How humans control their prehension movements?

자료: http://www.gaitech.net/How%20humans%20control%20their%20prehension%20movements.pdf

By Yue Leng, Research Centre for Learning Science, Southeast University

Abstracts: 

Prehension is traditionally described as consisting of two components that are based

on different visual information. The transport component is directed by the extrinsic

properties of visual information; while the grasp component is guided by the

intrinsic properties of visual information. The visual information transports in the

dorsomedial visual stream through the parieto-occipital cortex to reach the frontal cortex. This

analysis of the prehension is named as the visuo-motor channel hypothesis. However,

an alternative description, called the digit channel hypothesis by some researchers,

which consists of determining suitable positions on the object------ on the basis of its

shape, surface roughness, and so on------ and then moving one’s thumb and fingers

more or less independently to these positions. This new view can make up the

disadvantage of traditional view from kinematics, anatomy and brain mechanism aspects.

Key words: prehension, transport component, grasp component, dorsal visual stream, the

digit channel hypothesis

Introduction

Prehension is an elegant and skilled object-directed behavior, which is defined as reaching out to

grasp an object. In the past 25 years, much research has been carried out on the cognitive theory of reaching-to-grasp; however, how humans administrate prehension movements is still under debate. This review will propose several hypotheses on the prehension movement that have been supported by reasonable evidence.

The visuo-motor channel hypothesis

Relation between anatomy and prehension

Early on, in 1981, Jeannerod [9] suggested that prehension is considered to consist of the control

of two components: the “transport” component or “reach” component, the movement of the hand to an appropriate location for gripping the object by moving the shoulder and elbow by

activation of proximal muscles; the “grasp” component or “manipulation” component, the

opening and closing of the aperture between the fingers as they prepare to grip the target by

activation of distal connection.

Relation between visual information and prehension

In reaching to grasp an object in space, visual information is required to specify both the

extrinsic and intrinsic properties of the object [10]. The term “extrinsic” information refers to

properties such as distance and orientation in environment, whereas the term “intrinsic”

information refers to properties which belong to object itself, such as object’s size, shape, color,

surface curve and possibly weight,. It was proved that the division between extrinsic and intrinsic information is useful for its correspondence with the division between the relatively independent, although temporally coupled, components of a prehension: the transport component and the grasp component [10, 21]. In detail, extrinsic properties are required to transport the hand in the correct orientation, in a particular direction and for a particular distance; however, intrinsic properties are necessary to control the grip aperture and to select the most appropriate grasp points [9]. Consequently, visual information about the properties of the object and its location is essential to program the required movements of the arm and hand [17]. 

Formulation of the visuo-motor channel hypothesis

Jeannerod postulated transport and grasp component are controlled by two independent

visuo-motor channels in parallel without sharing information, a change of object location should

affect only the transport phase, and a change in object size of shape only the manipulation phase.

This hypothesis is known as the visuo-motor channel hypothesis. This “classical approach” has

allowed paramount development in the research in prehension. The main reason for finding this

description so attractive is that the two channels correspond nicely to two distinct anatomical

structures and to two distinct types of visual information.

Based on this classical approach, Hoff and Arbib (1993) established a model controlling the

transport and grasp components on the basis of a minimum-jerk approach which developed by

Flash and Hogan (1985), combined with on-line feedback controllers. They proposed that a

“pre-shape controller” determines the grasp component in conjunction with a “hand-closure

controller”.

Concerning the hand pre-shaping, Supuk, Kodek and Bajd recently developed a new method for

evaluating hand pre-shaping during reaching-to-grasp movement, which makes use of all five

fingers in estimation of prehension. The experiment was performed on six healthy subjects

grasping three different objects at various positions and orientations. They found new parameters for the evaluation of finger preshaping, such as pentagon surface area, angle between the pentagon and hand normal vectors, and the angle between the pentagon and object normal vectors. The proposed pentagon approach is more informative than hand aperture used in previous studies, since it involves all five fingers [6].

Temporal coordination of the two components

The execution of the hand to reach and grasp an object is examined by means of various

prehension indices. The transport component is assessed by the wrist velocity profiles, typical

measurements include peak velocity, time to peak velocity, total time, etc. The grasp component

is measured by the maximum grip aperture and time to maximum grip aperture.

The use of objects of different size, shape, and axis orientation requiring different types of

prehension is a common strategy for the study of grasping. Almost, prehension movements were

recorded using the OPTOTRAK 3D system, which is a non-contact motion measurement system

tracks small infrared (IRED) markers that are attached to a subject or object. The main

outstanding features of this system are true real-time 3D/6D data rates (in excess of 2500

markers/second) as well as high accuracy. Researchers use this system extensively to collect data describing hand/arm movements in three spaces. Here we will present several typical

experiments as followed.

