Functional Connectivity Between Cerebellum and Primary Motor Cortex in the Awake Monkey

Holdefer, Robert N.; Miller, Lee E.; Chen, L. L.; Houk, James C.

doi:10.1152/jn.2000.84.1.585

Cited by 110 publications

(71 citation statements)

References 16 publications

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“…However, to our knowledge, this is the first direct demonstration that cerebellar activity at approximately 10 Hz is coherent with a peripheral measure such as acceleration. The DCN can influence motor output via multiple pathways, including via the motor cortex (16,34) and reticular formation (35). The realization that the reticulospinal tract is likely to provide some of the descending oscillatory command during slow finger movements marks an important contribution to understanding the highly distributed nature of this system.…”

Section: Discussionmentioning

confidence: 99%

Spinal interneuron circuits reduce approximately 10-Hz movement discontinuities by phase cancellation

Williams

Soteropoulos

Baker

2010

Proc. Natl. Acad. Sci. U.S.A.

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Tremor imposes an important limit to the accuracy of fine movements in healthy individuals and can be a disabling feature of neurological disease. Voluntary slow finger movements are not smooth but are characterized by large discontinuities (i.e., steps) in the tremor frequency range (approximately 10 Hz). Previous studies have shown that these discontinuities are coherent with activity in the primary motor cortex (M1), but that other brain areas are probably also involved. We investigated the contribution of three important subcortical areas in two macaque monkeys trained to perform slow finger movements. Local field potential and singleunit activity were recorded from the deep cerebellar nuclei (DCN), medial pontomedullary reticular formation, and the intermediate zone of the spinal cord (SC). Coherence between LFP and acceleration was significant at 6 to 13 Hz for all areas, confirming the highly distributed nature of the central network responsible for this activity. The coherence phase at 6 to 13 Hz for DCN and pontomedullary reticular formation was similar to our previous results in M1. By contrast, for SC the phase differed from M1 by approximately π rad. Examination of single-unit discharge confirmed that this was a genuine difference in neural spiking and could not be explained by different properties of the local field potential. Convergence of antiphase oscillations from the SC with cortical and subcortical descending inputs will lead to cancellation of approximately 10 Hz oscillations at the motoneuronal level. This could appreciably limit drive to muscle at this frequency, thereby reducing tremor and improving movement precision.T remor is a key limitation to human fine motor performance.However, in tremor research, the puzzle is not so much why our hands shake, but why they often do not. Numerous mechanisms can contribute to unstable contraction: motoneurons are recruited at a fixed frequency, limb segments have mechanical resonance, the monosynaptic stretch reflex arc can produce feedback oscillations, and there are a plethora of central neural oscillators. These factors often converge to produce mechanical oscillations at approximately 10 Hz, the dominant frequency of physiological tremor. Yet despite these multiple sources of instability, in most people, most of the time, tremor is small enough not to impact daily life. We have hypothesized that a specific neural system might have evolved to reduce tremor (1), with clear survival advantages.Slow finger movements in man are characterized by steps or discontinuities that occur at approximately 10 Hz (2). These discontinuities provide a good model for studying tremor, as even though they occur within the same frequency range, they are an order of magnitude bigger (2), facilitating quantitative analysis. Work on both physiological tremor and slow finger movement discontinuities has shown that there is an approximately 10

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Section: Discussionmentioning

confidence: 99%

Spinal interneuron circuits reduce approximately 10-Hz movement discontinuities by phase cancellation

Williams

Soteropoulos

Baker

2010

Proc. Natl. Acad. Sci. U.S.A.

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“…The intensity of stimulation current was monitored by measuring the voltage across a serially connected 1-kΩ resistor, and was adjusted within a range of 80-100 μA. According to the previous study (Holdefer et al, 2000), this current intensity was effective to elicit neuronal response in the cerebral cortex. Because electrical stimulation did not evoke any obvious movement and exhibited only a small change in saccade latency (see Results), we used the same stimulation parameters throughout the experiments.…”

Section: Physiological Proceduresmentioning

confidence: 99%

Facilitation of temporal prediction by electrical stimulation to the primate cerebellar nuclei

