basal ganglia of the rat. J. Neurophysiol. 92, 2122-2136. doi: 10.1152/jn.00333.2004
48. Malapani, C., Rakitin, B., Levy, R., Meck, W. H., Deweer, B., Dubois, B.,et al. (1998). Coupled temporal memories in Parkinson's disease: a dopamine-related dysfunction. J. Cogn. Neurosci. 10, 316-331. doi: 10.1162/089892998562762
49. Matell, M. S., and Meck, W. H. (2004). Cortico-striatal circuits and interval timing: coincidence detection of oscillatory processes. Brain Res. Cogn. Brain Res. 21, 139-170. doi: 10.1016/j.cogbrainres.2004.06.012
50. Matell, M. S., Meck, W. H., and Nicolelis, M. A. (2003). Interval timing and the encoding of signal duration by ensembles of cortical and striatal neurons. Behav. Neurosci. 117, 760-773. doi: 10.1037/0735-7044.117.4.760
51. Middleton, F. A., and Strick, P. L. (2000). Basal ganglia output and cognition: evidence from anatomical, behavioral, and clinical studies. Brain Cogn. 42, 183-200. doi: 10.1006/brcg.1999.1099
52. Mita, A., Mushiake, H., Shima, K., Matsuzaka, Y., and Tanji, J. (2009). Interval time coding by neurons in the presupplementary and supplementary motor areas. Nat. Neurosci. 12, 502-507. doi: 10.1038/nn.2272
53. Murer, M. G., Tseng, K. Y., Kasanetz, F., Belluscio, M., and Riquelme, L. A. (2002). Brain oscillations, medium spiny neurons, and dopamine. Cell. Mol. Neurobiol. 22, 611-632. doi: 10.1023/A:1021840504342
54. Nienborg, H., and Cumming, B. (2010). Correlations between the activity of sensory neurons and behavior: how much do they tell us about a neuron's causality? Curr. Opin. Neurobiol. 20, 376-381. doi: 10.1016/j.conb.2010.05.002
55. O'Reilly, J. X., Mesulam, M. M., and Nobre, A. C. (2008). The cerebellum predicts the timing of perceptual events. J. Neurosci. 28, 2252-2260. doi: 10.1523/JNEUROSCI.2742-07.2008
56. Parsons, B. D., Novich, S. D., and Eagleman, D. M. (2013). Motor-sensory recalibration modulates perceived simultaneity of cross-modal events at different distances. Front. Psychol. 4:46. doi: 10.3389/fpsyg.2013.00046
57. Pastor, M. A., Artieda, J., Jahanshahi, M., and Obeso, J. A. (1992). Time estimation and reproduction is abnormal in Parkinson's disease. Brain 115, 211-225. doi: 10.1093/brain/115.1.211
58. Pastore, R. E., and Farrington, S. M. (1996). Measuring the difference limen for identification of order of onset for complex auditory stimuli. Percept. Psychophys. 58, 510-526. doi: 10.3758/BF03213087
59. Peterburs, J., Nitsch, A. M., Miltner, W. H., and Straube, T. (2013). Impaired representation of time in schizophrenia is linked to positive symptoms and cognitive demand. PLoS ONE 8:e67615. doi: 10.1371/journal.pone.0067615
60. Piras, F., and Coull, J. T. (2011). Implicit, predictive timing draws upon the same scalar representation of time as explicit timing. PLoS ONE 6:e18203. doi: 10.1371/journal.pone.0018203
61. Poppel, E. (1994). Temporal mechanisms in perception. Int. Rev. Neurobiol. 37, 185-202; discussion 203-187.
62. Poppel, E. (1997). A hierarchical model of temporal perception. Trends Cogn. Sci. 1, 56-61. doi: 10.1016/S1364-6613(97)01008-5
63. Prevosto, V., Graf, W., and Ugolini, G. (2011). Proprioceptive pathways to posterior parietal areas MIP and LIPv from the dorsal column nuclei and the postcentral somatosensory cortex. Eur. J. Neurosci. 33, 444-460. doi: 10.1111/j.1460-9568.2010.07541.x
64. Purves, D., Augustine, G. J., Fitzpatrick, D., and Et, A. l., eds. (2001). Neuroscience. Sunderland MA: Sinauer Associates. Available at:
65. Raman, I. M., Gustafson, A. E., and Padgett, D. (2000). Ionic currents and spontaneous firing in neurons isolated from the cerebellar nuclei. J. Neurosci. 20, 9004-9016.
66. Rath, M. F., Rovsing, L., and Moller, M. (2014). Circadian oscillators in the mouse brain: molecular clock components in the neocortex and cerebellar cortex. Cell Tissue Res. doi: 10.1007/s00441-014-1878-9 [Epub ahead of print].