Jeannerod showed that the velocity of the transport component (as measured by wrist velocity)

has a bell-shaped profile. During movement, the grasp component (as measured by grip aperture between the index finger and thumb in a precision grip task) reaches maximum grasp aperture (MGA) approximately two-thirds of the way through the duration of the reaching movement. Wrist velocity and grip aperture are temporally coupled as the hand moves toward the goal object.

Furthermore, Timmann, Stelmach and Bloedel (1996) designated subjects started with a normal

finger posture but were required to briefly open and close their thumb and index finger while

transporting the wrist to grasp the object. The changes in the aperture altered most of the

kinematic landmarks of the wrist. As the result, most kinematic characteristics for the wrist

transport, and the velocity profile of the wrist showed two peaks. The time of occurrence of the

firs peak was poorly correlated with the time of the first maximal finger aperture. In contrast, the second wrist velocity peak was highly correlated with the time to the second maximal finger

aperture. The researchers concluded that, as the reach progressed and the object to be grasped

was approached, the temporal relationship between the wrist and aperture components of the

movement became more temporally related.

Then, Mon-Williams and James (2001) showed a remarkably simple “rule of thumb”, in which

they argue that the duration ratio of the opening and closing phases of grip apertures is

proportional to the ratio of MGA and the size of the goal object. This “rule of thumb” is simple

and plausible, but predicts a time of maximum grip aperture that is much earlier than is typically

observed in empirical studies.

However, none of these previous models can deal adequately with the observed temporal

coupling between the transport component and the grasp component of prehension. One reason

for this is that no one has experimentally examined in detail this type of coupling between the

two components.

Hu et al. (2005) offered a quantitative model of the temporal coupling between grip aperture and wrist velocity which has shed some light on this issue, showed experimentally that the

correlation between grip apertures and object size is a sigmoidal function of movement duration.

When wrist velocity reaches its peak values, the correlation between the grip aperture and the

size of the goal object has reached half of the correlation that is achieved by the end of the

movement.

Binocular and Monocular Vision

There is strong evidence from physiological, neurological and behavioral studies to suggest that

binocular vision is important for the control of prehension in both patients (Dijkerman, Milner &

Carey) and normal participants (Servos, Goodale & Jakobson).

Servos, Goodale and Jakboson (1992) demonstrated that grasp movements made under monocular viewing were less “efficient” than those performed under binocular viewing conditions, achieving lower peak velocities and showing prolonged periods of deceleration during the closing phase of the grasp.

As part of a continuing investigation into the role that monocular cues play in visuo-motor control, Marotta, Kruyer and Goodale (1998) examined whether or not subjects could use retinal motion information, derived from movements of the head, to help program and control transport and grasp movements when binocular vision is denied. In their experiment, subjects reached out in the dark to an illuminated sphere presented at eye-level, under both monocular and binocular viewing conditions with their head either free to move or restricting. The result is that, under the monocular condition, they showed fewer on-line corrections when they were allowed to move

their head; whereas under the binocular condition, no such difference in performance was seen.

These results suggested that under normal viewing conditions the visuo-motor system prefers to use binocular information, but can fall back on retinal motion information when binocular vision is not available.

Furthermore, Watt, Bradshaw (2000) asked the subjects to reach for and pick up objects under

binocular and monocular viewing both in the absence of a visible scene around the target objects

(complete darkness with “self-illuminated” objects and hand) , and under normal (fully

illuminated). Analysis of the kinematic parameters indicated that binocular information may play

an important role in normal grasp formation; by contrast, the transport of the prehension appears less dependent on binocular information.

Nevertheless, if one eye becomes worse than the other, the overall binocular visual performance

reaches the monocular levels, and in some cases the overall binocular performance is lower than

that of the good eye alone. This phenomenon is called binocular inhibition which has been

presented in the clinic experiment. Recently, Pardhan, Gonzalez-Alvarez (2005) presented

evidence of binocular visuo-motor inhibition by various tasks under various experimental

conditions, whereby when the vision of one eye is decreased, and the binocular motor

performance is worse than that of the good eye alone.

Brain mechanisms of visuo-motor channel hypothesis

Many authors have investigated the anatomical substrate of transport and grasp visuo-motor

channels, following the flow of visual information from the occipital pole to the frontal cortex.

Visual information leaves the primary visual cortex following two main pathways:

1. a dorsal one directed to the posterior parietal cortex;

2. a ventral one that reaches the cortex of the inferior temporal lobe

The functional characteristics of posterior parietal neurons, and the existence of direct

connections between posterior parietal and premotor frontal cortices, suggested that the dorsal

visual stream was involved in the visual guidance of prehension.

The dorsal visual stream includes at least tow separate channels, a medial one passing mainly

through the visual areas of the SPL, and a lateral one passing mainly through the visual areas of

the IPL. The dorso-medial visual stream has been supposed to carry out the visuomotor

transformation necessary of guiding transport movements of the arms, while the dorsolateral

visual stream the visuomotor transformations necessary for grasp movements [21, 27]. However, recent physiological and anatomical data suggest that the dorsomedial visual stream is involved in both transport and grasp action. This proposal is based on new data on functional organization and anatomical connections of medial sector of parieto-occipital cortex, the region of the brain visual information passes through on the way to reach the frontal cortex.

