Summary

This chapter reviews impairments of grasping and other fine motor tasks following disorders of the somatosensory system. The first part reports findings from transient anesthesia induced experimentally in healthy human subjects. The second part summarizes studies on the effects of lesions to the peripheral sensory system. Findings in patients with sensory deficits following polyneuropathy or carpal tunnel syndrome are differentiated from chronic complete somatosensory deafferentation. The latter group of very rare subjects provides the unique possibility of investigating the function of the motor system deprived of sensory input. The last part summarizes the effects of central lesions due to stroke or cerebral palsy that frequently affect the somatosensory system. The results for various motor tasks including prehensile movements are reported. Specific emphasis is placed on analyses of grip-force control during object manipulation since somatosensory feedback is particularly important for these activities and ample research has been performed during the last few years, enabling comparisons between patient groups.

Introduction

Clarifying the role of sensory information in the control of voluntary movement and force production is one of the most essential questions in sensorimotor research. The most obvious way to investigate this question is to study the effects of damage to the sensory system on movement execution. Indeed, there was controversy about the effects of a complete lack of sensory information at the beginning of the 20th century.

Summary

Grasping behavior has been well studied in both human and non-human primates. Studies have revealed a classic grasping circuit that involves several regions, such as the motor, prefrontal and parietal cortices. However, the functional contribution of the basal ganglia to grasping control is often overlooked. This is surprising because many basal ganglia disorders (e.g. Parkinson's disease) have been experimentally associated with deficits in grasping control. Recent work in our laboratory used fMRI to demonstrate that the caudate, putamen, internal and external segments of the globus pallidus (GPi and GPe, respectively), and subthalamic nucleus (STN) participate in circuits that independently regulate the selection and scaling of parameters important for grasping. These findings provide new evidence that grasping must be considered as a behavior that is processed in both cortical and subcortical structures.

Introduction

Prehension remains one of the most important functions of primate motor systems. The remarkable adaptability and effortlessness with which primates can reach for and grasp objects of variable size, shape and mass has had unequivocal evolutionary importance. Nevertheless, it is widely accepted that even simple reach-to-grasp movements pose considerable challenges for the primate sensorimotor system (Johnson-Frey, 2003). During the prehension of a given object, individuals must use visual (i.e. object distance, direction) and somatosensory information (i.e. joint angle) to transport the hand to the object location via a precisely aimed reaching movement.

Summary

This chapter offers an overview of the most recent techniques for recording of cortical activity in the awake, behaving monkey. We review the different types of signals that can be extracted from extracellular cortical recordings made with microelectrodes. We also discuss how these signals can be related to dexterous hand movements. This leads us to consider the functional organization of the motor cortex for the control of the distal muscles during grasp.

Introduction

The unique ability of human and non-human primates to interact with their environment is dependent upon the skilled use of the hands for grasping and manipulation of objects. The grasping of objects requires continuous interaction between the sensory processing of the object's physical properties and the motor mechanisms controlling the shape of the hand and the positioning of the hand and digits upon the object. Over the past 30 years, intracortical extracellular recording techniques in the awake monkey have been an essential tool to investigate the organization of the cortical circuits involved in the control of grasp. It has been shown that multiple areas in the parietal and frontal lobes contribute to the transformation from sensory inputs to motor outputs for efficient grasp. This cortical network influences the spinal circuitry that controls the distal hand and digit muscles. Part of this corticospinal control is mediated by direct cortico-motoneuronal (CM) projections from the primary motor cortex (M1) onto motoneurons innervating hand muscles.

Summary

It is widely held that schizophrenia is associated with a variety of subtle sensory and motor impairments – so called neurological soft signs – that may impact on manual dexterity. Neurological soft signs (NSS) in schizophrenia appear to be part of the underlying disorder. The motor deficit of the hand, however, may also worsen as a side effect of antipsychotic treatment. Within the theoretical framework of internal models schizophrenia has been associated with a deficit of self-monitoring and awareness of action. Deficient monitoring of the sensory consequences of voluntary movement may be directly related to the motor deficit to be found in schizophrenia. This chapter summarizes kinetic and kinematic aspects of impaired manual dexterity in schizophrenia and discusses the motor disability within the context of internal models for the sensorimotor processing of voluntary actions.

