Lori-Ann R. Sacrey

Similar hand shaping in reaching-for-food (skilled reaching) in rats and humans provides evidence of homology in release, collection, and manipulation movements.

Many animal species use their forelimbs to assist in eating, such as occurs in a reach-to-eat task (skilled reaching) in which a forelimb is extended to grasp food that is placed in the mouth for eating. It is unclear the extent to which the skilled reaching movements of different species share common ancestry and so are homologous or evolved independently and so are analogous (homoplasy). Here hand shaping (the movements of the hand and digits) that occur as the hand is transported to the target, were examined using high-speed (1000 frames/s) video recording and kinematic measurement (Peak Motus) in the rat (Rattus norvegicus) and human (Homo sapiens). Ten movement similarities were identified from the point that the limb initiated transport towards the food item to the point that the food was grasped. The digits were closed and semi-flexed as the hand was lifted (released from a substrate) and supinated. They closed further as the hand was collected for aiming. They then extended as the hand was transported to the target and then opened in conjunction with pronation to orient the hand for grasping (manipulation). Finally the digits were flexed and closed for grasping. These movements occurred at approximately the same point of limb transport in both species even though the rat used a whole paw grasp and the humans used a pincer grasp. Bushbabies (Galago garnettii), titi monkeys (Callicebus brunneus), rhesus monkeys (Macaca mulatta) and the bonobo (Pan paniscus) displayed similar hand shaping in skilled reaching despite species differences in grasping movements. Homologous hand shaping in the rodent clade and the primate clade and within the primate lineage is discussed in relation to its possible derivation from hand shaping movements associated with stepping.

The use of rodent skilled reaching as a translational model for investigating brain damage and disease

Neurological diseases, including Parkinsons disease, Huntingtons disease, and brain damage caused by stroke, cause severe motor impairments. Deficits in hand use are one of the most debilitating motor symptoms and include impairments in body posture, forelimb movements, and finger shaping for manipulating objects. Hand movements can be formally studied using reaching tasks, including the skilled reaching task, or reach-to-eat task. For skilled reaching, a subject reaches for a small food item, grasps it with the fingers, and places it in the mouth for eating. The human movement and its associated deficits can be modeled by experimental lesions to the same systems in rodents which in turn provide an avenue for investigating treatments of human impairments. Skilled reaching movements are scored using three methods: (1) end point measures of attempts and success, (2) biometric measures, and (3) movement element rating scales derived from formal descriptions of movement. The striking similarities between human and rodent reaching movements allow the analysis of the reach-to-eat movement to serve as a powerful tool to generalize preclinical research to clinical conditions.

Precocious hand use preference in reach-to-eat behavior versus manual construction in 1- to 5-year-old children

The variation in hand use as a function of task and developmental age poses a problem for understanding how and when handedness, preferred use of one hand, develops. The present cross-section study is the first to contrast hand preference use for the natural and frequently used reach-to-eat movement with a constructional task that requires a very similar reach-to-grasp movement. Thirty children between the ages of 1 and 3 years completed an eating task, in which they grasped small food items (Cheerios™ or Froot Loops™) that they brought to the mouth for eating. Thirty children between the ages of 3 and 5 years completed the construction task, in which they grasped LEGO® pieces to construct 3D models. Hand use preference for grasping in the eating and construction tasks was calculated by comparing the percentage of grasps made by the right hand and by the left hand. There were two main findings: First, right hand preference for grasping in the eating task is present as early as 1 year of age, whereas right hand preference for grasping in the construction task does not develop until 4 years of age. Second, right hand preference for grasping is greater in the eating than in the construction task. The results are discussed in relation to the idea that a consideration for task constraints (e.g., unimanual vs. bimanual; eating vs. construction; natural vs. praxic) should be incorporated into the experimental design when measuring hand use in children.

