ReviewCorrection and suppression of reaching movements in the cerebral cortex: Physiological and neuropsychological aspects
Graphical abstract
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.
References (203)
- et al.
The accuracy of aiming at a target. Some further evidence for a theory of intermittent control
Acta Psychol.
(1972) - et al.
A hand and a field effect in on-line motor control in unilateral optic ataxia
Cortex
(2008) - et al.
Parietal modules for reaching
Neuropsychologia
(2009) - et al.
Reaching a moveable visual target: dissociations in brain tumour patients
Brain Cogn.
(2013) - et al.
Dynamics of saccade target selection: race model analysis of double step and search step saccade production in human and macaque
Vision Res.
(2007) - et al.
Cognitive constraint on the ‘automatic pilot’ for the hand: movement intention influences the hand's susceptibility to involuntary on-line corrections
Conscious Cogn.
(2009) - et al.
Probabilistic fibre tract analysis of cytoarchitectonically defined human inferior parietal lobule areas reveals similarities to macaques
Neuroimage
(2011) - et al.
Control of prepotent responses by the superior medial frontal cortex
Neuroimage
(2009) - et al.
Neural correlates of reaching decisions in dorsal premotor cortex: specification of multiple direction choices and final selection of action
Neuron
(2005) - et al.
Immunocytochemical evidence for glutamatergic cortico-cortical connections in monkey
Brain Res.
(1988)
Action control in visual neglect
Neuropsychologia
Have we been asking the right questions when assessing response inhibition in go/no-go tasks with fMRI? A meta-analysis and critical review
Neurosci. Biobehav. Rev.
Response selection deficits in frontal excisions
Neuropsychologia
Primate models of movement disorders of basal ganglia origin
Trends Neurosci.
Forward modeling allows feedback control for fast reaching movements
Trends Cogn. Sci.
Go-no go learning after frontal lobe lesions in humans
Cortex
Muscular synergies during motor corrections: investigation of the latencies of muscle activities
Behav. Brain Res.
Computational mechanisms of sensorimotor control
Neuron
Saccade control and eye–hand coordination in optic ataxia
Neuropsychologia
Divided and focused attention in patients with lesion of the prefrontal cortex
Brain Cogn.
Implicit online corrections of reaching movements
Curr. Opin. Neurobiol.
A lesion of the posterior parietal cortex disrupts on-line adjustments during aiming movements
Neuropsychologia
The role of the right inferior frontal gyrus: inhibition and attentional control
Neuroimage
Inactivation of the Parietal Reach Region causes optic ataxia, impairing reaches but not saccades
Neuron
Internal models for motor control and trajectory planning
Curr. Opin. Neurobiol.
Corticospinal neurons in macaque ventral premotor cortex with mirror properties: a potential mechanism for action suppression?
Neuron
The distinct modes of vision offered by feedforward and recurrent processing
Trends Neurosci.
Corticocortical and thalamocortical responses of neurons in the monkey primary motor cortex and their relation to a trained motor task
J. Neurophysiol.
Sublayer-specific microcircuits of corticospinal and corticostriatal neurons in motor cortex
Nat. Neurosci.
Cortical mechanisms for on-line control of hand movement trajectory: the role of the posterior parietal cortex
Cereb. Cortex
On-line control of hand trajectory and evolution of motor intention in the parietofrontal system
J. Neurosci.
Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans
Nat. Neurosci.
Cortical and subcortical contributions to stop signal response inhibition: role of the subthalamic nucleus
J. Neurosci.
Statistical analysis of the parieto-frontal cognitive-motor network
J. Neurophysiol.
Deafferentation and pointing with visual double-step perturbations
Exp. Brain Res.
ADHD and the Nature of Self-control
Multiple levels of representation of reaching in the parieto-frontal network
Cereb. Cortex
Temporal evolution and strength of neural activity in parietal cortex during eye and hand movements
Cereb. Cortex
Impairment of on-line control of hand and eye movements in a monkey model of optic ataxia
Cereb. Cortex
Anticipation of moving stimuli by the retina
Nature
Salience network integrity predicts default mode network function after traumatic brain injury
Proc. Natl. Acad. Sci. U.S.A.
Inhibitory control in mind and brain: an interactive race model of countermanding saccades
Psychol. Rev.
Fast responses of the human hand to changes in target position
J. Mot. Behav.
Neural dynamics of planned arm movements: emergent invariants and speed-accuracy properties during trajectory formation
Psychol. Rev.
Effect of transcranial magnetic stimulation (TMS) on parietal and premotor cortex during planning of reaching movements
PLoS ONE
Spatio-motor representations in reading: evidence for subtypes of optic ataxia
Cogn. Neuropsychol.
The sources of visual information to the primate frontal lobe: a novel role for the superior parietal lobule
Cereb. Cortex
Evolution amplified processing with temporally-dispersed, slow, neural connectivity in primates
Proc. Natl. Acad. Sci. U.S.A.
Dissociable mechanisms of cognitive control in prefrontal and premotor cortex
J. Neurophysiol.
Executive brake failure following deactivation of human frontal lobe
J. Cogn. Neurosci.
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All authors contributed equally to this work.