Review
The biological and behavioral basis of upper limb asymmetries in sensorimotor performance

https://doi.org/10.1016/j.neubiorev.2007.10.006Get rights and content

Abstract

Asymmetries in upper limb performance are a fundamental aspect of human behavior. This phenomenon, commonly known as handedness, has inspired a great deal of research over the course of the past century garnering interest across a multitude of scientific domains. In the present paper, a thorough review of this literature is provided focusing on the current state of knowledge regarding neuro-anatomical and behavior-based arm asymmetries. It is hoped that this information will provide a basis for new insights regarding the design and implementation of future studies regarding arm laterality.

Introduction

The ability to perform skilled movements of the upper limbs is a defining feature of modern day humans, and has been since the time of their upright standing ancestors some 2.5 million years ago (Bradshaw and Rogers, 1996). Given the gross anatomical symmetry of the arms, however, it is perhaps surprising that the left and right arms did not evolve to have similar degrees of dexterity. Rather, the two arms often demonstrate vast differences in sensorimotor ability, a quality that has been defined as “handedness” and one which has been the subject of intense study within the realms of psychology, neurophysiology and others. The focus of the present paper, therefore, is to review this vast scientific literature with a particular emphasis on upper limb asymmetries in sensorimotor behavior. For reasons that will become more apparent in the section to follow, most research in this area has been biased towards the study of individuals with right-arm preference and, thus, it will generally be beyond the scope of this review to discuss studies involving left-handed individuals. Briefly, however, it should be noted that individuals with left-arm preference appear less lateralized and more variable than their right-handed counterparts, and are not the simple genetic (McManus, 1995) or behavioral inverse (Perelle and Ehrman, 2005).

Section snippets

Right arm biases for movement

While limb asymmetries in motor behavior are evident to some extent in many animal species (see Vallortigara and Rogers, 2005 for a review), humans appear unique in that a clear population level bias exists for using one arm versus the other. Indeed, based largely on self-report questionnaires, it has been estimated that 9 out of 10 individuals are right-handed such that the right arm is preferred over the left when performing tasks such as reaching for a target or manipulating an object (

An enhanced role for the left hemisphere in movement control

In light of the discovery by Broca (1861), and later Wernicke (1874), that the left hemisphere is specialized for various aspects of language, Liepmann (1908) was the first to suggest that asymmetries in motor behavior might also be sub-served by hemispheric processing differences. Specifically, it was hypothesized that the hemisphere contralateral to the preferred arm (most often the left) played an enhanced role for both preferred and non-preferred arm movements. Liepmann (1920) later

Anatomical correlates of handedness

Given the asymmetries in hemispheric function described above, exploration into a potential anatomical substrate for handedness has been undertaken at both macroscopic and microscopic levels. One gross structural component that initially received particular attention is the planum temporale (PT), which is located on the posterior portion of the temporal lobe. Based on postmortem studies, a more abrupt and anterior upward curving of the PT has been reported for the right hemisphere, in contrast

Arm asymmetries in motor output

In line with the functional/anatomical differences outlined above, one of the most traditional approaches to the study of handedness has been the quantification of arm differences in the generation of motor output. A well-known demonstration of this lies in the now classic studies of Woodworth (1899) who assessed the ability of subjects to accurately draw lines of equivalent length with either the preferred or non-preferred hand. In this case, it was found that movements of the preferred right

The dynamic-dominance hypothesis of handedness

Sainburg (2002) first proposed the dynamic-dominance hypothesis of handedness based on several fundamental differences in movement strategy that were observed between the preferred and non-preferred arms of right-handed individuals. Unlike many other behavioral approaches to handedness research, where performance of the non-preferred arm is thought to be inferior for most aspects of movement, this hypothesis proposes that each arm is specialized for a different aspect of movement control.

Open versus closed-loop model of handedness

In contrast to studies of individuals with unilateral brain injury indicating greater arm deficits for left versus right hemisphere damage (Haaland et al., 1977; Haaland and Delaney, 1981; Liepmann, 1908, Liepmann, 1920; Wyke, 1971), more recent behavioral studies by Haaland and Harrington, 1989a, Haaland and Harrington, 1989b, Haaland and Harrington, 1994 and Winstein and Pohl (1995) have supported the notion that each hemisphere may be specialized for different aspects of motor control. In

Upper limb asymmetries in the utilization of sensory feedback

There has been increasing interest over the past several decades in the role that sensory feedback might play in determining arm performance asymmetries. Perhaps the most influential study in this area was conducted by Flowers (1975) who assessed arm performance during a “ballistic” (i.e. relatively feedback independent) tapping task, and a more “corrective” (i.e. relatively feedback dependent) visual aiming task. In the tapping task, subjects were asked to tap the preferred or non-preferred

Summary

The goal of this paper was to review relevant literature regarding the biological and behavioral basis of upper limb sensorimotor behavior. It was shown that, for the majority of individuals, the right arm is preferred over the left when performing many activities of daily living, and that this arm bias likely reflects structural/anatomical differences in the neuromotor system. Despite the preponderance of literature that has focused on right arm motor dominance, however, one novel aspect of

References (180)

  • R.G. Carson et al.

    The preparation of aiming movements

    Brain Cognition

    (1995)
  • C.D. Chapman et al.

    Memory for kinesthetically defined target location: evidence for manual asymmetries

    Brain Cognition

    (2001)
  • C. Civardi et al.

    Hemispheric asymmetries of cortico-cortical connections in human hand motor areas

    Clinical Neurophysiology

    (2000)
  • A. Colley

    Spatial location judgements by right and left-handers

    Cortex

    (1984)
  • C.A. Crosby et al.

