Abstract
The study of non-human primates in complex behaviors such as rhythm perception and entrainment is critical to understand the neurophysiological basis of human cognition. Next to reviewing the role of beta oscillations in human beat perception, here we discuss the role of primate putaminal oscillatory activity in the control of rhythmic movements that are guided by a sensory metronome or internally gated. The analysis of the local field potentials of the behaving macaques showed that gamma-oscillations reflect local computations associated with stimulus processing of the metronome, whereas beta-activity involves the entrainment of large putaminal circuits, probably in conjunction with other elements of cortico-basal ganglia-thalamo-cortical circuit, during internally driven rhythmic tapping. Thus, this review emphasizes the need of parametric neurophysiological observations in non-human primates that display a well-controlled behavior during high-level cognitive processes.
Similar content being viewed by others
References
Arnal LH, Giraud AL (2012) Cortical oscillations and sensory predictions. Trends Cogn Sci 16(7):390–398
Baker SN, Olivier E, Lemon RN (1997) Coherent oscillations in monkey motor cortex and hand muscle EMG show task-dependent modulation. J Physiol 501(1):225–241
Bartolo R, Merchant H (2009) Learning and generalization of time production in humans: rules of transfer across modalities and interval durations. Exp Brain Res 197(1):91–100
Bartolo R, Merchant H (2015) β oscillations are linked to the initiation of sensory-cued movement sequences and the internal guidance of regular tapping in the monkey. J Neurosci 35(11):4635–4640
Bartolo R, Prado L, Merchant H (2014) Information processing in the primate basal ganglia during sensory guided and internally driven rhythmic tapping. J Neurosci 34(11):3910–3923
Bastos AM, Usrey WM, Adams RA, Mangun GR, Fries P, Friston KJ (2012) Canonical microcircuits for predictive coding. Neuron 76(4):695–711
Brown P, Oliviero A, Mazzone P, Insola A, Tonali P, Di Lazzaro V (2001) Dopamine dependency of oscillations between subthalamic nucleus and pallidum in Parkinson’s disease. J Neurosci 21(3):1033–1038
Buhusi CV, Meck WH (2005) What makes us tick? Functional and neural mechanisms of interval timing. Nat Rev Neursci 6:755–765
Buzsaki G (2006) Rhythms of the brain. Oxford University Press, Oxford
Buzsaki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304:1926–1929
Carrillo-Reid L, Hernandez-Lopez S, Tapia D, Galarraga E, Bargas J (2011) Dopaminergic modulation of the striatal microcircuit: receptor-specific configuration of cell assemblies. J Neurosci 31(42):14972–14983
Collyer CE, Broadbent HA, Church RM (1994) Preferred rates of repetitive tapping and categorical time production. Attent Percept Psychophys 55(4):443–453
Courtemanche R, Fujii N, Graybiel AM (2003) Synchronous, focally modulated β-band oscillations characterize local field potential activity in the striatum of awake behaving monkeys. J Neurosci 23(37):11741–11752
Crowe DA, Zarco W, Bartolo R, Merchant H (2014) Dynamic representation of the temporal and sequential structure of rhythmic movements in the primate medial premotor cortex. J Neurosci 34(36):11972–11983
Deffains M, Iskhakova L, Katabi S, Haber SN, Israel Z, Bergman H (2016) Subthalamic, not striatal, activity correlates with basal ganglia downstream activity in normal and parkinsonian monkeys. Elife 5:e16443
Diehl RL, Lotto AJ, Holt LL (2004) Speech perception. Annu Rev Psychol 55:149–179
Donnet S, Bartolo R, Fernandes JM, Cunha JPS, Prado L, Merchant H (2014) Monkeys time their pauses of movement and not their movement-kinematics during a synchronization-continuation rhythmic task. J Neurophysiol 111(10):2138–2149
Engel AK, Fries P (2010) Beta-band oscillations—signalling the status quo? Curr Opin Neurobiol 20(2):156–165
Engel AK, Fries P, Singer W (2001) Dynamic predictions: oscillations and synchrony in top-down processing. Nat Rev Neurosci 2:704–716
Eusebio A, Brown P (2009) Synchronisation in the beta frequency-band—the bad boy of parkinsonism or an innocent bystander? Exp Neurol 217(1):1–3
Fitch W (2013) Rhythmic cognition in humans and animals: distinguishing meter and pulse perception. Front Syst Neurosci 7:68
