Oscillatory interactions between sensorimotor cortex and the periphery

Current Opinion in Neurobiology

Volumn 17, Issue 6, 2007, Pages 649-655

  Baker, Stuart N ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CENTRAL NERVOUS SYSTEM; CONCEPT ANALYSIS; ELECTRIC POTENTIAL; FEEDBACK SYSTEM; HUMAN; MOTOR CORTEX; MUSCLE CONTRACTION; OSCILLATION; PRIORITY JOURNAL; RECORDING; REVIEW; SENSORIMOTOR CORTEX; SENSORY NERVE; SOMATOSENSORY CORTEX;

ANIMALS; BETA RHYTHM; BIOLOGICAL CLOCKS; ELECTROENCEPHALOGRAPHY; FEEDBACK; HUMANS; MOTOR CORTEX; PERIPHERAL NERVES; SOMATOSENSORY CORTEX;

EID: 40849114335     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.conb.2008.01.007     Document Type: Review

References (45)

1. Riddle C.N., and Baker S.N. Digit displacement, not object compliance, underlies task dependent modulations in human corticomuscular coherence. Neuroimage 33 (2006) 618-627. Subjects performed precision grip movements, followed by steady contractions. During this holding phase, beta-band corticomuscular coherence was greatest following a large movement than following a small movement. Using a robotic manipulandum, the authors dissociated object compliance and displacement, and showed that displacement was the key variable affecting coherence.
2. Baker S.N., Pinches E.M., and Lemon R.N. Synchronization in monkey motor cortex during a precision grip task. II. Effect of oscillatory activity on corticospinal output. J Neurophysiol 89 (2003) 1941-1953
3. Baker S.N., Olivier E., and Lemon R.N. Coherent oscillations in monkey motor cortex and hand muscle EMG show task-dependent modulation. J Physiol 501 Pt 1 (1997) 225-241
4. Fries P. A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn Sci 9 (2005) 474-480
5. Fries P., Nikolic D., and Singer W. The gamma cycle. Trends Neurosci 30 (2007) 309-316
6. Singer W., and Gray C.M. Visual feature integration and the temporal correlation hypothesis. Annu Rev Neurosci 18 (1995) 555-586
7. Traub R.D., Jeffreys J.G.R., and Whittington M.A. Fast Oscillations in Cortical Circuits (1999), The MIT Press, Cambridge, Mass
8. Pauluis Q., Baker S.N., and Olivier E. Emergent oscillations in a realistic network: the role of inhibition and the effect of the spatiotemporal distribution of the input. J Comput Neurosci 6 (1999) 27-48
9. Baker M.R., and Baker S.N. The effect of diazepam on motor cortical oscillations and corticomuscular coherence studied in man. J Physiol 546 (2003) 931-942
10. Roopun A.K., Middleton S.J., Cunningham M.O., LeBeau F.E.N., Bibbig A., Whittington M.A., and Traub R.D. A beta2-frequency (20-30 Hz) oscillation in nonsynaptic networks of somatosensory cortex. PNAS 103 (2006) 15646-15650. This study demonstrates that gap-junctional coupling between axons of pyramidal neurones can generate beta-band oscillations in the absence of synaptic activity.
11. Wetmore D.Z., and Baker S.N. Post-spike distance-to-threshold trajectories of neurones in monkey motor cortex. J Physiol 555 (2004) 831-850
12. Chen D., and Fetz E.E. Characteristic membrane potential trajectories in primate sensorimotor cortex neurons recorded in vivo. J Neurophysiol 94 (2005) 2713-2725
13. Witham C.L., and Baker S.N. Network oscillations and intrinsic spiking rhythmicity do not covary in monkey sensorimotor areas. J Physiol 580 (2007) 801-814. This study shows that oscillations in various somatosensory areas of the cortex are actually stronger than in M1. Using a statistical method, it demonstrates some cells have an intrinsic tendency to fire rhythmically around beta-frequencies. This tendency is most pronounced for M1 corticospinal cells, suggesting preferential transmission of oscillations to the spinal cord.
14. Pfurtscheller G., Stancák Jr. A., and Neuper C. Post-movement beta synchronization. A correlate of an idling motor area?. Electroencephalogr Clin Neurophysiol 98 (1996) 281-293
15. Rubino D., Robbins K.A., and Hatsopoulos N.G. Propagating waves mediate information transfer in the motor cortex. Nat Neurosci 9 (2006) 1549-1557. This study provides evidence for travelling waves within the activity of motor cortex, which encode information about behavioural cues in the parameters. This is an important study, because such waves have previously only been reported for sensory cortex, and theoretical work suggests that this activity may be capable of computation [16].
16. Ermentrout G.B., and Kleinfeld D. Traveling electrical waves in cortex: insights from phase dynamics and speculation on a computational role. Neuron 29 (2001) 33-44
