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Figure 5. Coherence between EMGs and between EMGs and primary motor cortex local field potentials in a primate performing a steady pincer grip task A-C relate to first dorsal interosseous muscle (1DI); D-F relate to adductor pollici muscle (AdP). The bars at the top of the two columns indicate the range over which the amplifiers had a flat frequency response. A and D, EMG power spectra. A small ~20 Hz peak is present in D. B and E, coherence between cortical slow wave and simultaneously recorded EMG from 1DI and AdP, respectively. C and F, coherence between cortical slow wave recording from a different cortical site and simultaneously recorded 1DI and AdP EMGs. Large values of coherence at 0 Hz (DC) have been removed. The insets in B-F represent cross-correlations between the slow wave and the EMG; the arrow indicates time zero. Scale bars are 20 ms, r = 0·01. G, coherence between simultaneously recorded EMGs from 1DI and AdP during a steady pincer grip. Coherence at ~20 Hz is present between the cortical slow wave and EMGs from 1DI and AdP. Due to electrical cross-talk coherence is present between 1DI and AdP EMGs at all frequencies. However, a large peak is present at ~20 Hz, the same frequency at which coherence is observed between the cortical slow wave and EMG. Compare, in this paper, Fig. 5G with Fig. 3B-C and Fig. 5B-F with Fig. 4E and G. (Reproduced from Baker et al. 1997.)

Does the experimental data from the motor system in primates and man allow for certain problems of motor control to be construed in terms of binding and combination with a solution in terms of temporal correlation? The architecture of the primary and pre-motor areas consists of multiple and spatially overlapping representations within an area (Kwan, MacKay, Murphy & Wong, 1978; Sanes, Donoghue, Thangaraj, Edelman & Warach, 1995) and through branching of corticospinal axons which are distributed to functionally related muscle groups, the existence of muscle fields (Shinoda, Zarzecki & Asanuma, 1979; Cheney & Fetz, 1985; for review, see also Porter & Lemon, 1993). As in the sensory system, the motor system must solve the problem of segregation and co-operation between neuronal assemblies whose relation to one another and their target motoneurones is spatially complex. The binding problem may be defined for the motor system as the formation of associations between the distributed motor systems necessary for the spatiotemporal co-ordination of the activity of different muscles involved in the same motor task. Avoidance of the 'combinatorial explosion' might involve the establishment of separate neural assemblies within the motor system in order to accomplish separate yet contemporaneous tasks, for example, walking and chewing gum, to quote a famous aphorism! For the reasons so clearly put forward by the sensory physiologists, the solutions to these problems offered by millisecond time scale temporal correlations would seem highly attractive and an essential addition to simple rate coding solutions. In the following sections I shall consider the problems and controversies that have arisen during the initial attempts to construe motor and sensorimotor integration in terms of millisecond time scale synchronization within and between rhythmically firing upper and lower motoneurones.

The question of phase

The studies of visual cortex demonstrate that the 40 Hz oscillations are synchronized, and thus in the time domain there is a peak at time zero despite significant conduction delays (see Fig. 1). In the frequency domain the phase would be flat at zero radians across the frequencies at which the signals are coherent. Singer (1993) has argued that it is the very rhythmicity of the neuronal firing that allows zero phase lag synchronization to develop within a few cycles. Because, during rhythmic firing, the time of occurrence of one spike predicts with accuracy the time of occurrence of the next spike, two groups of neurones firing rhythmically at similar frequencies may, within a few cycles, synchronize their discharges. Recently a mechanism of doublet firing has been proposed to explain zero time lag synchronization across large cortical distances (Traub, Whittington, Stanford & Jefferys, 1996). Data from the primate motor system suggest that at the level of the cortex synchronization is maintained across considerable distances and even between homologous left and right cortical areas (Murthy & Fetz, 1996b). However, phase reversal may occur as a function of cortical depth (Murthy & Fetz, 1996a). Recordings of human MEG and EMG suggest that the signals are synchronized (see Fig. 4G). Although there is no pure delay, the phase between MEG and EMG may vary between 0 and 180 deg. Thus Conway et al. (1995) failed to demonstrate a consistent phase lag corresponding to the known 20-25 ms conduction delay between sensorimotor cortex and muscles activated during isometric contraction (for discussion, see also Halliday et al. 1998). Volkmann et al. (1996) investigated MEG-EMG correlations using magnetic field tomography to define the spatiotemporal distribution of cortical currents during Parkinsonian resting tremor. They found that in relation to the onset of flexor muscle EMG a magnetic source appeared in the sensorimotor cortex at -2 ms, i.e. practically synchronous with the EMG burst. In contrast, the study of Salenius et al. (1997), whilst confirming the presence of 20 Hz coherence between MEG and EMG during steady muscle contraction, claimed also to show a phase lag corresponding to the conduction time between motor cortex and muscle. This study used spike-triggered averaging to calculate the lag between MEG and EMG. It can be seen from their published records that the spike-triggered averaged MEG may have undergone phase reversal, possibly reflecting differing dipole orientation in leg compared with hand areas of the motor cortex. Possibly this, rather than a pure phase delay, explains the apparent shift which, it is claimed, mirrors the known increase in cortex to muscle conduction time when comparing arm with leg muscles.