Hand shaping in the rat: Conserved release and collection vs. flexible manipulation in overground walking, ladder rung walking, cylinder exploration, and skilled reaching

Hand shaping in terrestrial mammals is adapted to many functions including walking, climbing, exploration, and skilled manipulation. Nevertheless, hand shaping is not well described in the rat (Rattus norvegicus) although the species is used to study the evolution of movement, the neural control of movement, and to model impairments that can result from brain injury. In the present study, rat hand movements were examined in standardized tests of overground walking, horizontal or inclined ladder rung walking, exploring a vertical wall of a cylinder, and skilled reaching for food. Behavior was filmed with high-speed (250-1000 f/s) video camera from which frame-by-frame behavioral and kinematic analyses (Peak Motus) were made. There were three hand actions common to all tasks. In release, the hand pushed off or was lifted from a substrate; in collection, the digits were closed and flexed though the midpoint of limb transport; and, in manipulation, the hand and digits were shaped to contact or grasp a target. The movements of release and collection, although variable in character, speed and duration, were very similar in the different tests. The movement of manipulation featured greater specialized digit use and varied sensory control (olfaction, vibrissae, and tactile senses) in different tasks. Conserved release and collection vs. the variability of manipulation is discussed in relation to the evolution, neural control, and neural commitment underlying hand movements.

Development of rotational movements, hand shaping, and accuracy in advance and withdrawal for the reach-to-eat movement in human infants aged 6–12 months

The reach-to-eat movement, transport of a hand to grasp an object that is withdrawn and placed in the mouth, is amongst the earliest developing functional movements of human infants. The present longitudinal study is the first description of the maturation of hand-rotation, hand shaping, and accuracy associated with the advance and withdrawal phases of the movement. Eight infants, aged 6-12 months, and eight adults, were video recorded as they reached for familiar objects or food items. Hand, arm, and trunk movements were assessed frame-by-frame with the Skilled Reaching Rating Scale, previously developed for the assessment of adult reaching, and supplementary kinematic analysis. Reach-to-eat maturation was characterized by three changes. First, for advance, a simple open hand transport gradually matured to a movement associated with pronation and hand shaping of the digits for precision grasping. Second, for withdrawal to the mouth, a direct withdrawal movement gradually became associated with hand supination that oriented the target object to the mouth. Third, associated with the maturation of rotational movements, inaccurate and fragmented hand transport and withdrawal movements developed into precise targeting of the hand-to-object and object-to-mouth. Across the age range, there was a decrease in bimanual reaching and an increase in right handed reaching. The results are discussed in relation to the idea that the maturation of the reach-to-eat movement involves the development of rotational and shaping movements of the hand and visual and somatosensory guidance of a preferred hand.

Visual Guidance for Hand Advance but Not Hand Withdrawal in a Reach-to-Eat Task in Adult Humans: Reaching Is a Composite Movement

Many animal species use reaching for food to place in the mouth (reach-to-eat) with a hand, and it may be a primitive movement. Although researchers (I. Q. Whishaw, 2005; A. N. Iwaniuk & I. Q. Whishaw, 2000; M. Gentiluci, I. Toni, S. Chieffi, & G. Pavesi, 1994) have described visual guidance of reaching in both normal and brain-injured human and nonhuman primates, researchers have not described the contribution of vision during advance of the limb to grasp food and during withdrawal of the limb with food to the mouth. To evaluate visual contributions, the authors monitored eye movements in young adults as they reached for food with and without vision. Participants visually engaged the target prior to the 1st hand movement and disengaged it as the food was grasped. Visual occlusion slowed limb advance and altered digit shaping but did not affect withdrawal. The dependence on visual control of advance but not withdrawal suggests that the reach-to-eat movement is a composite of 2 basic movements under visual and tactile/proprioceptive guidance, respectively.

Music Attenuates Excessive Visual Guidance of Skilled Reaching in Advanced but Not Mild Parkinson's Disease

Parkinsons disease (PD) results in movement and sensory impairments that can be reduced by familiar music. At present, it is unclear whether the beneficial effects of music are limited to lessening the bradykinesia of whole body movement or whether beneficial effects also extend to skilled movements of PD subjects. This question was addressed in the present study in which control and PD subjects were given a skilled reaching task that was performed with and without accompanying preferred musical pieces. Eye movements and limb use were monitored with biomechanical measures and limb movements were additionally assessed using a previously described movement element scoring system. Preferred musical pieces did not lessen limb and hand movement impairments as assessed with either the biomechanical measures or movement element scoring. Nevertheless, the PD patients with more severe motor symptoms as assessed by Hoehn and Yahr (HY) scores displayed enhanced visual engagement of the target and this impairment was reduced during trials performed in association with accompanying preferred musical pieces. The results are discussed in relation to the idea that preferred musical pieces, although not generally beneficial in lessening skilled reaching impairments, may normalize the balance between visual and proprioceptive guidance of skilled reaching.

Proximal movements compensate for distal forelimb movement impairments in a reach-to-eat task in Huntington's disease: new insights into motor impairments in a real-world skill.