Fraisse P (1982) Rhythm and tempo. In: Deutsch D (ed) Psychology of music. Academic, New York, pp 149–180
Fujii N, Graybiel AM (2003) Representation of action sequence boundaries by macaque prefrontal cortical neurons. Science 301(5637):1246–1249
Fujioka T, Trainor LJ, Large EW, Ross B (2009) Beta and gamma rhythms in human auditory cortex during musical beat processing. Ann N Y Acad Sci 1169(1):89–92
Fujioka T, Trainor LJ, Large EW, Ross B (2012) Internalized timing of isochronous sounds is represented in neuromagnetic beta oscillations. J Neurosci 32(5):1791–1802
Fujioka T, Ross B, Trainor LJ (2015) Beta-band oscillations represent auditory beat and its metrical hierarchy in perception and imagery. J Neurosci 35(45):15187–15198
Gamez J, Bartolo R, Mendoza G, Prado L, Merchant H (2017) Coupling of periodic neural state trajectories during rhythmic tapping. Nat Commun (submitted)
García-Garibay O, Cadena-Valencia J, Merchant H, de Lafuente V (2016) Monkeys share the human ability to internally maintain a temporal rhythm. Front Psychol 7:1971. doi:10.3389/fpsyg.2016.01971
Gouvêa TS, Monteiro T, Motiwala A, Soares S, Machens C, Paton JJ (2015) Striatal dynamics explain duration judgments. eLife 4:e11386
Grahn JA, Brett M (2007) Rhythm and beat perception in motor areas of the brain. J Cogn Neurosci 19(5):893–906
Grahn JA, Rowe JB (2009) Feeling the beat: premotor and striatal interactions in musicians and nonmusicians during beat perception. J Neurosci 29(23):7540–7548
Grube M, Cooper FE, Chinnery PF, Griffiths TD (2010) Dissociation of duration-based and beat-based auditory timing in cerebellar degeneration. Proc Natl Acad Sci 107(25):11597–11601
Gupta DS, Merchant H (2017) Editorial: understanding the role of the time dimension in the brain information processing. Front Psychol 8:240
Hammond C, Bergman H, Brown P (2007) Pathological synchronization in Parkinson’s disease: networks, models and treatments. Trends Neurosci 30(7):357–364
Harrington DL, Haaland KY, Hermanowitz N (1998) Temporal processing in the basal ganglia. Neuropsychology 12(1):3
Helmuth LL, Mayr U, Daum I (2000) Sequence learning in Parkinson’s disease: a comparison of spatial-attention and number-response sequences. Neuropsychologia 38(11):1443–1451
Honing H (2013) Structure and interpretation of rhythm in music. In: Deutsch D (ed) Psychology of Music, 3rd edn. Academic press, London, pp 369–404
Honing H, Merchant H (2014) Differences in auditory timing between human and nonhuman primates. Behav Brain Sci 37(06):557–558
Honing H, Merchant H, Háden GP, Prado L, Bartolo R (2012) Rhesus monkeys (Macaca mulatta) detect rhythmic groups in music, but not the beat. PLoS One 7(12):e51369
Honing H, Bouwer FL, Prado L, Merchant H (2017). Rhesus monkeys (Macaca mulatta) detect isochrony in rhythm, but not the beat. Cortex (submitted)
Howe MW, Atallah HE, McCool A, Gibson DJ, Graybiel AM (2011) Habit learning is associated with major shifts in frequencies of oscillatory activity and synchronized spike firing in striatum. Proc Natl Acad Sci 108(40):16801–16806
Iversen JR, Repp BH, Patel AD (2009) Top-down control of rhythm perception modulates early auditory responses. Ann N Y Acad Sci 1169(1):58–73
Jaidar O, Carrillo-Reid L, Hernandez A, Drucker-Colín R, Bargas J, Hernandez-Cruz A (2010) Dynamics of the parkinsonian striatal microcircuit: entrainment into a dominant network state. J Neurosci 30(34):11326–11336
Janata P, Grafton ST (2003) Swinging in the brain: shared neural substrates for behaviors related to sequencing and music. Nat Neurosci 6:682–687
Jazayeri M, Shadlen MN (2015) A neural mechanism for sensing and reproducing a time interval. Curr Biol 25(20):2599–2609
Jin X, Costa RM (2010) Start/stop signals emerge in nigrostriatal circuits during sequence learning. Nature 466(7305):457–462
Kay LM, Beshel J (2010) A beta oscillation network in the rat olfactory system during a 2-alternative choice odor discrimination task. J Neurophysiol 104(2):829–839
Knudsen EB, Powers ME, Moxon KA (2014) Dissociating movement from movement timing in the rat primary motor cortex. J Neurosci 34(47):15576–15586
Kühn AA, Kempf F, Brücke C, Doyle LG, Martinez-Torres I, Pogosyan A, Vandenberghe W (2008) High-frequency stimulation of the subthalamic nucleus suppresses oscillatory β activity in patients with Parkinson’s disease in parallel with improvement in motor performance. J Neurosci 28(24):6165–6173