The available monkey data derived from cycle triggered averages and cross-correlations demonstrates co-modulation of LFP oscillations and EMG. The co-modulation appears out of phase but there is no consistent phase delay (Murthy & Fetz, 1992, 1996a; Baker et al. 1997). The timing of CM discharge with respect to rhythmic fluctuations in the LFP is still being studied. Murthy & Fetz (1996b) noted a close temporal relationship, with the CM discharging 2·7 ms before the peak LFP negativity.

Studies of hippocampus suggest an interesting way of considering the phase relationship between unitary and slow wave activity. It has been shown that a systematic change in the phase relationship between complex spike discharges of single CA1 and CA3 units and the hippocampal theta rhythm oscillations accompanies alterations in an animal's spatial position (O'Keefe & Reece, 1993). In the motor system the overall correlation between MEG/EEG/LFP and EMG may be at zero delay; it is possible, however, that the discharges of single corticomotoneurones may vary their timing systematically with respect to the 20 Hz cortical rhythm. Whether such a delay can be demonstrated to reflect systematically either differing limb to cortex conduction times or changes in limb position it is not yet known. The issue of phase, phase reversal and phase delay clearly will remain contentious. The studies discussed above apply only to maintained posture. We do not know if correlation between cortical activity and the EMG occurs during fast ballistic movements and whether during such movements, which are less dependent on sensory feedback, if correlation is present, a different phase relationship obtains.

The question of frequency

There are numerous rhythms represented in the animal and human brain. Studies of visual processing have focused on 40 Hz oscillations in the so-called gamma range. The primate motor system studies suggest that the important oscillations are somewhat slower at 20-30 Hz (the beta range of frequencies), although in cat 30-100 Hz oscillations in the cerebellothalamic pathway have been found to be synchronous with motor cortex potentials (Timofeev & Steriade, 1997). The 20-30 Hz motor cortex oscillations are most prominent during preparation to move and during maintained posture. During actual movement they reduce (Sanes & Donoghue, 1993). In man, slow finger movements can be shown to be discontinuous with a frequency of 10 Hz (Valbo & Wessberg, 1993). Synchronization at 10 Hz has been detected between different muscles during movement (Conway, Biswas, Halliday, Farmer & Rosenberg, 1997) but as yet 10 Hz synchronization has not been found in MEG-EMG coherence (B. A. Conway, D. M. Halliday, S. F. Farmer & J. R. Rosenberg, unpublished observations). It is possible that during slow movement 10 Hz drive may not be expressed at the level of the motor cortex, and one might speculate at this point about the possible role of the somatosensory cortex and cerebellum in producing such rhythms (see Salmelin & Hari, 1994; for discussion of 13-18 Hz cerebellar LFP oscillations, see Welsh & Llinas, 1997; Pellerin & Lamarre, 1997).

Do the various different frequencies expressed at the levels of cortex and muscle have differing significance? The study of Roelfsema, Engel, Konig & Singer (1997) has demonstrated zero time lag synchronization between different cortical areas involved with visual processing and behavioural response. In this study, correlations between LFPs occured in the range 20-25 Hz. The correlations were maximal between functionally related areas, for example between areas 7 and 17 (visual cortex and posterior parietal association area) and between areas 5 and 4 (anterior parietal association area and motor cortex). Correlations were absent between the visual (area 17) and motor (area 4) cortices. The earlier studies suggested that during feature detection visual cortical synchronization occurs at 40 Hz. The sensorimotor cortex synchronization occurs at 20-30 Hz. Do different frequencies modulate one another? Do these areas interact through an interim frequency? Can one frequency act as a carrier? Are the frequencies task dependent? Also it should be noted that within a functional system, frequencies can reduce with time from the gamma to the beta range (Whittington, Traub, Faulkner, Stanford & Jefferys, 1997; Roelfsema et al. 1997). We do not yet know at the level of the cortex how different frequencies interact; the necessary mathematical analysis required in order to demonstrate such interaction is complex and non-linear (Bullock & Achimowicz, 1994; Halliday, Rosenberg, Amjad, Breeze, Conway & Farmer, 1995; Friston et al. 1996). Nevertheless the relationship between different frequency ranges and its functional significance needs to be addressed.