The digit channel hypothesis

In recent years, the theory of parallel visuo-motor channel hypothesis has been debated and

criticized by several authors from both the experimental and theoretical points of view (see [3, 15, and 23]).

On one hand, viewed from an informational perspective, recent experiments demonstrated that a change in object size or other intrinsic properties affects the kinematics of the transport phase.

Goodale et al. (1994) found that, when grasping irregular objects, the final grip aperture is

determined by the grasping locations on the object’s surface. Similarly, Paulignan et al.,

Jakobson, Chieffi and Gentilucci also put forward objection in terms of the correspondence

between visual information and two components. Consequently, these observations suggest that

the coordination of transport and grasp may not occur via separate channels but rather that there may be a coupled integration which can alter the kinematic relationship of these two features in a functionally specific manner.

On the other hand, from the aspect of the anatomy, against the classical description, Wing et al.,

Haggard and Lemon et al., argued that neither the correspondence between the transport

component and movements of proximal segments, nor the correspondence between the grasp

component and the activation of distal muscles are unequivocal.

Furthermore, in the visuo-motor channel hypothesis, functional and anatomical data suggested

that reaching movements are controlled by a medial parietofrontal circuit that involves the

superior parietal lobule (SPL) and the dorsal premotor cortex (PMd), while grasping movements

are controlled by a lateral parietofrontal circuit involving the inferior parietal lobule (IPL) and

the ventral premotor cortex (PMv, [11, 31]). Nevertheless, it has been demonstrated that the

pathways linking posterior parietal cortex with PMd and PMv, though largely segregated, also

partially overlap [26]. In addition, it is now clear that both PMd and PMv contain cells encoding

the arm direction of movement [1, 12 and 30], as well as proximal and distal representations of

the arm [4, 5 and 19]. The conclusion is that the medial and lateral parietofrontal circuits can

hardly be considered as two separate visuo-motor channels for transport and grasp. They seem

more likely involved in both processes.

Formulation of the digit channel hypothesis

Based on the above objections, an alternative model suggests that separate visuo-motor channels exist for the finger and the thumb, which was proposed by Smeets and Brenner (1999). This hypothesis is known as the digit channel hypothesis. In the digit channel hypothesis, Smeets and Brenner abandoned grip as a variable within grasping. Instead, they regarded grasp as simply moving the fingers and thumb to position on the surface of an object of interest. Recently, there have been more and more studies to support this new view. OPTOTRAK 3D system is used to measure the prehension movements.

Smeets, Brenner (2001) asked subjects to grasp disks with different diameters at marked

positions with tow digits [21]. The positions were at opposite sides of the disk, at the same

distance from the starting position, so that the orientation of the surface was the same for both

digits. The subjects grasped the disks either with index finger and thumb of the dominant hand,

with the same digits of the non-dominant hand, or bimanually with both index fingers. The

results demonstrated that the well-known relation between object size and grip aperture holds for each digit; that the same relation holds if the object is grasped with hands instead of with the

thumb and finger of one hand.

Cuijpers, Smeets and Brenner (2004) have studied the relation between object shape and

grasping kinematics. They asked subjects to grasp elliptical cylinders with different aspect ratios

at various orientations and distances from the subject [2]. The results show that the perceived

shape of the cylinder is used for selecting appropriate grasping locations before or early in the

movement and that the grip aperture and orientation are gradually attuned to these locations

during the movement.

Although the digit channel hypothesis has some advantages over the visuo-motor channel

hypothesis, it still remains an empirical question as to which hypothesis best captures the nature

of prehension. According to the digit channel hypothesis, both the thumb and the index finger are being transported when carrying out a precision grasp, however, in some special situations, the visuo-motor channel controlling the grasp aperture formation will ensure that the distance

between the digits is sufficient for grasping the object whilst avoiding any obstacles within the

workspace. To retain many of the very attractive features of the digit channel hypothesis within

an alternative account, Mon-Williams, McIntosh (2000) have christened the third-way hypothesis. According to this hypothesis, the system transports either the tip of the thumb or the tip of the index finger with the grip formation being controlled relatively independently. This hypothesis suggests why some evidence points towards transport of the thumb whilst other evidence suggests that it is the index finger that is transported. Nowadays, more evidence to support this new hypothesis is still needed [15].

Summary

We have collected all the reasonable hypotheses of the control of the prehension movement,

changing the perspective from one based on transport and grasp to one based on movements of

the individual digits. We compare the two hypotheses from anatomical, neuropsychological,

cognitive perspectives. We expect more and more experimental research on the human’s

prehension movement that is going to be carried out to verify which hypothesis is more

advisable.