Introduction

Early in the 20th century, Bleuler (1908) and Kraepelin (1919) described several motor abnormalities in schizophrenia, such as problems in the sequencing and spacing of steps when walking and dyscoordination of hand and arm movements when performing handiwork and crafts. In this era antipsychotic drugs did not exist and, consequently, these early clinical observations cannot simply be considered a side effect of antipsychotic treatment. Today, deficits of fine motor performance, also referred to as neurological soft signs (NSS), are still observed in a substantial proportion of schizophrenic subjects, but their nature is still not completely understood and their semiology is not easily distinguishable from side effects of antipsychotic treatment.

Summary

Precise control of grasping when manipulating objects depends on intact function of the cerebellum. Given its stereotyped cytoarchitecture, the widespread connections with cortical and subcortical sensorimotor structures and the neural activity of cerebellar Purkinje cells during sensorimotor tasks, the cerebellum is considered to play a major role in the establishment and maintenance of sensorimotor representations related to grasping. Such representations are necessary to predict the consequences of movements. This chapter summarizes anatomical and theoretical aspects, electrophysiological and behavioral data characterizing the cerebellum, a key player in the processing of healthy grasping and in its dysfunction.

The anatomy of the cerebellum and its relation to the control of grasping

The cerebellum has attracted the attention of theorists and modelers for many years. The attraction is that the regular cytoarchitecture of the cerebellar cortex, with only one output cell and four main classes of interneurons, and the functional cerebellar circuitry have been very well documented (Wolpert et al., 1998). The circuitry of the cerebellum is unique by its stereotyped geometric arrangement and its modular organization, highly reminiscent of a machinery designed to process neuronal information in a unique manner (Ito, 2006). The cerebellum appears highly foliated, and this foliation is the reason for subdivision into smaller units (Larouche & Hawkes, 2006). From a structural standpoint, the cerebellum is made of pairs of nuclei embedded in white matter and surrounded by a mantle of cortex (Colin et al., 2002).

The numerous skeletal and muscular degrees of freedom of the hand provide the human with an enormous dexterity that has not yet been achieved by any other species on earth. The human hand can take on a huge variety of shapes and functions, providing its owner with a powerful hammer at one time or a delicate pair of forceps at another. The universal utility of the hand is even more enhanced by the ability to amplify the function of the hand by using tools. True opposition between the thumb and index finger is only observed in humans, the great apes and Old World monkeys. The human thumb is much longer, relative to the index finger, than the thumb of other primates and this allows humans to grasp and manipulate objects between the tips of the thumb and index finger. Humans have more individuated muscles and tendons with which to control the digits and have evolved extensive cortical systems for controlling the hand. In addition to its manipulative function the hand is a highly sensitive perceptive organ, orchestrated by myriads of tactile and somatosensory receptors, which enables humans to perceive the world within their reach. Taken together all these phylogenetic developments have provided humans with the ability to interact with each other, make love and war, and also to shape the world.

Summary

The last 10 years have seen major advances in the functional magnetic resonance imaging (fMRI) of the brain's role in grasping. A number of technical problems related to artefacts produced by arm movements and the registration of movements and fingertip forces have been solved. Reproducible activation of key areas involved in grasping, such as the ventral premotor cortex and the anterior part of the intraparietal sulcus, has been reported. More than that, fMRI seems to be capable of detecting biologically relevant activity in all the cortical and subcortical structures involved in the control of reaching, grasping and manipulation. Importantly, imaging has also been able to identify how activity in these areas supports key sensorimotor control mechanisms used in human dexterous manipulation. In particular, the anticipatory and reactive control of grip forces during object manipulation has been associated with specific neuronal responses in motor, parietal and cerebellar areas. Particularly interesting new lines of research include the use of effective connectivity analyses to characterize the neural interactions between the nodes in the frontoparietal circuits, and the combination of computational neuroscience approaches and functional imaging.