The behavioural significance of oscillations

The components of movement may be summarized as follows: (a) preparation to move; (b) movement (with varying types and amount of sensory feedback); (c) maintenance of posture (again with differing sensory feedback). Components (a)-(c) may involve motor synergies as well as isolated movement.

In insects it has been demonstrated that chemical blocking of 30 Hz LFP olfactory oscillations results in impairment of odour discrimination and degradation of a conditioned behavioural task (Stopfer, Bhagavan, Smith & Laurent, 1997). At the level of the primate motor cortex, synchronous 20 Hz oscillations may be proposed to have a functional role in segregating and integrating the activities of different muscle representations engaged in a motor task. Furthermore, task-dependent coherence may be detected between cortical activity and the EMG and between EMGs of different muscles. Such a model predicts that the different cortical representations of muscles and the motoneurones of different muscles, engaged in the same motor task, will be commonly modulated by high frequency 20 Hz oscillations and that this common modulation will be lost when the muscles are acting independently. Farmer et al. (1993a) found that during co-abduction of the index and middle fingers, the motor unit discharges of first and second dorsal interosseous muscles were coherent at zero phase lag in the frequency range 16-32 Hz. In monkey and man it has been shown that 20 Hz LFP/MEG/EEG oscillations are present during motor preparation, decrease during limb movement and are re-established during maintained contraction (Penfield, 1954; Pfurtscheller, 1981; Pfurtscheller & Arinbar, 1989; Sanes & Donoghue, 1993; Feige, Kristeva-Feige, Rossi, Pizzella & Rossini, 1996; Baker et al. 1997; Pfurtscheller, Stancak & Edlinger, 1997). During a ramp and hold pincer grip task in monkey task related changes in 20 Hz coherence have been demonstrated (Baker et al. 1997). During the movement phase of the task there is little 20 Hz coherence between LFPs from different cortical sites, between the LFPs and the EMG or between EMGs of functionally related muscles (1DI and AdP; see Fig. 5). However, synchronous 20 Hz activity develops between cortical sites, between the LFP and EMG and between the EMGs themselves during the maintained (hold) phase of the task. There is some evidence that this also occurs in humans. Conway et al. (1997) demonstrated that coherence between the EMGs of different muscles during slow movements occurs at 10 Hz. In contrast, during maintained co-contraction of the same muscle pair, 20 Hz coherence is observed between the EMGs. Coherence between the MEG and EMG in man is not present during movement but develops in the frequency range 16-26 Hz during maintained contraction (B. A. Conway, D. M. Halliday, S. F. Farmer & J. R. Rosenberg, unpublished observations).

The difficult question of how rhythmic synchronization may help to unite distributed neuronal assemblies in the monkey motor cortex has been further addressed in a detailed study by Murthy & Fetz (1996a, b). In this study, motor cortex LFPs along with single and multiple CM unit activity and EMGs were recorded from awake behaving monkeys performing a variety of tasks. Murthy & Fetz (1996b) defined task-sensitive CM cells as those that modulated their discharge rates in response to exploratory or manipulative hand movements. The degree of synchronization between neurones that were sensitive to the same task was compared with that seen when one or both of the neurones were not task sensitive. Some tasks were well rehearsed and required little sensory feedback for successful completion; other tasks, for example use of a Kluver board, or retrieval of a reward from a position away from the monkey's line of vision, were complex and judged to require sustained attention and high levels of sensorimotor integration. The temporal binding hypothesis suggests that the more demanding tasks will be associated with greater prevalence and more widespread synchronization between disparate cell groups in the motor cortex. In addition, neurones with similar task sensitivity may show greater synchronization than neurones with differing task sensitivity. Furthermore, tasks requiring bilateral hand movements should show greater inter-hemispheric synchronization than tasks requiring unilateral hand movements. Finally, it was predicted that, to a degree, the presence or absence of synchronization would be independent of CM firing rate.

In the event, Murthy & Fetz (1996a, b) failed to establish a simple relationship between task, the performance of complex movements and the need for greater levels of intra- and inter-cortical synchronization. They have interpreted their findings as supporting a role for 20-30 Hz oscillations in tasks requiring sustained attention. However, two points need to be made. First, the study only used time domain analysis. Comparisons across tasks were to some extent made difficult because only data where visible oscillations were present were used in the analysis. Frequency domain analysis may, through emphasizing the data differently, have given different results. Secondly, although the tasks differed in complexity all required fine finger movements during which period, according to the findings of Sanes & Donoghue (1993) and Baker et al. (1997), a reduction in 20-30 Hz oscillations would have been expected. The experiments did not examine different maintained 'hold' tasks of varying type and complexity when oscillations might be expected to be more prevalent and important.

