Jenni M. Karl

Different evolutionary origins for the Reach and the Grasp: an explanation for dual visuomotor channels in primate parietofrontal cortex

The Dual Visuomotor Channel Theory proposes that manual prehension consists of two temporally integrated movements, each subserved by distinct visuomotor pathways in occipitoparietofrontal cortex. The Reach is mediated by a dorsomedial pathway and transports the hand in relation to the target’s extrinsic properties (i.e., location and orientation). The Grasp is mediated by a dorsolateral pathway and opens, preshapes, and closes the hand in relation to the target’s intrinsic properties (i.e., size and shape). Here, neuropsychological, developmental, and comparative evidence is reviewed to show that the Reach and the Grasp have different evolutionary origins. First, the removal or degradation of vision causes prehension to decompose into its constituent Reach and Grasp components, which are then executed in sequence or isolation. Similar decomposition occurs in optic ataxic patients following cortical injury to the Reach and the Grasp pathways and after corticospinal tract lesions in non-human primates. Second, early non-visual PreReach and PreGrasp movements develop into mature Reach and Grasp movements but are only integrated under visual control after a prolonged developmental period. Third, comparative studies reveal many similarities between stepping movements and the Reach and between food handling movements and the Grasp, suggesting that the Reach and the Grasp are derived from different evolutionary antecedents. The evidence is discussed in relation to the ideas that dual visuomotor channels in primate parietofrontal cortex emerged as a result of distinct evolutionary origins for the Reach and the Grasp; that foveated vision in primates serves to integrate the Reach and the Grasp into a single prehensile act; and, that flexible recombination of discrete Reach and Grasp movements under various forms of sensory and cognitive control can produce adaptive behavior.

Recovery of skilled reaching following motor cortex stroke : do residual corticofugal fibers mediate compensatory recovery

Motor cortex (MC) injury impairs skilled reaching in rats, but success scores are eventually restored to approximate preoperative levels. The improvement is attributed to compensatory strategies, such as substituting trunk rotations for the chronically lost rotatory movement of the forelimb, that occur during transport and withdrawal. The present study examined the contributions of the rostral motor cortex (RMC) and the caudal motor cortex (CMC) to skilled reaching performance. The study also examined the role of the ipsilateral and the contralateral hemispheres in supporting the spontaneous recovery. Rats were trained to reach for single food pellets, and their recovery from partial or complete MC injury was documented with quantitative scores and movement element measures in three experiments: (1) devascularization of the CMC, or the RMC, or both, in the hemisphere contralateral to the reaching paw; (2) additional lesions to the CMC and RMC injuries such that the conjoint damage amounted to an MC lesion; and (3) MC lesion followed by damage in the neocortex lateral to the injury or in the opposite MC. The results showed that the CMC made the main contribution to skilled reaching performance, and that there was a lesser contribution by the RMC. MC damage was exacerbated by additional damage to the ipsilateral neocortex as compared to the contralateral neocortex. The results are discussed in relation to the idea that the involvement of the neocortical areas in skilled reaching performance and its recovery is proportional to the region from which corticospinal projections originate.

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.

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.

Thinning, movement, and volume loss of residual cortical tissue occurs after stroke in the adult rat as identified by histological and magnetic resonance imaging analysis

Plasticity of residual cortical tissue has been identified as an important mediator of functional post-stroke recovery. Many studies have been directed toward describing biochemical, electrophysiological, and cytoarchitectural changes in residual cortex and correlating them with functional changes. Additionally, after neonatal stroke the thickness of residual tissue can change, the tissue can move, and tissue can fill in the stroke core. The purpose of the present study was to systematically investigate and document possible gross morphological changes in peri-infarct tissue after forelimb motor cortex stroke in the adult rat. Rats received a unilateral forelimb motor cortex stroke of equivalent size by pial strip devascularization or photothrombotic occlusion and were then examined using histology or magnetic resonance imaging (MRI) at 1 h, 1, 3, 7, 14, or 31 days post-stroke. Middle cerebral artery occlusion was used as a control stroke procedure. Decreases in cortical thickness, volume, and neural density were found to extend far beyond the stroke infarct and included most of the sensorimotor regions of the stroke and intact hemispheres. Movement of residual tissue towards the infarct was observed and confirmed using anatomical markers placed in intact cortical tissue at the time of stroke induction. The results are discussed in relation to the idea that extensive time-dependent morphological changes that occur in residual tissue must be considered when evaluating plasticity-related cortical changes associated with post-stroke recovery of function.

