Review
Correction and suppression of reaching movements in the cerebral cortex: Physiological and neuropsychological aspects

https://doi.org/10.1016/j.neubiorev.2014.03.002Get rights and content

Highlights

  • A common modular architecture underlies both correction and suppression of reaching.

  • The key node of the parieto-frontal network for movement correction and suppression is premotor cortex.

  • Reaching and its correction are based on the same set of muscle synergies appropriately modulated in amplitude and timing.

Abstract

Modification or suppression of reaches occurs in everyday life. We argue that a common modular architecture, based on similar neural structures and principles of kinematic and kinetic control, is used for both direct reaches and for their on-line corrections. When a reach is corrected, both the pattern of neural activity in parietal, premotor and motor cortex and the muscle synergies associated with the first movement can be smoothly blended or sharply substituted into those associated with the second one. Premotor cortex provides the early signaling for trajectory updating, while parietal and motor cortex provide the fine-grained encoding of hand kinematics necessary to reshape the motor plan. The cortical contribution to the inhibitory control of reaching is supported by the activity of a network of frontal areas. Premotor cortex has been proposed as a key structure for reaching suppression. Consistent with this, lesions in different nodes of this network result in different forms of motor deficits, such as Optic Ataxia in parietal patients, and commission errors in frontal ones.

Introduction

Aside from locomotion, reaching provides the basic foundation for the great majority of the actions of humans and monkeys. Frequently, however, a reach must be modified in some way either just before or during execution, as the reached for object moves or there are signs that it might be inappropriate to touch. Therefore reaching must be a flexible form of motor behavior that requires planning and on-line control in order to modify or suppress the original motor plan or the ongoing hand movement, when needed. This flexibility can be studied at different levels of analysis, such as its behavioral characteristics, anatomical substrates, neurophysiological mechanisms and the consequences of brain lesions in patients. In this review, which is concerned with the cortical systems involved, we present experimental evidence for common, modular elements that are shared by both direct, unperturbed reaching and reaching modified because of either sudden target shifts or the need to stop the movement. Findings from both macaques and humans will be discussed, and functional parallels will be drawn based on the similarity in the anatomical structures involved in cortical motor control between these species. Different theoretical models and ideas will be illustrated and contrasted. We will argue that the overall set of finding is compatible with a relatively simple functional and anatomical model.

Section snippets

The problem

The problem of reaching a target, whether stationary or jumping, can be described in a straightforward manner. We define the motor error as the vector underlying desired hand movement, that is, the vector difference between target location and hand location. A successful reach involves nulling the motor error vector or reducing it to within a tolerance window defined by the task. Accordingly, signals about the target and limb state must be translated into neural commands appropriate to drive

Cell-recordings in the monkey during on-line corrections

In spite of the wealth of information available on on-line control of movement from behavioral studies, only four cell-recording studies exist in the literature on the on-line control of hand movement trajectory (Archambault et al., 2009, Archambault et al., 2011, Dickey et al., 2013, Georgopoulos et al., 1983). They have been devoted to the analysis of the role of premotor, motor, and posterior parietal cortex. In the first three studies monkeys were trained in a Double-Step center-out task,

Reaching disorders and on-line fast movement corrections in Optic Ataxia

On-line automatic correction of a movement has been most studied from a neuropsychological perspective in Optic Ataxia (OA). Patients with OA have impairments in the visuomotor domain, especially when they are required to perform reaching and pointing movements to a target in the periphery (extrafoveal condition), although cases of foveal OA have been observed (e.g. Buxbaum and Coslett, 1998). Reaching errors in such patients can be independent of any primary motor, sensory, praxis or

Neurophysiological studies in animals

In animal models, most of the studies exploring neural modulations underlying inhibitory control of arm movements have so far used two main paradigms: the Go/No-Go task and the Stop (countermanding) task. Behaviorally, both paradigms give rise to commission errors. However, they explore two different aspects of the explicit suppression of a motor response. In the Go/No-Go paradigms it is a potential and not an ongoing movement that has to be halted. Instead only the Stop task allows one to

Conclusions

The literature reviewed in this paper provides converging evidence across a range of disciplines and procedures on the basic mechanisms involved in correcting a reach when it has to be changed in direction or inhibited with particular reference to the roles of the ventrolateral prefrontal, premotor, motor, and parietal cortices. Moreover, despite the apparent differences that exist between the monkey and the human in the organization of premotor and particularly the parietal cortex, it now

Acknowledgments

This work was partially supported by the MIUR of Italy (prot. 2010MEFNF7_004 to RC, and prot. 2008J7YFNR_004 to TS), by the Italian Space Agency (DCMC and CRUSOE grants to FL), and by the European Commission (FP7 Collaborative Research Project BRAINLEAP – ref. 306502 – to SF). We are grateful to Prof. Y. Rossetti for providing the material used in Fig. 4.

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    All authors contributed equally to this work.

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