The relationship between motor task, cortical oscillations and EMG modulation is therefore complex. I believe human and primate data may be summarized as follows. In monkey, Sanes & Donoghue (1993) and Baker et al. (1997) have shown a decrease in 20 Hz oscillations with movement, with an increase during maintained contraction. Murthy & Fetz (1992, 1996a, b) have used more complex natural tasks and observe a positive relationship between the prevalence of 20 Hz oscillations and task complexity yet do not demonstrate a simple relationship between time domain measures of synchronization and task-related neurones. Baker et al. (1997) further demonstrated increased coherence during maintained co-contraction. In man, the primate findings are mirrored by 20 Hz EEG/MEG power decreases before and during movement (Pfurtscheller, 1981; Pfurtscheller & Arinbar, 1989; Feige et al. 1996), yet interestingly, and in contrast to the findings of Baker et al. (1997), coupling between different motor areas as expressed by 20 Hz EEG coherence has recently been shown to actually increase during movement (Leocani, Toro, Manganotti, Zhuang & Hallett, 1997). This raises the interesting possibility of a task-related dissociation between the 20 Hz coherence observed to involve different motor cortex areas (e.g. primary motor cortex and supplementary motor area) and that observed within primary motor cortex or between primary motor cortex and muscle.

Some of the apparent differences between the above may yet be resolved through the more uniform application of signal analysis techniques. Ultimately, however, the difficulty may be that the very nature of synchronization, both at the level of the cortex, between cortex and EMG and between EMGs, is extremely dynamic and flexible and thus difficult to associate closely with motor task. This may explain why, so far, close relationships have been demonstrated only for relatively simple ramp and hold pincer grip tasks. It is of great interest, therefore, that the use of a dynamic correlation measure in which temporally nearly coincident (within 5 ms) CM discharges were logged, has shown task- and context-dependent synchronization (Riehle, Grun, Diesmann & Aertsen, 1997). Tightly synchronized CM discharges may occur in temporal relation to different phases of a voluntary movement. They were shown to occur in temporal relation to external events, i.e. stimuli and movements, but also during periods of stimulus expectancy. During the latter paradigm, spike synchronization occurred independently of firing rate modulations. Interestingly, as far as could be ascertained using time domain measures, the synchronization was not conspicuously periodic. Thus in primates brief time varying temporal associations may provide a flexible code suitable for solving the motor system binding problem.

Conclusions

Whilst there is much more work to be done, the evidence in sensory and motor systems of animals and man indicates that synchronous oscillatory activity is ubiquitous, spreads across large anatomical distances and is behaviourally relevant. Temporal pattern coding is likely to prove an important addition to rate coding and may well provide a solution to the binding problem for the motor system. Finally, in man many pathological states such as Parkinson's disease, essential tremor, dystonia and myoclonus may involve abnormal synchronization between motoneurones themselves and between EMG activity and the motor cortex (Volkmann et al. 1995; Halliday et al. 1997; Farmer et al. 1998; P. Brown, S. F. Farmer, D. M. Halliday & J. R. Rosenberg, unpublished observations). Time and frequency domain analysis of simultaneous MEG/EEG and EMG recordings affords a fascinating opportunity to uncover more of the pathophysiology of these conditions.

Baker, S. N., Olivier, E. & Lemon, R. N. (1997). Coherent oscillations in the monkey motor cortex and hand muscle EMG show task-dependent modulation. The Journal of Physiology 501, 225-241.

[Abstract] Bouyer, J. J., Montaron, M. F., Vahnee, J. M., Albert, M. P. & Rougeul, A. (1987). Anatomical localization of cortical beta rhythms in cat. Neuroscience 22, 863-869.

[Medline] Bullock, T. H. & Achimowicz, J. Z. (1994). A comparative study of event-related brain oscillations. In Oscillatory Event-related Brain Dynamics, ed. Pantev, C., Elbert, T. & Lutkenhoner, B., pp. 11-26. Plenum Press, New York.

Cheney, P. D. & Fetz, E. E. (1985). Comparable patterns of muscle facilitation evoked by individual corticomotoneuronal (CM) cells and by single intracortical microstimulation in primate. Evidence for functional groups of CM cells. Journal of Neurophysiology 53, 786-804.

