Functional anatomy of motor urgency

doi:10.1016/j.neuroimage.2007.04.049

NeuroImage

Volume 37, Issue 1, 1 August 2007, Pages 243-252

https://doi.org/10.1016/j.neuroimage.2007.04.049 Get rights and content

Abstract

This PET H₂¹⁵O study uses a reaching task to determine the neural basis of the unconscious motor speed up observed in the context of urgency in healthy subjects. Three conditions were considered: self-initiated (produce the fastest possible movement toward a large plate, when ready), externally-cued (same as self-initiated but in response to an acoustic cue) and temporally-pressing (same as externally-cued with the plate controlling an electromagnet that prevented a rolling ball from falling at the bottom of a tilted ramp). Results show that: (1) Urgent responses (Temporally-pressing versus Externally-cued) engage the left parasagittal and lateral cerebellar hemisphere and the sensorimotor cortex (SMC) bilaterally; (2) Externally-driven responses (Externally-cued versus Self-initiated) recruit executive areas within the contralateral SMC; (3) Volitional responses (Self-initiated versus Externally-cued) involve prefrontal cortical areas.

These observations are discussed with respect to the idea that neuromuscular energy is set to a submaximal threshold in self-determined situations. In more challenging tasks, this threshold is raised and the first answer of the nervous system is to optimize the response of the lateral (i.e. crossed) corticospinal tract (contralateral SMC) and ipsilateral cerebellum. In a second step, the anterior (i.e. uncrossed) corticospinal tract (ipsilateral SMC) and the contralateral cerebellum are recruited. This recruitment is akin to the strategy observed during recovery in patients with brain lesions.

Introduction

In 1921 Souques described Parkinson's disease (PD) patients who could not stand up nor walk without help, but suddenly became able to run or climb a set of stairs when facing an urgent situation. This surprising improvement of motor performance was named “paradoxical kinesia”. To account for this phenomenon it was suggested that the basal ganglia (BG) could play a much more important role in internally than in externally regulated movements.

Recently, a behavioral study was conducted by our group that led us to question the notion of “paradoxical kinesia” in PD. We used a ball-catch paradigm, to investigate the effect of motor urgency in PD patients and normal subjects (Ballanger et al., 2006). We compared reaching movements requiring to press a large plate under three conditions: self-initiated: produce the fastest possible movement; externally-cued: same as self-initiated but in response to an acoustic cue; temporally-pressing: same as externally-cued with the plate controlling an electromagnet that prevented a ball falling at the bottom of a tilted ramp. Results showed that external cues and urgent conditions increased movement speed by a similar amount in PD patients and healthy subjects (temporally-pressing > externally-cued > self-initiated). This observation suggested (1) that the so-called “paradoxical kinesia” were not so paradoxical after all, and (2) that contextual variations of movement velocity were independent of BG dysfunctions.

The main aim of the present study is to investigate the neural basis of the motor speed up observed in urgent situations. As shown in previous experiments involving healthy subjects, the pattern of cerebral activation is clearly different between self-initiated and externally guided movement (Deiber et al., 1991, Deiber et al., 1999, Playford et al., 1992, Jahanshahi et al., 1995, Jenkins et al., 2000). The dorsolateral prefrontal cortex (DLPFC), rostral supplementary motor area (SMA), anterior cingulate cortex (ACC) and lateral premotor cortex have been consistently associated with self-generated motor task, and the caudal SMA, primary motor cortex and basal ganglia (BG) with externally-cued movement (Deiber et al., 1991, Deiber et al., 1999, Playford et al., 1992, Jahanshahi et al., 1995, Jenkins et al., 2000, Cunnington et al., 2002). Concerning the BG, it is worth mentioning that a significant involvement of this structure in externally-cued actions was only observed when different movements types were compared to a rest condition. No higher activation in the BG network was observed when self-initiated and externally-cued movements were compared with each other (Jahanshahi et al., 1995, Jenkins et al., 2000, Cunnington et al., 2002). An absence of systematic involvement of the BG for internally-regulated movements was also reported in electrophysiological and inactivation studies in monkeys (Kimura et al., 1992, Inase et al., 1996, Turner and Anderson, 2005).

To our knowledge, no functional imaging studies have been conducted in order to investigate the neurophysiological mechanisms that underlie the improvement of motor performance in urgent situations. The present work aims to fill this gap.

Section snippets

Subjects

Eight healthy subjects (4 males, 4 females; mean age ± S.D.: 54 ± 8.1) participated in the study. All subjects were right-handed and did not present any neurological disease.

The study was approved by the local research ethics committee. All subjects participated after the aims of the study and the nature of the procedures had been fully explained. They signed an informed consent form according to the Declaration of Helsinki.

Task

The behavioral apparatus is shown in Fig. 1. It is similar to the one used

Behavioral results

For movement duration (MD), a significant effect of the condition factor (F_2,14 = 19.50, p < 0.0001) was found. More specifically: (1) MD was longer in the Self-initiated condition (252 ms) than in the Externally-cued condition (199 ms; post-hoc, p < 0.05); (2) MD was longer in the Externally-cued (199 ms) than in the Temporally-pressing condition (164 ms; post-hoc, p < 0.05).

For the Externally-cued and Temporally-pressing experimental conditions, reaction time (RT) showed the same pattern of variation

Discussion

Behavioral data of this study shows that healthy subjects can exhibit faster motor responses when facing urgency. PET data indicate that this modulation engage the left parasagittal cerebellum, the left lateral cerebellum and the SMC bilaterally. These key findings are discussed below.

Acknowledgment

This study has been supported by a grant from the Association France Parkinson.

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¹: Both authors equally contributed to this work.

View full text

Functional anatomy of motor urgency

Abstract

Introduction

Section snippets

Subjects

Task

Behavioral results

Discussion

Acknowledgment

Behav. Brain Res.

NeuroImage

NeuroImage

NeuroImage

NeuroImage

NeuroImage

Magn. Reson. Imaging

Attentional activation of the cerebellum independent of motor involvement

Science

Movement parameters and neural activity in motor cortex and area 5

Cereb. Cortex

Associations between a cerebellar motor dysfunction scale and movement initiation and completion in olivopontocerebellar atrophy

Rev. Neurol. (Paris)

“Paradoxical kineses” are not a hallmark of Parkinson's disease but a general property of the motor system

Mov. Disord.

Pathophysiology of bradykinesia in Parkinson's disease

Brain

Rate dependence of regional cerebral activation during performance of a repetitive motor task: a PET study

J. Cereb. Blood Flow Metab.

Planning and execution of pointing movements in cerebellar patients

Mov. Disord.

Sequential activation brain mapping after subcortical stroke: changes in hemispheric balance and recovery

NeuroReport

The contribution of the anterior cingulate cortex to executive processes in cognition

Rev. Neurosci.

Functional classes of primate corticomotoneuronal cells and their relation to active force

J. Neurophysiol.

Cerebellar Purkinje cell simple spike discharge encodes movement velocity in primates during visuomotor arm tracking

J. Neurosci.

Neural activity relating to generation and representation of galvanic skin conductance responses: a functional magnetic resonance imaging study

J. Neurosci.

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Exp. Brain Res.

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J. Neurophysiol.

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