Nonvisual learning of intrinsic object properties in a reaching task dissociates grasp from reach

The Dual Visuomotor Channel theory proposes that skilled reaching is composed of a Reach that directs the hand in relation to the extrinsic properties of an object (e.g., location) and a Grasp that opens and closes the hand in relation to the intrinsic properties of an object (e.g., size). While Reach and Grasp movements are often guided by vision, they can also be performed without vision when reaching for a body part or an object on one’s own body. Memory of a recently touched but unseen object can also be used to guide Reach and Grasp movements although the touch-response memory durations described are extremely brief (Karl et al. in Exp Brain Res 219:59–74, 2012a). The purpose of the present study was to determine whether repeated nonvisual reaching for a consistent object could calibrate Reach and Grasp movements in a way similar to those guided by vision. The nonvision group wore vision-occluding goggles and reached for fifty consecutive trials for a round donut ball placed on a pedestal. The control group performed the same task with vision. Frame-by-frame video analysis and linear kinematics revealed that nonvision participants consistently used an elevated Reach trajectory, in which the hand, rather than being directed toward the target in the horizontal plane, was first elevated above the target before being lowered to touch and locate it. First contact was established with the dorsal surface of the target, and thus, adjustments in contact locations were often required for purchase. Although nonvision participants initially used an open and extended hand during transport, with practice they began to scale digit aperture to object size with an accuracy and temporal relation similar to vision participants. The different ways in which the Reach and Grasp movements respond to nonvisual learning are discussed in relation to support for the dual channel theory of reaching and to the idea that the Reach and Grasp channels may be differentially dependent on online visual guidance.

Intact intracortical microstimulation (ICMS) representations of rostral and caudal forelimb areas in rats with quinolinic acid lesions of the medial or lateral caudate-putamen in an animal model of Huntington's disease.

Neurotoxic, cell-specific lesions of the rat caudate-putamen (CPu) have been proposed as a model of human Huntingtons disease and as such impair performance on many motor tasks, including skilled forelimbs tasks such as reaching for food. Because the CPu and motor cortex share reciprocal connections, it has been proposed that the motor deficits are due in part to a secondary disruption of motor cortex. The purpose of the present study was to examine the functionality of the motor cortex using intracortical microstimulation (ICMS) following neurotoxic lesions of the CPu. ICMS maps have been shown to be sensitive indicators of motor skill, cortical injury, learning, and experience. Long-evans hooded rats received a sham, a medial, or a lateral CPu lesion using the neurotoxin, quinolinic acid (2,3-pyridinedicarboxylic acid). Two weeks later the motor cortex was stimulated under light ketamine anesthesia. Neither lateral nor medial lesions of the CPu altered the stimulation threshold for eliciting forelimb movements, the type of movements elicited, or the size of the rostral forelimb (RFA) and caudal forelimb areas (CFA) from which movements were elicited. The preservation of ICMS forelimb movement representations (the forelimb map) in rats with cell-specific CPu lesions suggests motor impairments following lesions of the lateral striatum are not due to the disruption of the motor map. Therefore, the impairments that follow striatal cell loss are due either to alterations in circuitry that is independent of motor cortex or to alterations in circuitry afferent to the motor cortex projections.

The functional origins of speech-related hand gestures.