[Medline] Conway, B. A., Biswas, P., Halliday, D. M., Farmer, S. F. & Rosenberg, J. R. (1997). Task-dependent changes in rhythmic motor output during voluntary elbow movement in man. The Journal of Physiology 501.P, 48-49P.

Conway, B. A., Halliday, D. M., Farmer, S. F., Shahani, U., Maas, P. Weir, A. I. & Rosenberg, J. R. (1995). Synchronization between motor cortex and spinal motoneuronal pool during the performance of a maintained motor task in man. The Journal of Physiology 489, 917-924.

[Abstract] Datta, A. K., Farmer, S. F. & Stephens, J. R. (1991). Central nervous pathways underlying synchronization of human motor unit firing studied during voluntary contractions. The Journal of Physiology 428, 561-577.

[Abstract] Datta, A. K. & Stephens, J. A. (1990). Short-term synchronization of motor unit activity during voluntary contraction in man. The Journal of Physiology 422, 397-419.

[Abstract] Eckhorn, R., Bauer, R, Jordan, W., Brosch, M., Kruse, W., Munk, M. & Reitbeock, H. J. (1988). Coherent oscillations: a mechanism for feature linking in the visual cortex? Multiple electrode and correlation analyses in the cat. Biological Cybernetics 60, 121-130.

[Medline] Engel, A. K., Konig, P., Kreiter, A. K., Schillen, T. B. & Singer, W. (1992). Temporal coding in the visual cortex: new vistas on integration in the nervous system. Trends in Neurosciences 15, 218-226.

[Medline] Engel, A. K., Kreiter, A. K., Konig, P. & Singer, W. (1991). Synchronization of oscillatory neuronal responses between striate and extrastriate visual cortical areas of the cat. Proceedings of the National Academy of Sciences of the USA 88, 6048-6052.

[Abstract] Farmer, C., Farmer, S. F., Halliday, D. M., Rosenberg, J. R. & Stephens, J. A. (1990a). Coherence analysis of motor unit firing recorded during voluntary contraction in man. The Journal of Physiology 420, 22P.

Farmer, S. F., Bremner, F. D., Halliday, D. M., Rosenberg, J. R. & Stephens, J. A. (1993a). The frequency content of common synaptic inputs to motoneurones studied during voluntary isometric contraction in man. The Journal of Physiology 470, 127-155.

[Abstract] Farmer, S. F., Ingram, D. A. & Stephens, J. A. (1990b). Mirror movements studied in a patient with Klippel-Feil syndrome. The Journal of Physiology 428, 467-484.

[Abstract] Farmer, S. F., Sheean, G. L., Mayston, M. J., Rothwell, J. C., Marsden, C. D., Conway, B. A., Halliday, D. M., Rosenberg, J. R. & Stephens, J. A. (1998). Abnormal motor unit synchronization between antagonist muscles underlies pathological co-contraction in upper limb dystonia. Brain 121, 799-812.

Farmer, S. F., Swash, M., Ingram, D. A. & Stephens, J. A. (1993b). Changes in motor unit synchronization following central nervous lesions in man. The Journal of Physiology 463, 83-105.

[Abstract] Feige, B., Kristeva-Feige, R., Rossi, S., Pizzella, V., Rossini, P.-M. (1996). Neuromagnetic study of movement-related changes in rhythmic brain activity. Brain Research 734, 252-260.

[Medline] Fries, P., Roelfsema, P. R., Engel, A. K., Konig, P. & Singer, W. (1997). Synchronization of oscillatory responses in visual cortex correlates with perception in interocular rivalry. Proccedings of the National Academy of Sciences of the USA 94, 12699-12704.

Friston, K. J., Stephan, K. M., Heather, J. D., Frith, C. D., Ioannides, A. A., Liu, L. C., Rugg, M. D., Vieth, J., Keber, H., Hunter, K. & Frackowiack, R. S. J. (1996). A multivariate analysis of evoked responses in EEG and MEG data. Neuroimage 3, 167-174.

[Medline] Gray, C. M. (1994). Synchronous oscillations in nervous systems: Mechanisms and functions. Journal of Computational Neuroscience 1, 11-38.

[Medline] Gray, C. M., Konig, P., Engel, A. K. & Singer, W. (1989). Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338, 334-337.

[Medline] Gray, C. M. & Singer, W. (1989). Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proceedings of the National Academy of Sciences of the USA 86, 1678-1702.

Halliday, D. M., Conway, B. A., Farmer, S. F. & Rosenberg, J. R. (1998). On the use of the EEG to explore functional aspects of correlations between cortical recordings and muscle EMG during voluntary contractions in human. Neuroscience Letters 241, 5-8.