Kung SJ, Chen JL, Zatorre RJ, Penhune VB (2013) Interacting cortical and basal ganglia networks underlying finding and tapping to the musical beat. J Cogn Neurosci 25(3):401–420
Large EW, Herrera JA, Velasco MJ (2015) Neural networks for beat perception in musical rhythm. Front Syst Neurosci 9:159. 2015, doi:10.3389/fnsys.2015.00159 (eCollection)
Leventhal DK, Gage GJ, Schmidt R, Pettibone JR, Case AC, Berke JD (2012) Basal ganglia beta oscillations accompany cue utilization. Neuron 73(3):523–536
Levy R, Ashby P, Hutchison WD, Lang AE, Lozano AM, Dostrovsky JO (2002) Dependence of subthalamic nucleus oscillations on movement and dopamine in Parkinson’s disease. Brain 125(6):1196–1209
Mallet N, Pogosyan A, Márton LF, Bolam JP, Brown P, Magill PJ (2008) Parkinsonian beta oscillations in the external globus pallidus and their relationship with subthalamic nucleus activity. J Neurosci 28(52):14245–14258
Matell MS, Meck WH (2004) Cortico-striatal circuits and interval timing: coincidence detection of oscillatory processes. Cogn Brain Res 21(2):139–170
Mello GB, Soares S, Paton JJ (2015) A scalable population code for time in the striatum. Curr Biol 25(9):1113–1122
Mendez JC, Prado L, Mendoza G, Merchant H (2011) Temporal and spatial categorization in human and non-human primates. Front Integr Neurosci 5:50
Méndez JC, Pérez O, Prado L, Merchant H (2014) Linking perception, cognition, and action: psychophysical observations and neural network modelling. PLoS One 9(7):e102553
Mendoza G, Merchant H (2014) Motor system evolution and the emergence of high cognitive functions. Prog Neurobiol 122:73–93
Mendoza G, Peyrache A, Gámez J, Prado L, Buzsáki G, Merchant H (2016) Recording extracellular neural activity in the behaving monkey using a semichronic and high-density electrode system. J Neurophysiol 116(2):563–574
Merchant H, Averbeck BB (2017) The computational and neural basis of rhythmic timing in medial premotor cortex. J Neurosci. doi:10.1523/JNEUROSCI.0367-17.2017
Merchant H, de Lafuente V (2014a) Introduction to the neurobiology of interval timing. Adv Exp Med Biol 829(1):1–13
Merchant H, de Lafuente V (2014b) Neurobiology of interval timing. Springer Editorial System, Berlin
Merchant H, Georgopoulos AP (2006) Neurophysiology of perceptual and motor aspects of interception. J Neurophysiol 95(1):1–13
Merchant H, Honing H (2014) Are non-human primates capable of rhythmic entrainment? Evidence for the gradual audiomotor evolution hypothesis. Front Neurosci 7:274
Merchant H, Yarrow K (2016) How the motor system both encodes and influences our sense of time. Curr Opin Behav Sci 8:22–27
Merchant H, Battaglia-Mayer A, Georgopoulos AP (2001) Effects of optic flow in motor cortex and area 7a. J Neurophysiol 86(4):1937–1954
Merchant H, Zarco W, Bartolo R, Prado L (2008a) The context of temporal processing is represented in the multidimensional relationships between timing tasks. PLoS One 3(9):e3169
Merchant H, Zarco W, Prado L (2008b) Do we have a common mechanism for measuring time in the hundreds of millisecond range? Evidence from multiple-interval timing tasks. J Neurophysiol 99(2):939–949
Merchant H, Luciana M, Hooper C, Majestic S, Tuite P (2008c) Interval timing and Parkinson’s disease: heterogeneity in temporal performance. Exp Brain Res 184(2):233–248
Merchant H, Zarco W, Prado L, Perez O (2009) Behavioral and neurophysiological aspects of target interception. Adv Exp Med Biol 629:201–220
Merchant H, Zarco W, Pérez O, Prado L, Bartolo R (2011) Measuring time with different neural chronometers during a synchronization-continuation task. Proc Natl Acad Sci USA 108:19784–19789
Merchant H, de Lafuente V, Pena-Ortega F, Larriva-Sahd J (2012) Functional impact of interneuronal inhibition in the cerebral cortex of behaving animals. Prog Neurobiol 99(2):163–178
Merchant H, Harrington D, Meck WH (2013a) Neural basis of the perception and estimation of time. Ann Rev Neurosci 36(1):313–336
Merchant H, Pérez O, Zarco W, Gámez J (2013b) Interval tuning in the primate medial premotor cortex as a general timing mechanism. J Neurosci 33(21):9082–9096
Merchant H, Bartolo R, Perez O, Mendez JC, Mendoza G, Gamez J, Yc K, Prado L (2014) Neurophysiology of timing in the hundreds of milliseconds: multiple layers of neuronal clocks in the medial premotor areas. Adv Exp Med Biol 829(1):143–154
