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Primate beta oscillations and rhythmic behaviors

  • Translational Neurosciences - Review Article
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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.

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References

  • Arnal LH, Giraud AL (2012) Cortical oscillations and sensory predictions. Trends Cogn Sci 16(7):390–398

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bastos AM, Usrey WM, Adams RA, Mangun GR, Fries P, Friston KJ (2012) Canonical microcircuits for predictive coding. Neuron 76(4):695–711

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Buhusi CV, Meck WH (2005) What makes us tick? Functional and neural mechanisms of interval timing. Nat Rev Neursci 6:755–765

    Article  CAS  Google Scholar 

  • Buzsaki G (2006) Rhythms of the brain. Oxford University Press, Oxford

    Book  Google Scholar 

  • Buzsaki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304:1926–1929

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Collyer CE, Broadbent HA, Church RM (1994) Preferred rates of repetitive tapping and categorical time production. Attent Percept Psychophys 55(4):443–453

    Article  CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Diehl RL, Lotto AJ, Holt LL (2004) Speech perception. Annu Rev Psychol 55:149–179

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Engel AK, Fries P (2010) Beta-band oscillations—signalling the status quo? Curr Opin Neurobiol 20(2):156–165

    Article  CAS  PubMed  Google Scholar 

  • Engel AK, Fries P, Singer W (2001) Dynamic predictions: oscillations and synchrony in top-down processing. Nat Rev Neurosci 2:704–716

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Fitch W (2013) Rhythmic cognition in humans and animals: distinguishing meter and pulse perception. Front Syst Neurosci 7:68

    PubMed  PubMed Central  Google Scholar 

  • Fraisse P (1982) Rhythm and tempo. In: Deutsch D (ed) Psychology of music. Academic, New York, pp 149–180

    Chapter  Google Scholar 

  • Fujii N, Graybiel AM (2003) Representation of action sequence boundaries by macaque prefrontal cortical neurons. Science 301(5637):1246–1249

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Gouvêa TS, Monteiro T, Motiwala A, Soares S, Machens C, Paton JJ (2015) Striatal dynamics explain duration judgments. eLife 4:e11386

    Article  PubMed  PubMed Central  Google Scholar 

  • Grahn JA, Brett M (2007) Rhythm and beat perception in motor areas of the brain. J Cogn Neurosci 19(5):893–906

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gupta DS, Merchant H (2017) Editorial: understanding the role of the time dimension in the brain information processing. Front Psychol 8:240

    Article  PubMed  PubMed Central  Google Scholar 

  • Hammond C, Bergman H, Brown P (2007) Pathological synchronization in Parkinson’s disease: networks, models and treatments. Trends Neurosci 30(7):357–364

    Article  CAS  PubMed  Google Scholar 

  • Harrington DL, Haaland KY, Hermanowitz N (1998) Temporal processing in the basal ganglia. Neuropsychology 12(1):3

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • Honing H, Merchant H (2014) Differences in auditory timing between human and nonhuman primates. Behav Brain Sci 37(06):557–558

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Janata P, Grafton ST (2003) Swinging in the brain: shared neural substrates for behaviors related to sequencing and music. Nat Neurosci 6:682–687

    Article  CAS  PubMed  Google Scholar 

  • Jazayeri M, Shadlen MN (2015) A neural mechanism for sensing and reproducing a time interval. Curr Biol 25(20):2599–2609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin X, Costa RM (2010) Start/stop signals emerge in nigrostriatal circuits during sequence learning. Nature 466(7305):457–462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Knudsen EB, Powers ME, Moxon KA (2014) Dissociating movement from movement timing in the rat primary motor cortex. J Neurosci 34(47):15576–15586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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)

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matell MS, Meck WH (2004) Cortico-striatal circuits and interval timing: coincidence detection of oscillatory processes. Cogn Brain Res 21(2):139–170

    Article  Google Scholar 

  • Mello GB, Soares S, Paton JJ (2015) A scalable population code for time in the striatum. Curr Biol 25(9):1113–1122

    Article  CAS  PubMed  Google Scholar 

  • Mendez JC, Prado L, Mendoza G, Merchant H (2011) Temporal and spatial categorization in human and non-human primates. Front Integr Neurosci 5:50

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Mendoza G, Merchant H (2014) Motor system evolution and the emergence of high cognitive functions. Prog Neurobiol 122:73–93

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Merchant H, de Lafuente V (2014a) Introduction to the neurobiology of interval timing. Adv Exp Med Biol 829(1):1–13

    PubMed  Google Scholar 

  • Merchant H, de Lafuente V (2014b) Neurobiology of interval timing. Springer Editorial System, Berlin

    Book  Google Scholar 

  • Merchant H, Georgopoulos AP (2006) Neurophysiology of perceptual and motor aspects of interception. J Neurophysiol 95(1):1–13

    Article  PubMed  Google Scholar 

  • Merchant H, Honing H (2014) Are non-human primates capable of rhythmic entrainment? Evidence for the gradual audiomotor evolution hypothesis. Front Neurosci 7:274

    Article  PubMed  PubMed Central  Google Scholar 

  • Merchant H, Yarrow K (2016) How the motor system both encodes and influences our sense of time. Curr Opin Behav Sci 8:22–27

    Article  Google Scholar 

  • Merchant H, Battaglia-Mayer A, Georgopoulos AP (2001) Effects of optic flow in motor cortex and area 7a. J Neurophysiol 86(4):1937–1954

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Merchant H, Zarco W, Prado L, Perez O (2009) Behavioral and neurophysiological aspects of target interception. Adv Exp Med Biol 629:201–220

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Merchant H, Harrington D, Meck WH (2013a) Neural basis of the perception and estimation of time. Ann Rev Neurosci 36(1):313–336

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Middleton FA, Strick PL (2000) Basal ganglia output and cognition: evidence from anatomical, behavioral, and clinical studies. Brain Cogn 42(2):183–200

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Morillon B, Schroeder CE (2015) Neuronal oscillations as a mechanistic substrate of auditory temporal prediction. Ann N Y Acad Sci 1337(1):26–31

    Article  PubMed  PubMed Central  Google Scholar 

  • Morillon B, Schroeder CE, Wyart V (2014) Motor contributions to the temporal precision of auditory attention. Nat Commun 5:5255. doi:10.1038/ncomms6255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Patel AD (2014) The evolutionary biology of musical rhythm: was Darwin wrong? PLoS Biol 12(3):e1001821

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Petter EA, Merchant H (2016) Temporal processing by intrinsic neural network dynamics. Timing Time Percept 4(4):399–410

    Google Scholar 

  • Repp BH, Su YH (2013) Sensorimotor synchronization: a review of recent research (2006–2012). Psychon Bull Rev 20(3):403–452

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schroeder CE, Lakatos P (2009) Low-frequency neuronal oscillations as instruments of sensory selection. Trends Neurosci 32(1):9–18

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Teki S (2014) Beta drives brain beats. Front Syst Neurosci 8:155

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Wing AM (2002) Voluntary timing and brain function: an information processing approach. Brain Cogn 48(1):7–30

    Article  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Zarco W, Merchant H (2009) Neural temporal codes for representation of information in the nervous system. Cogn Crit 1(1):1–30

    Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

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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.

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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

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