17. Jackson A., Spinks R.L., Freeman T.C., Wolpert D.M., and Lemon R.N. Rhythm generation in monkey motor cortex explored using pyramidal tract stimulation. J Physiol 541 (2002) 685-699
18. Gross J., Tass P.A., Salenius S., Hari R., Freund H.J., and Schnitzler A. Cortico-muscular synchronization during isometric muscle contraction in humans as revealed by magnetoencephalography. J Physiol 527 (2000) 623-631
19. Mima T., Steger J., Schulman A.E., Gerloff C., and Hallett M. Electroencephalographic measurement of motor cortex control of muscle activity in humans. Clin Neurophysiol 111 (2000) 326-337
20. Halliday D.M., Conway B.A., Farmer S.F., and Rosenberg J.R. Using electroencephalography to study functional coupling between cortical activity and electromyograms during voluntary contractions in humans. Neurosci Lett 241 (1998) 5-8
21. Riddle C.N., and Baker S.N. Manipulation of peripheral neural feedback loops alters human corticomuscular coherence. J Physiol 566 (2005) 625-639. This is a detailed examination of the phase of corticomuscular coherence in normal human subjects, suggesting that subjects can be classified into two groups on the basis of their phase-frequency relationship. The changes in phase after slowing peripheral conduction by cooling the arm were also investigated. The results argue strongly for a contribution to corticomuscular coherence by feedback, as well as feedforward pathways.
22. Lemon R.N., and Porter R. Afferent input to movement-related precentral neurones in conscious monkeys. Proc R Soc Lond, Ser B 194 (1976) 313-339
23. Gerstner W., van Hemmen J.L., and Cowan J.D. What matters in neuronal locking?. Neural Comput 8 (1996) 1653-1676
24. Baker S.N., Chiu M., and Fetz E.E. Afferent encoding of central oscillations in the monkey arm. J Neurophysiol 95 (2006) 3904-3910. A direct demonstration that activity in single afferent units is coherent with oscillations in muscle over a wide frequency range, including the beta band. This was also the case for a small population of units identified as muscle spindle primary afferents using spike-triggered averaging methods. Directed coherence (Granger Causality) analysis was also applied to these units, leading to the conclusion that oscillations flow both in the direction from afferents to muscle and vice versa.
25. Soteropoulos D.S., and Baker S.N. Cortico-cerebellar coherence during a precision grip task in the monkey. J Neurophysiol 95 (2006) 1194-1206
26. Witham CL, Wang M, Baker SN: Cells in somatosensory areas show synchrony with beta oscillations in monkey motor cortex. Eur J Neurosci 2007, in press. Single units recorded from a variety of somatosensory areas show coherence with M1 oscillations. The coherence is similar in both phase and magnitude to that between M1 cells and M1 oscillations, indicating very tight coupling between S1 and M1 at near-zero phase lag.
27. Kilner J.M., Fisher R.J., and Lemon R.N. Coupling of oscillatory activity between muscles is strikingly reduced in a deafferented subject compared with normal controls. J Neurophysiol 92 (2004) 790-796
28. Patino L., Chakarov V., Schulte-Monting J., Hepp-Reymond M.C., and Kristeva R. Oscillatory cortical activity during a motor task in a deafferented patient. Neurosci Lett 401 (2006) 214-218
29. Fisher R.J., Galea M.P., Brown P., and Lemon R.N. Digital nerve anaesthesia decreases EMG-EMG coherence in a human precision grip task. Exp Brain Res 145 (2002) 207-214
30. Gerloff C., Braun C., Staudt M., Hegner Y.L., Dichgans J., and Krageloh-Mann I. Coherent corticomuscular oscillations originate from primary motor cortex: evidence from patients with early brain lesions. Hum Brain Mapp 27 (2006) 789-798. This is an investigation of patients who have sustained damage to M1 around the time of birth. Following reorganisation, the contra-lesional hand is now controlled by ipsilateral M1, but contralateral S1. Corticomuscular coherence is seen only with M1, not S1. This argues that corticomuscular coherence is not related to sensory pathways.
31. Soteropoulos D.S., and Baker S.N. Different contributions of the corpus callosum and cerebellum to motor coordination in monkey. J Neurophysiol 98 (2007) 2962-2973
32. Pfurtscheller G., Neuper C., Brunner C., and da Silva F.L. Beta rebound after different types of motor imagery in man. Neurosci Lett 378 (2005) 156-159
33. MacKay W.A. Synchronised neuronal oscillations and their role in motor processes. Trends Cogn Sci 1 (1997) 176-182