Many theories of language posit its recent evolution, perhaps contemporaneous with the evolution of Homo sapiens. The embodied language theory, however, in proposing that language includes gestures, provides an avenue for tracing language origins to phylogenetically earlier ancestral species. Here, evidence is presented that the structure of functional hand movements (e.g., reaching for food, climbing a ladder, or crawling), in rats and humans is similar. The structure of these functional hand movements is then compared to speech-related hand gestures in humans. The sequence of language-related gestures are also found to be characteristic of functional hand movements. It is suggested that these findings show that the arm and hand gestures that accompany human speech are derived from the same neural substrates that produce functional movements. Additionally, evidence is reviewed that supports the idea that speech-related gestures resemble the movements elicited by long-train stimulation of the primate motor cortex. Together, this evidence suggests that speech-related hand gestures have their evolutionary origins in functional hand movements of ancestral non-primate and primate species and may be constrained by the neural substrate for those movements. These findings are further discussed in relation to the idea that speech-related gestures reflect forelimb motor cortex contributions to embodied language.

Independent development of the Reach and the Grasp in spontaneous self-touching by human infants in the first 6 months

The Dual Visuomotor Channel Theory proposes that visually guided reaching is a composite of two movements, a Reach that advances the hand to contact the target and a Grasp that shapes the digits for target purchase. The theory is supported by biometric analyses of adult reaching, evolutionary contrasts, and differential developmental patterns for the Reach and the Grasp in visually guided reaching in human infants. The present ethological study asked whether there is evidence for a dissociated development for the Reach and the Grasp in nonvisual hand use in very early infancy. The study documents a rich array of spontaneous self-touching behavior in infants during the first 6 months of life and subjected the Reach movements to an analysis in relation to body target, contact type, and Grasp. Video recordings were made of resting alert infants biweekly from birth to 6 months. In younger infants, self-touching targets included the head and trunk. As infants aged, targets became more caudal and included the hips, then legs, and eventually the feet. In younger infants hand contact was mainly made with the dorsum of the hand, but as infants aged, contacts included palmar contacts and eventually grasp and manipulation contacts with the body and clothes. The relative incidence of caudal contacts and palmar contacts increased concurrently and were significantly correlated throughout the period of study. Developmental increases in self-grasping contacts occurred a few weeks after the increase in caudal and palmar contacts. The behavioral and temporal pattern of these spontaneous self-touching movements suggest that the Reach, in which the hand extends to make a palmar self-contact, and the Grasp, in which the digits close and make manipulatory movements, have partially independent developmental profiles. The results additionally suggest that self-touching behavior is an important developmental phase that allows the coordination of the Reach and the Grasp prior to and concurrent with their use under visual guidance.

Reach and Grasp reconfigurations reveal that proprioception assists reaching and hapsis assists grasping in peripheral vision.

Abstract The dual visuomotor channel theory proposes that prehension consists of a Reach that transports the hand in relation to an object’s extrinsic properties (e.g., location) and a Grasp that shapes the hand to an object’s intrinsic properties (e.g., size and shape). In central vision, the Reach and the Grasp are integrated but when an object cannot be seen, the movements can decompose with the Reach first used to locate the object and the Grasp postponed until it is assisted by touch. Reaching for an object in a peripheral visual field is an everyday act, and although it is reported that there are changes in Grasp aperture with target eccentricity, it is not known whether the configuration of the Reach and the Grasp also changes. The present study examined this question by asking participants to reach for food items at 0° or 22.5° and 45° from central gaze. Participants made 15 reaches for a larger round donut ball and a smaller blueberry, and hand movements were analyzed using frame-by-frame video inspection and linear kinematics. Perception of targets was degraded as participants could not identify objects in peripheral vision but did recognize their differential size. The Reach to peripheral targets featured a more dorsal trajectory, a more open hand, and less accurate digit placement. The Grasp featured hand adjustments or target manipulations after contact, which were associated with a prolonged Grasp duration. Thus, Grasps to peripheral vision did not consist only of a simple modification of visually guided reaching but included the addition of somatosensory assistance. The kinematic and behavioral changes argue that proprioception assists the Reach and touch assists the Grasp in peripheral vision, supporting the idea that Reach and Grasp movements are used flexibly in relation to sensory guidance depending upon the salience of target properties.