Merchant H, Grahn J, Trainer L, Rohrmeier M, Fitch TW (2015a) Finding the beat: a neural perspective across humans and non-human primates. Philos Trans R Soc Lond B Biol Sci 370:186–202
Merchant H, Perez O, Bartolo R, Mendez JC, Mendoza G, Gamez J, Yc K, Prado L (2015b) Sensorimotor neural dynamics during isochronous tapping in the medial premotor cortex of the macaque. Eur J Neurosci 41(5):586–602
Middleton FA, Strick PL (2000) Basal ganglia output and cognition: evidence from anatomical, behavioral, and clinical studies. Brain Cogn 42(2):183–200
Mita A, Mushiake H, Shima K, Matsuzaka Y, Tanji J (2009) Interval time coding by neurons in the presupplementary and supplementary motor areas. Nat Neurosci 12:502–507
Morillon B, Schroeder CE (2015) Neuronal oscillations as a mechanistic substrate of auditory temporal prediction. Ann N Y Acad Sci 1337(1):26–31
Morillon B, Schroeder CE, Wyart V (2014) Motor contributions to the temporal precision of auditory attention. Nat Commun 5:5255. doi:10.1038/ncomms6255
Murthy VN, Fetz EE (1996) Synchronization of neurons during local field potential oscillations in sensorimotor cortex of awake monkeys. J Neurophysiol 76(6):3968–3982
Parent A, Hazrati LN (1995) Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain Res Rev 20(1):91–127
Patel AD (2014) The evolutionary biology of musical rhythm: was Darwin wrong? PLoS Biol 12(3):e1001821
Perez O, Kass R, Merchant H (2013) Trial time warping to discriminate stimulus-related from movement-related neural activity. J Neurosci Methods 212(2):203–210
Petter EA, Merchant H (2016) Temporal processing by intrinsic neural network dynamics. Timing Time Percept 4(4):399–410
Repp BH, Su YH (2013) Sensorimotor synchronization: a review of recent research (2006–2012). Psychon Bull Rev 20(3):403–452
Sanes JN, Donoghue JP (1993) Oscillations in local field potentials of the primate motor cortex during voluntary movement. Proc Natl Acad Sci 90(10):4470–4474
Schroeder CE, Lakatos P (2009) Low-frequency neuronal oscillations as instruments of sensory selection. Trends Neurosci 32(1):9–18
Schwartze M, Keller PE, Patel AD, Kotz SA (2011) The impact of basal ganglia lesions on sensorimotor synchronization, spontaneous motor tempo, and the detection of tempo changes. Behav Brain Res 216(2):685–691
Takahashi K, Kim S, Coleman TP, Brown KA, Suminski AJ, Best MD, Hatsopoulos NG (2015) Large-scale spatiotemporal spike patterning consistent with wave propagation in motor cortex. Nature Commun 6:7169. doi:10.1038/ncomms8169
Teki S (2014) Beta drives brain beats. Front Syst Neurosci 8:155
Teki S, Grube M, Kumar S, Griffiths TD (2011) Distinct neural substrates of duration-based and beat-based auditory timing. J Neurosci 31(10):3805–3812
Teki S, Grube M, Griffiths TD (2012) A unified model of time perception accounts for duration-based and beat-based timing mechanisms. Front Integr Neurosci 5:90
Weinberger M, Hutchison WD, Dostrovsky JO (2009) Pathological subthalamic nucleus oscillations in PD: can they be the cause of bradykinesia and akinesia? Exp Neurol 219(1):58–61
Wing AM (2002) Voluntary timing and brain function: an information processing approach. Brain Cogn 48(1):7–30
Wright BA, Buonomano DV, Mahncke HW, Merzenich MM (1997) Learning and generalization of auditory temporal–interval discrimination in humans. J Neurosci 17(10):3956–3963
Zarco W, Merchant H (2009) Neural temporal codes for representation of information in the nervous system. Cogn Crit 1(1):1–30
Zarco W, Merchant H, Prado L, Mendez JC (2009) Subsecond timing in primates: comparison of interval production between human subjects and rhesus monkeys. J Neurophysiol 102(6):3191–3202
Acknowledgements
We thank Yaneri Ayala and Dobromir Dotov for their fruitful comments on the manuscript. We thank Luis Prado and Raul Paulín for their technical assistance. Supported by CONACYT: 236836, CONACYT: 196, and PAPIIT: IN202317 Grants to H. Merchant.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Merchant, H., Bartolo, R. Primate beta oscillations and rhythmic behaviors. J Neural Transm 125, 461–470 (2018). https://doi.org/10.1007/s00702-017-1716-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00702-017-1716-9