Huntingtons disease (HD) causes severe motor impairments that are characterized by chorea, dystonia, and impaired fine motor control. The motor deficits include deficits in the control of the forelimb, but as yet there has been no comprehensive assessment of the impairments in arm, hand and digit movements as they are used in every-day tasks. The present study investigated the reaching of twelve HD subjects and twelve age-matched control subjects on a reach-to-eat task. The subjects were asked to reach for a small food item, with the left or the right hand, and then bring it to the mouth for eating. The task assesses the major features of skilled forelimb use, including orienting to a target, transport of the hand to a target, use of a precision grasp of the target, limb withdrawal to the mouth, and release of the food item into the mouth, and the integration of the movements into a smooth act. The movements were analyzed frame-by-frame by scoring the video record using an established movement element rating scale and by biometric analysis to describe limb trajectory. All HD subjects displayed greater reliance on more proximal movements in reaching. They also displayed overall jerkiness, a significant impairment in end point error correction (i.e. no smooth trajectories), deficits in timing and terminating motion (overshooting the target), impairments in rotation of the hand, abnormalities in grasping, and impairments in releasing the food item to the mouth. Although impairment in the control of the distal segments of the limb was common to all subjects, the intrusion of choreatic movements produced a pattern of highly variable performance between subjects. The quantification of reaching performance as measured by this analysis provides new insights into the impairments of HD subjects, allows an easily administered and inexpensive way to document the many skilled limb movement abnormalities, and relates the impairments to a real-world context. The protocol can serve as a useful clinical tool to evaluate innovative therapeutic interventions in HD such as physiotherapy, drug therapy, or functional neurosurgical procedures.

Hand shaping using hapsis resembles visually guided hand shaping

The reach-to-grasp movement is composed of a number of movement elements including hand transport, hand shaping, and grasping. These movement elements are featured in grasping when it is guided by vision, when it is guided by haptic input from the non-reaching hand or other body parts, and when it is guided by off-line perceptual (remembered) knowledge. An unanswered question is how is the reach-to-grasp movement achieved when all information about the target must be acquired by the grasping hand? The answer to this question was obtained by asking participants to reach for three randomly presented food items that varied in size: an orange slice, a small round donut ball, or a blueberry. In order to constrain the grasping pattern, participants were asked to pick up an item with the intention of placing it in the mouth. Thus, in the unsighted condition, participants did not know which item they were reaching for until they made haptic contact with it. Hand transport, shaping, and grasping were examined using frame-by-frame video analysis and linear kinematics. These measures showed that in unsighted reaching, hand transport first served to establish haptic contact between either the second or third digit and the target. After haptic identification of the target, the hand and/or grasping digits adjusted their trajectory, reshaped, and reoriented for grasping. A comparison of haptically guided grasping and visually guided grasping indicated that the two were very similar. This similarity is discussed in relation to contemporary ideas concerning the neural mechanisms that guide hand use.

Drug treatment and familiar music aids an attention shift from vision to somatosensation in Parkinson's disease on the reach-to-eat task

Sensory control of the natural skilled movement of reaching for a food target to eat (reach-to-eat) is closely coupled to the successive phases of the movement. Control subjects visually fixate the target from hand movement onset to the point that the digits contact the food, at which point they look away. This relationship between sensory attention and limb movement suggests that whereas limb advance is under visual control, grasping, limb withdrawal, and releasing the food to the mouth is guided by somatosensation. The pattern of sensory control is altered in Parkinsons disease (PD). PD subjects may visually fixate the target for longer durations prior to movement initiation, during the grasp, and during the initial portion of hand withdrawal suggesting that vision compensates for a somatosensory impairment. Because both medication and listening to favorite musical pieces have been reported to normalize some movements in subjects with PD, the present study compared the effect of medication and listening to preferred musical pieces on sensory attention shifts from vision to somatosensation during the reach-to-eat movement. Biometric measures of eye movement and the movement of the reaching limb were collected from PD subjects and aged-matched control subjects in four conditions in their own homes: off medication, off medication with music, on medication, and on medication with music. Unmedicated PD subjects were slower to visually disengage the target after grasping it. Their disengage latency was shortened by both music and medication. Medication and music did not improve other aspects of reaching, including reaching duration and the ratings of the movement elements of limb advance, grasping, and limb withdrawal. The results are discussed in relation to the idea that one way in which medication and music may aid movement in PD by normalizing somatosensory control of forelimb movement thus reducing compensatory visual monitoring.