34. Ahissar E. Temporal-code to rate-code conversion by neuronal phase-locked loops. Neural Comput 10 (1998) 597-650
35. Ahissar E., Haidarliu S., and Zacksenhouse M. Decoding temporally encoded sensory input by cortical oscillations and thalamic phase comparators. Proc Natl Acad Sci U S A 94 (1997) 11633-11638
36. Cordo P., Gurfinkel V.S., Bevan L., and Kerr G.K. Proprioceptive consequences of tendon vibration during movement. J Neurophysiol 74 (1995) 1675-1688
37. Harris C.M., and Wolpert D.M. Signal-dependent noise determines motor planning. Nature 394 (1998) 780-784
38. Perez M.A., Lundbye-Jensen J., and Nielsen J.B. Changes in corticospinal drive to spinal motoneurones following visuo-motor skill learning in humans. J Physiol 573 (2006) 843-855. Subjects were trained to perform complex ankle movements to trace an outline under visual feedback. Following a training session, beta-band corticomuscular coherence was transiently enhanced. This did not occur following a control session involving movement without visuomotor skill learning.
39. Gilbertson T., Lalo E., Doyle L., Di Lazzaro V., Cioni B., and Brown P. Existing motor state is favored at the expense of new movement during 13-35 Hz oscillatory synchrony in the human corticospinal system. J Neurosci 25 (2005) 7771-7779. Subjects made rapid ballistic movements in response to a visual cue, which was triggered either from periods of high beta-band activity in a finger tremor recording, or randomly. Movements triggered during oscillations were smaller in amplitude. Additionally, the transcortical component of the stretch reflex was enhanced during oscillatory epochs. Results were confirmed using electrocorticogram recordings from somatosensory and motor cortices of patients. This suggests that during beta-oscillations, the motor system is configured to maintain a stable state.
40. Androulidakis A.G., Doyle L.M., Gilbertson T.P., and Brown P. Corrective movements in response to displacements in visual feedback are more effective during periods of 13-35 Hz oscillatory synchrony in the human corticospinal system. Eur J Neurosci 24 (2006) 3299-3304
41. Androulidakis A.G., Doyle L.M., Yarrow K., Litvak V., Gilbertson T.P., and Brown P. Anticipatory changes in beta synchrony in the human corticospinal system and associated improvements in task performance. Eur J Neurosci 25 (2007) 3758-3765. Subjects were asked to resist a stretch perturbation to the finger. Prior to the stimulus, a warning cue indicated that a stretch would occur. This led to a rise in beta-band coherence between the cortex and the periphery. By contrast, a cue indicating that the subject must make a voluntary reaction to a subsequent stimulus produced a fall in beta-band coherence. These results support the idea that beta-band oscillations act to stabilise motor output.
42. Kristeva R., Patino L., and Omlor W. Beta-range cortical motor spectral power and corticomuscular coherence as a mechanism for effective corticospinal interaction during steady-state motor output. Neuroimage 36 (2007) 785-792. Subjects tried to exert steady contractions. Periods of high beta-band corticomuscular coherence were associated with more stable motor output.
43. Baker S.N., Kilner J.M., Pinches E.M., and Lemon R.N. The role of synchrony and oscillations in the motor output. Exp Brain Res 128 (1999) 109-117
44. Omlor W., Patino L., Hepp-Reymond M.C., and Kristeva R. Gamma-range corticomuscular coherence during dynamic force output. Neuroimage 34 (2007) 1191-1198. When subjects attempted to maintain a constant finger position in the face of a slowly varying (0.7 Hz) sinusoidal resisting force, corticomuscular coherence at gamma-band (∼40 Hz) appeared. This contrasted with beta-band coherence during steady contraction. The authors suggest the higher frequency oscillations subserve integration of visual and somatosensory information.
45. Schoffelen J.M., Oostenveld R., and Fries P. Neuronal coherence as a mechanism of effective corticospinal interaction. Science 308 (2005) 111-113. Subjects exerted a steady contraction as they waited to respond to a cue. Gamma band corticomuscular coherence occurred. The time course of the coherence modulation during the holding period paralleled changes in the 'hazard rate': the probability that the subject would be required to respond at any given moment. The authors suggested the gamma band coherence promoted effective corticospinal communication, so that the response to the cue was better transmitted to the motoneuron pools.