[Medline] Halliday, D. M., Conway, B. A., Shahani, U., Russell, A., Farmer, S. F., Weir, A. I. & Rosenberg, J. R. (1997). Coherence estimates between cortical activity and motor output in subjects with essential tremor. The Journal of Physiology 501.P, 38P.

Halliday, D. M., Rosenberg, J. R., Amjad, A. M., Breeze, P., Conway, B. A. & Farmer, S. F. (1995). A framework for the analysis of mixed time series/point process data-theory and application to the study of physiological tremor, single motor unit discharges and electromyograms. Progress in Biophysics and Molecular Biology 64, 237-278.

[Medline] Kirkwood, P. A. & Sears, T. A. (1978). Synaptic connections to intercostal motoneurones as revealed by the common excitation potential. The Journal of Physiology 275, 102-134.

Kwan, H. C., Mackay, W. A., Murphy, J. T. & Wong, Y. C. (1978). Spatial organization of precentral cortex in awake primates. II Motor outputs. Journal of Neurophysiology 41, 1120-1131.

[Medline] Leocani, L., Toro, C., Manganotti, P., Zhuang, P. & Hallett, M. (1997). Event-related coherence and event-related desynchronization/synchronization in the 10 Hz and 20 Hz EEG during self-paced movements. Electroencephalography and Clinical Neurophysiology 104, 199-206.

[Medline] Mills, K. R. & Schubert, M. (1995). Short term synchronization of human motor units and their responses to transcranial magnetic stimulation. The Journal of Physiology 483, 511-523.

[Abstract] Murthy, V. N & Fetz, E. E. (1992). Coherent 25- to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys. Proceedings of the National Academy of Sciences of the USA 89, 5670-5674.

[Abstract] Murthy, V. N & Fetz, E. E. (1996a). Oscillatory activity in sensorimotor cortex of awake monkeys: Synchronization of local field potentials and relation to behaviour. Journal of Neurophysiology 76, 3949-3967.

[Medline] Murthy, V. N & Fetz, E. E. (1996b). Synchronizaton of neurones during local field potential oscillations in sensorimotor cortex of awake monkeys. Journal of Neurophysiology 76, 3968-3982.

[Medline] Nunez, P. L. (1995). Neocortical Dynamics and Human EEG Rhythms. Oxford University Press, New York.

O'Keefe, J. & Reece, M. L. (1993). Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3, 317-330.

[Medline] Pellerin, J.-P. & Lamarre, Y. (1997). Local field potential oscillations in primate cerebellar cortex during voluntary movement. Journal of Neurophysiology 78, 3502-3507.

[Abstract/Full Text] Penfield, W. (1954). Mechanisms of voluntary movement. Brain 77, 1-17.

Pfurtscheller, G. (1981). Central beta rhythm during sensorimotor activities in man. Electroencephalography and Clinical Neurophysiology 51, 253-264.

[Medline] Pfurtscheller, G. & Aranibar, A. (1989). Event-related desynchronization detected by power measurements of scalp EEG. Electroencephalography and Clinical Neurophysiology 72, 250-258.

[Medline] Pfurtscheller, G., Stancak, A. & Edlinger, G. (1997). On the existence of different types of central beta rhythms below 30 Hz. Electroencephalography and Clinical Neurophysiology 102, 316-325.

[Medline] Porter, R. & Lemon, R. (1993). Corticospinal Function and Voluntary Movement. Monographs of the Physiological Society, No. 45, Oxford University Press, New York.

Riehle, A., Grun, S., Diesmann, M. & Aertsen, A. (1997). Spike synchronization and rate modulation differentially involved in motor cortical function. Science 278, 1950-1953.

[Abstract/Full Text] Roelfsema, P. R., Engel, A. K., Konig, P. & Singer, W. (1997). Visuomotor integration is associated with zero time-lag synchronization among cortical areas. Nature 385, 157-161.

[Medline] Salenius, S., Portin, K., Kajola, M., Salmelin, R. & Hari, R. (1997). Cortical control of human motoneuron firing during isometric contraction. Journal of Neurophysiology 77, 3401-3405.

[Abstract/Full Text] Salmelin, R. & Hari, R. (1994). Spatiotemporal characteristics of sensorimotor neuromagnetic rhythms related to thumb movement. Neuroscience 60, 537-550.

[Medline] Sanes, J. N. & Donoghue, J. P. (1993). Oscillations in local field potentials of the primate motor cortex. Proceedings of the National Academy of Sciences of the USA 90, 4470-4474.

[Abstract] Sanes, J. N., Donoghue, J. P., Thangaraj, V., Edelman, R. R. & Warach, S. (1995). Shared neural correlates controlling hand movements in human motor cortex. Science 268, 1775-1777.