Functional magnetic resonance imaging is one of the most important techniques available to cognitive neuroscientists. It is a non-invasive, relatively inexpensive, whole-brain imaging modality that can be used to investigate the brain basis of perception, action and cognition with an anatomical resolution of 2–3 mm. In this chapter we will describe the contribution of this method to the understanding of human grasping and object manipulation.

Summary

A satisfactory description of human hand movements during the action of grasping was not available until the early 1980s. Kinematic parameters extracted from the displacements of anatomical landmarks located on the hand were used to differentiate between a transport component carrying the hand at the target location and a grasp component shaping the finger according to the object shape and size. These parameters, including the maximum grip aperture (MGA) are now currently adopted for testing vision for action in normal subjects, including in children at different stages of their visuomotor development, and in a wide range of pathological disorders affecting goal-directed movements.

Introduction: hand grasping movements before 1980

The hand is both a sensory and a motor organ. On the sensory side, in Sherrington's terms, it is the fovea of the somesthetic system, to the same extent as the center of the retina is the fovea of the visual system. The hand explores the haptic world by touching, grasping and manipulating objects in the same way as eye movements explore the visual world by displacing the retina between fixation points. The sensory and motor functions of the hand are complementary with one another. The movements of the fingers contribute to the exploration and perception of object shape and texture during manipulation and conversely sensory cues arising from the skin receptors contribute to the control of hand movements.

Summary

Aging-related decline in hand function is ubiquitous and inexorable, beginning at about age 60 years. This decline disproportionately impacts dexterous grasp and manipulation. Many potential explanations for this decline have been offered, but the causes remain poorly understood. Here we report observations from our laboratory on timed tasks demonstrating that the forces and kinematics of dexterous grasp and manipulation in old adults differ from young adults, even at “comfortable” performance speeds. These observations support recent suggestions that controlling the moments of force applied to grasped objects is a fundamental problem in old age. Possible explanations lead to a review of contemporary issues related to the sensorimotor control of the aging hand. These topics include: sensory deterioration (both peripheral and central); reduced ability to coordinate muscle forces to control force vectors at the fingertip of a single digit and across digits; increased moment-to-moment force fluctuations; and loss of independent control of the right and left hands. On an optimistic note, training and practice appears to slow or reverse declining hand function in healthy aging.

Introduction

Hand function deteriorates unequivocally in healthy aging. Well-known decreases in muscle strength, mostly from sarcopenia (Holloszy, 1995; Hughes et al., 2001; Doherty, 2003), can account for increased difficulty in accomplishing some daily living skills, such as opening containers (Sperling, 1960; Shiffman, 1992). Manual dexterity also declines in old age, but in a manner that is dissociated from decreasing muscle strength.

Summary

Focal hand dystonia (FHD) is a disabling movement disorder. Affected patients show abnormal patterns of muscle activity of the forearm and hand while performing a specific task. This includes co-contractions of agonist and antagonist muscles and overflow of motor activity to muscles that are normally not involved in a given movement. Patients with writer's or musician's cramp may present with dystonic symptoms that only occur during a selective task (referred to as “simple” writer's cramp or musician's cramp) or may develop symptoms with multiple tasks (referred to as “dystonic” writer's or musician's cramp). Neurophysiological and neuroimaging studies in humans have identified several mechanisms that may be relevant to the pathophysiology of FDH. These mechanisms include impaired sensorimotor integration, maladaptive plasticity and deficient inhibition at various levels in the sensorimotor system. This work has been complemented by the successful establishment of a primate model in which excessive training of skilled finger movements induced a dystonia-like phenotype. Based on these lines of research, novel non-pharmacological interventions have been developed to improve dystonia in patients with FDH. In this chapter, we give an update on the range of therapeutic approaches that have been proposed for FDH.

Clinical presentation of focal hand dystonia

Task-specific dystonia of the hand often develops in individuals whose work involves skilled repetitive movements, requiring a high level of performance (Byl & Melnick, 1997; Frucht, 2004). In some patients, dystonia may show a progression and they may develop dystonia with other less specific motor actions of the involved limb.