2017

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The cerebellum is known to be involved in temporal information processing. However, the underlying neuronal mechanisms remain unclear. In our previous study, monkeys were trained to make a saccade in response to a single omission of periodically presented visual stimuli. To detect stimulus omission, animals had to predict the timing of each next stimulus. During this task, neurons in the cerebellar dentate nucleus exhibited a transient decrement of activity followed by a gradual increase in firing rate that peaked around the time of the next stimulus (Ohmae et al., 2013). In the present study, to address how these two components of neuronal activity contributed to omission detection, we applied electrical microstimulation to the recording site at different timing during the task. We found that electrical stimulation just before the stimulus omission shortened the latencies of both contraversive and ipsiversive saccades. Because the changes in saccade latency non-linearly depended on the timing of stimulation in each inter-stimulus interval, and electrical stimulation just before the early stimulus in the sequence failed to evoke saccades, the neuronal activity in the dentate nucleus might regulate temporal prediction rather than facilitating saccade execution. Our results support the hypothesis that the firing modulation in each inter-stimulus interval in the dentate nucleus represents neuronal code for the temporal prediction of next stimulus. AbbreviationsFP, fixation point; MRI, magnetic resonance images; SOA, stimulus onset asynchrony

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“…Thus, the plasticity that deteriorates after 40 d is more likely to be supraspinal and to be responsible for the CST influence that maintains the spinal cord plasticity. Plasticity in sensorimotor cortex and associated regions, which occurs in many physiological and pathological situations (Nudo 2003;Siebner and Rothwell 2003;Field-Fote 2004;Luft et al 2005;Sawaki 2005), is a strong possibility, and the pathways mediating cerebrocerebellar interactions, which are important for a variety of motor behaviors (Glickstein and Yeo 1990;Leiner et al 1991;Raymond et al 1996;Houk 1997;Schmahmann and Pandyat 1997;Desmond and Fiez 1998;Middleton and Strick 1998;Thach 1998;Holdefer Molinari et al 2002;Andre and Arrogi 2003;Mori et al 2004;Nitschke et al 2005), are likely to support the maintenance of this plasticity. DIN ablation had no lasting effect on animal well-being, gross motor behavior, or activity level: Rats gained weight, walked normally, and satisfied the background EMG requirement (see Materials and Methods) with the same daily frequency as before ablation.…”

Section: The Delayed H-reflex Increasementioning

confidence: 99%

The cerebellum in maintenance of a motor skill: A hierarchy of brain and spinal cord plasticity underlies H-reflex conditioning

Wolpaw¹,

Chen²

2006

Learn. Mem.

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Operant conditioning of the H-reflex, the electrical analog of the spinal stretch reflex, is a simple model of skill acquisition and involves plasticity in the spinal cord. Previous work showed that the cerebellum is essential for down-conditioning the H-reflex. This study asks whether the cerebellum is also essential for maintaining down-conditioning. After rats decreased the soleus H-reflex over 50 d in response to the down-conditioning protocol, the cerebellar output nuclei dentate and interpositus (DIN) were ablated, and down-conditioning continued for 50-100 more days. In naive (i.e., unconditioned) rats, DIN ablation itself has no significant long-term effect on H-reflex size. During down-conditioning prior to DIN ablation, eight Sprague-Dawley rats decreased the H-reflex to 57% (±4 SEM) of control. It rose after ablation, stabilizing within 2 d at about 75% and remaining there until ∼40 d after ablation. It then rose to ∼130%, where it remained through the end of study 100 d after ablation. Thus, DIN ablation in down-conditioned rats caused an immediate increase and a delayed increase in the H-reflex. The final result was an H-reflex significantly larger than that prior to down-conditioning. Combined with previous work, these remarkable results suggest that the spinal cord plasticity directly responsible for down-conditioning, which survives only 5-10 d on its own, is maintained by supraspinal plasticity that survives ∼40 d after loss of cerebellar output. Thus, H-reflex conditioning seems to depend on a hierarchy of brain and spinal cord plasticity to which the cerebellum makes an essential contribution.The challenge presented by the phenomena of learning has changed greatly in recent years. In the past, the challenge was to discover activity-dependent central nervous system (CNS) plasticity that might account for learning. Now, many different kinds of activity-dependent plasticity are known to occur throughout the CNS, and the challenge is to define exactly how this plasticity accounts for learned behavioral changes. The complexity and limited accessibility of the CNS and the fact that even simple learning involves multisite plasticity obscure the causal connections between this plasticity and behavioral changes (Wolpaw

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Functional Connectivity Between Cerebellum and Primary Motor Cortex in the Awake Monkey

Cited by 110 publications

References 16 publications

Spinal interneuron circuits reduce approximately 10-Hz movement discontinuities by phase cancellation

Spinal interneuron circuits reduce approximately 10-Hz movement discontinuities by phase cancellation

Facilitation of temporal prediction by electrical stimulation to the primate cerebellar nuclei

The cerebellum in maintenance of a motor skill: A hierarchy of brain and spinal cord plasticity underlies H-reflex conditioning

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