[Medline] Sears, T. A. & Stagg, D. (1976). Short-term synchronization of intercostal motoneurone activity. The Journal of Physiology 263, 357-381.

[Abstract] Shinoda, Y., Zarzecki, P. & Asanuma, H. (1979). Spinal branching of pyramidal tract neurones in the monkey. Experimental Brain Research 34, 59-72.

[Medline] Singer, W. (1993). Synchronization of cortical activity and its putative role in information processing and learning. Annual Review of Physiology 55, 349-374.

[Medline] Singer, W. & Gray, C. M., (1995). Visual feature integration and the temporal correlation hypothesis. Annual review of Neuroscience 18, 555-586

[Medline] Stopfer, M., Bhagavan, S., Smith, B. H. & Laurent, G. (1997). Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature 390, 70-74.

[Medline] Timofeev, I. & Steriade, M. (1997). Fast (mainly 30-100 Hz) oscillations in the cat cerebellothalamic pathway and their synchronization with cortical potentials. The Journal of Physiology 504, 153-168.

[Abstract] Traub, R. D., Whittington, M. A., Stanford, I. M. & Jefferys, J. G. R. (1996). A mechanism for the generation of long-range synchronous fast oscillations in the cortex. Nature 383, 621-624.

[Medline] Valbo, A. B. & Wessberg, J. (1993). Organization of motor output in slow finger movements in man. The Journal of Physiology 469, 673-691.

[Abstract] Volkmann, J., Joliot, M., Mogilner, A., Ionnides, A. A., Lado, F., Fazzini, E., Ribary, U. & Llinas, R. (1996). Central motor loop oscillations in Parkinsonian resting tremor revealed by magnetoenephalography. Neurology 46, 1359-1370.

[Abstract] Von der Malsburg, C. (1995). Binding in models of perception and brain function. Current Opinion in Neurobiology 5, 520-526.

[Medline] Welsh, J. & Llinas, R. (1997). Some organizing principals for the control of movement based on olivocerebellar physiology. In The Cerebellum from Structure to Control, ed. De Zeeuw, C. I., Strata, P. & Voogd, J., Progress in Brain Research , vol. 114, pp. 449-461. Elsevier, New York.

Whittington, M. A., Traub, R. D., Faulkner, H. J., Stanford, I. M. & Jefferys, J. G. R. (1997). Recurrent excitatory post synaptic potentials induced by synchronized fast oscillations. Proceedings of the National Academy of Sciences of the USA 94, 12198-12203.

[Abstract/Full Text]

Acknowledgements

My great thanks to Dr Bernie Conway, Dr David Halliday and Professor Jay Rosenberg for our friendship, collaboration and discussions over many years.

Address for correspondence

Department of Neurology, The National Hospital for Neurology and Neurosurgery, Queen Square, London WC1N 3BE, UK.

Author's email address

s.farmer@ion.ucl.ac.uk

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				V. Marchenko and R. F. Rogers Time-frequency coherence analysis of phrenic and hypoglossal activity in the decerebrate rat during eupnea, hyperpnea, and gasping Am J Physiol Regulatory Integrative Comp Physiol, November 1, 2006; 291(5): R1430 - R1442. [Abstract] [Full Text] [PDF]

				F. J. Urbano, J. I. Simpson, and R. R. Llinas Somatomotor and oculomotor inferior olivary neurons have distinct electrophysiological phenotypes PNAS, October 31, 2006; 103(44): 16550 - 16555. [Abstract] [Full Text] [PDF]

				J. Y. Sebe, J. F. van Brederode, and A. J. Berger Inhibitory Synaptic Transmission Governs Inspiratory Motoneuron Synchronization J Neurophysiol, July 1, 2006; 96(1): 391 - 403. [Abstract] [Full Text] [PDF]

				M. A. Perez, J. Lundbye-Jensen, and J. B. Nielsen Changes in corticospinal drive to spinal motoneurones following visuo-motor skill learning in humans J. Physiol., June 15, 2006; 573(3): 843 - 855. [Abstract] [Full Text] [PDF]

				J. A. Johnston, S. A. Winges, and M. Santello Periodic Modulation of Motor-Unit Activity in Extrinsic Hand Muscles During Multidigit Grasping J Neurophysiol, July 1, 2005; 94(1): 206 - 218. [Abstract] [Full Text] [PDF]