67. Regehr, W. G. (2012). Short-term presynaptic plasticity. Cold Spring Harb. Perspect. Biol. 4:a005702. doi: 10.1101/cshperspect.a005702
68. Riesen, J. M., and Schnider, A. (2001). Time estimation in Parkinson's disease: normal long duration estimation despite impaired short duration discrimination. J. Neurol. 248, 27-35. doi: 10.1007/s004150170266
69. Sannita, W. G. (2000). Stimulus-specific oscillatory responses of the brain: a time/frequency-related coding process. Clin. Neurophysiol. 111, 565-583. doi: 10.1016/S1388-2457(99)00271-0
70. Santos, L., Opris, I., Hampson, R., Godwin, D. W., Gerhardt, G., and Deadwyler, S. (2014). Functional dynamics of primate cortico-striatal networks during volitional movements. Front. Syst. Neurosci. 8:27. doi: 10.3389/fnsys.2014.00027
71. Sarko, D. K., Ghose, D., and Wallace, M. T. (2013). Convergent approaches toward the study of multisensory perception. Front. Syst. Neurosci. 7:81. doi: 10.3389/fnsys.2013.00081
72. Schaap, J., Albus, H., Vanderleest, H. T., Eilers, P. H., Detari, L., and Meijer, J. H. (2003). Heterogeneity of rhythmic suprachiasmatic nucleus neurons: implications for circadian waveform and photoperiodic encoding. Proc. Natl. Acad. Sci. U.S.A. 100, 15994-15999. doi: 10.1073/pnas.2436298100
73. Schneider, B. A., and Ghose, G. M. (2012). Temporal production signals in parietal cortex. PLoS Biol. 10:e1001413. doi: 10.1371/journal.pbio.1001413
74. Schubotz, R. I. (2007). Prediction of external events with our motor system: towards a new framework. Trends Cogn. Sci. 11, 211-218. doi: 10.1016/j.tics.2007.02.006
75. Simen, P., Balci, F., De Souza, L., Cohen, J. D., and Holmes, P. (2011). A model of interval timing by neural integration. J. Neurosci. 31, 9238-9253. doi: 10.1523/JNEUROSCI.3121-10.2011
76. Snyder, L. H., Grieve, K. L., Brotchie, P., and Andersen, R. A. (1998). Separate body- and world-referenced representations of visual space in parietal cortex. Nature 394, 887-891. doi: 10.1038/29777
77. Strick, P. L., Dum, R. P., and Fiez, J. A. (2009). Cerebellum and nonmotor function. Annu. Rev. Neurosci. 32, 413-434. doi: 10.1146/annurev.neuro.31.060407.125606
78. Teki, S., Grube, M., and Griffiths, T. D. (2011a). A unified model of time perception accounts for duration-based and beat-based timing mechanisms. Front. Integr. Neurosci. 5:90. doi: 10.3389/fnint.2011.00090
79. Teki, S., Grube, M., Kumar, S., and Griffiths, T. D. (2011b). Distinct neural substrates of duration-based and beat-based auditory timing. J. Neurosci. 31, 3805-3812. doi: 10.1523/JNEUROSCI.5561-10.2011
80. Timmann, D., Watts, S., and Hore, J. (1999). Failure of cerebellar patients to time finger opening precisely causes ball high-low inaccuracy in overarm throws. J. Neurophysiol. 82, 103-114.
81. Walther, S., and Strik, W. (2012). Motor symptoms and schizophrenia. Neuropsychobiology 66, 77-92. doi: 10.1159/000339456
82. Wiener, M., Turkeltaub, P., and Coslett, H. B. (2010a). The image of time: a voxel-wise meta-analysis. Neuroimage 49, 1728-1740. doi: 10.1016/j.neuroimage.2009.09.064
83. Wiener, M., Turkeltaub, P. E., and Coslett, H. B. (2010b). Implicit timing activates the left inferior parietal cortex. Neuropsychologia 48, 3967-3971. doi: 10.1016/j.neuropsychologia.2010.09.014
84. Wittmann, M. (1999). Time perception and temporal processing levels of the brain. Chronobiol. Int. 16, 17-32. doi: 10.3109/07420529908998709
85. Wittmann, M. (2009). The inner experience of time. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 1955-1967. doi: 10.1098/rstb.2009.0003
86. Wright, B. A., Buonomano, D. V., Mahncke, H. W., and Merzenich, M. M. (1997). Learning and generalization of auditory temporal-interval discrimination in humans. J. Neurosci. 17, 3956-3963.
87. Xing, D., Shen, Y., Burns, S., Yeh, C. I., Shapley, R., and Li, W. (2012). Stochastic generation of gamma-band activity in primary visual cortex of awake and anesthetized monkeys. J. Neurosci. 32, 13873-13880a. doi: 10.1523/JNEUROSCI.5644-11.2012