    Hand strength: normative values

    Journal of Hand Surgery—American Volume

    (1994)
  • G. Dellatolas et al.

    Age and cohort effects in adult handedness

    Neuropsychologia

    (1991)
  • D. Elliott et al.

    The influence of target perturbation on manual aiming asymmetries in right-handers

    Cortex

    (1995)
  • S.J. Ellis et al.

    Hand preference in a normal population

    Cortex

    (1988)
  • M. Gentilucci et al.

    From manual gesture to speech: a gradual transition

    Neuroscience and Biobehavioral Reviews

    (2006)
  • G.A. Ghacibeh et al.

    Ipsilateral motor activation during unimanual and bimanual motor tasks

    Clinical Neurophysiology

    (2007)
  • A.N. Gilbert et al.

    Hand preference and age in the United States

    Neuropsychologia

    (1992)
  • D.J. Goble et al.

    Development of upper limb proprioceptive accuracy in children and adolescents

    Human Movement Science

    (2005)
  • K.Y. Haaland et al.

    The role of the hemispheres in closed loop movements

    Brain Cognition

    (1989)
  • K.Y. Haaland et al.

    Hemispheric control of the initial and corrective components of aiming movements

    Neuropsychologia

    (1989)
  • K.Y. Haaland et al.

    Limb-sequencing deficits after left but not right hemisphere damage

    Brain Cognition

    (1994)
  • K.Y. Haaland et al.

    Hemispheric asymmetry of movement

    Current Opinion in Neurobiology

    (1996)
  • G. Hammond

    Correlates of human handedness in primary motor cortex: a review and hypothesis

    Neuroscience and Biobehavioral Reviews

    (2002)
  • M. Kawato

    Internal models for motor control and trajectory planning

    Current Opinion in Neurobiology

    (1999)
  • A. Adam et al.

    Hand dominance and motor unit firing behavior

    Journal of Neurophysiology

    (1998)
  • S.V. Adamovich et al.

    Pointing in 3D space to remembered targets. I. Kinesthetic versus visual target presentation

    Journal of Neurophysiology

    (1998)
  • S.V. Adamovich et al.

    Pointing in 3D space to remembered targets. II. Effects of movement speed toward kinesthetically defined targets

    Experimental Brain Research

    (1999)
  • J.M. Aimonetti et al.

    Proprioceptive control of wrist extensor motor units in humans: dependence on handedness

    Somatosensory and Motor Research

    (1999)
  • J. Annett et al.

    The control of movement in the preferred and non-preferred hands

    Quarterly Journal of Experimental Psychology

    (1979)
  • M. Annett

    The distribution of manual asymmetry

    British Journal of Psychology

    (1972)
  • M. Annett

    Genetic and nongenetic influences on handedness

    Behavior Genetics

    (1978)
  • M. Annett

    Left, Right, Hand and Brain: The Right Shift Theory

    (1985)
  • M. Annett

    Handedness and cerebral dominance: the right shift theory

    Journal of Neuropsychiatry and Clinical Neuroscience

    (1998)
  • L.B. Bagesteiro et al.

    Handedness: dominant arm advantages in control of limb dynamics

    Journal of Neurophysiology

    (2002)
  • L.B. Bagesteiro et al.

    Nondominant arm advantages in load compensation during rapid elbow joint movements

    Journal of Neurophysiology

    (2003)
  • L.B. Bagesteiro et al.

    Interlimb transfer of load compensation during rapid elbow joint movements

    Experimental Brain Research

    (2005)
  • S. Barthelemy et al.

    Manual asymmetries in the directional coding of reaching: further evidence for hemispatial effects and right hemisphere dominance for movement planning

    Experimental Brain Research

    (2002)
  • G. Baud-Bovy et al.

    Pointing to kinesthetic targets in space

    Journal of Neuroscience

    (1998)
  • J.L. Bradshaw et al.

    Tool use and the evolutionary development of manual asymmetry

  • J. Brinkman et al.

    Ipsilateral and contralateral eye-hand control in split-brain rhesus monkeys

    Brain Research

    (1970)
  • T.C. Britton et al.

    Central motor pathways in patients with mirror movements

    Journal of Neurology Neurosurgery and Psychiatry

    (1991)
  • P. Broca

    Remarques sur le siege de la faculte du langage articule, suivies d’une observation d’aphemie

    Bulletin de la Societe Anatomique

    (1861)
  • M.P. Bryden et al.

    The measurement of handedness and its relation to neuropsychological issues

  • P.R. Burgess et al.

    Signaling of kinesthetic information by peripheral sensory receptors

    Annual Review of Neuroscience

    (1982)
  • A.J. Butler et al.

    Neural mechanisms underlying reaching for remembered targets cued kinesthetically or visually in left or right hemispace

    Human Brain Mapping

    (2004)
  • R. Cantello et al.

    Magnetic brain stimulation: the silent period after the motor evoked potential

    Neurology

    (1991)
  • Cited by (143)

    • Associations between Turning Characteristics and Corticospinal Inhibition in Young and Older Adults

      2020, Neuroscience
      Citation Excerpt :

      While limited, there are studies supporting similar roles for the right hemisphere in controlling the lower extremities for postural control and locomotion. Specifically, that the right hemisphere engages in spatial orientation, programing, and executing familiar automated movements such as walking (Fling et al., 2014; Goble and Brown, 2008; Wolpert et al., 1998). Further, Fling et al. (2014) demonstrated significant associations between postural balance control and right hemispheric fiber tract structure where poorer white matter microstructural integrity was strongly associated with reduced proprioception in neurotypical and atypical individuals (Fling et al., 2014).

    View all citing articles on Scopus
    View full text