				P. Silberstein, A. Pogosyan, A. A. Kuhn, G. Hotton, S. Tisch, A. Kupsch, P. Dowsey-Limousin, M. I. Hariz, and P. Brown Cortico-cortical coupling in Parkinson's disease and its modulation by therapy Brain, June 1, 2005; 128(6): 1277 - 1291. [Abstract] [Full Text] [PDF]

				J. G. Semmler, M. V. Sale, F. G. Meyer, and M. A. Nordstrom Motor-Unit Coherence and Its Relation With Synchrony Are Influenced by Training J Neurophysiol, December 1, 2004; 92(6): 3320 - 3331. [Abstract] [Full Text] [PDF]

				N. L. Hansen and J. B. Nielsen The effect of transcranial magnetic stimulation and peripheral nerve stimulation on corticomuscular coherence in humans J. Physiol., November 15, 2004; 561(1): 295 - 306. [Abstract] [Full Text] [PDF]

				A. M. Taylor and R. M. Enoka Quantification of the Factors That Influence Discharge Correlation in Model Motor Neurons J Neurophysiol, February 1, 2004; 91(2): 796 - 814. [Abstract] [Full Text] [PDF]

				S. F. Farmer, L. M. Harrison, M. J. Mayston, A. Parekh, L.M. James, and J. A. Stephens Abnormal cortex-muscle interactions in subjects with X-linked Kallmann's syndrome and mirror movements Brain, February 1, 2004; 127(2): 385 - 397. [Abstract] [Full Text] [PDF]

				B. Pollok, J. Gross, M. Dirks, L. Timmermann, and A. Schnitzler The cerebral oscillatory network of voluntary tremor J. Physiol., February 1, 2004; 554(3): 871 - 878. [Abstract] [Full Text] [PDF]

				R. Maex and E. De Schutter Resonant Synchronization in Heterogeneous Networks of Inhibitory Neurons J. Neurosci., November 19, 2003; 23(33): 10503 - 10514. [Abstract] [Full Text] [PDF]

				M. A. Parkis, J. L. Feldman, D. M. Robinson, and G. D. Funk Oscillations in Endogenous Inputs to Neurons Affect Excitability and Signal Processing J. Neurosci., September 3, 2003; 23(22): 8152 - 8158. [Abstract] [Full Text] [PDF]

				A. M. Taylor, E. A. Christou, and R. M. Enoka Multiple Features of Motor-Unit Activity Influence Force Fluctuations During Isometric Contractions J Neurophysiol, August 1, 2003; 90(2): 1350 - 1361. [Abstract] [Full Text] [PDF]

				M. C. Tresch and O. Kiehn Synchronization of Motor Neurons during Locomotion in the Neonatal Rat: Predictors and Mechanisms J. Neurosci., November 15, 2002; 22(22): 9997 - 10008. [Abstract] [Full Text] [PDF]

				V. Marchenko, A. R. Granata, and M. I. Cohen Respiratory cycle timing and fast inspiratory discharge rhythms in the adult decerebrate rat Am J Physiol Regulatory Integrative Comp Physiol, October 1, 2002; 283(4): R931 - R940. [Abstract] [Full Text] [PDF]

				R. Courtemanche, J.-P. Pellerin, and Y. Lamarre Local Field Potential Oscillations in Primate Cerebellar Cortex: Modulation During Active and Passive Expectancy J Neurophysiol, August 1, 2002; 88(2): 771 - 782. [Abstract] [Full Text] [PDF]

				A. M. Taylor, J. W. Steege, and R. M. Enoka Motor-Unit Synchronization Alters Spike-Triggered Average Force in Simulated Contractions J Neurophysiol, July 1, 2002; 88(1): 265 - 276. [Abstract] [Full Text] [PDF]

				S. Farmer Neural rhythms in Parkinson's disease Brain, June 1, 2002; 125(6): 1175 - 1176. [Full Text] [PDF]

				J H McAuley, D M Corcos, J C Rothwell, N P Quinn, and C D Marsden Levodopa reversible loss of the Piper frequency oscillation component in Parkinson's disease J. Neurol. Neurosurg. Psychiatry, April 1, 2001; 70(4): 471 - 475. [Abstract] [Full Text] [PDF]

				B. Feige, A. Aertsen, and R. Kristeva-Feige Dynamic Synchronization Between Multiple Cortical Motor Areas and Muscle Activity in Phasic Voluntary Movements J Neurophysiol, November 1, 2000; 84(5): 2622 - 2629. [Abstract] [Full Text] [PDF]

				W.-X. Huang and M. I. Cohen Population and Unit Synchrony of Fast Rhythms in Expiratory Recurrent Laryngeal Discharges J Neurophysiol, August 1, 2000; 84(2): 1098 - 1102. [Abstract] [Full Text] [PDF]