Elsevier

Neuropsychologia

Volume 47, Issue 6, May 2009, Pages 1397-1408
Neuropsychologia

There may be more to reaching than meets the eye: Re-thinking optic ataxia

https://doi.org/10.1016/j.neuropsychologia.2009.01.035Get rights and content

Abstract

Optic ataxia (OA) is generally thought of as a disorder of visually guided reaching movements that cannot be explained by any simple deficit in visual or motor processing. In this paper we offer a new perspective on optic ataxia; we argue that the popular characterisation of this disorder is misleading and is unrepresentative of the pattern of reaching errors typically observed in OA patients. We begin our paper by reviewing recent neurophysiological, neuropsychological, and functional brain imaging studies that have led to the proposal that the medial parietal cortex in the vicinity of the parietal-occipital junction (POJ) – the key anatomical site associated with OA – represents reaching movements in eye-centred coordinates, and that this ability is impaired in optic ataxia. Our perspective stresses the importance of the POJ and superior parietal regions of the human PPC for representing reaching movements in both extrinsic (eye-centred) and intrinsic (postural) coordinates, and proposes that it is the ability to simultaneously represent multiple spatial locations that must be directly compared with one another that is impaired in non-foveal OA patients. In support of this idea we review recent fMRI and behavioural studies conducted by our group that have investigated the anatomical correlates of posturally guided movements, and the movements guided by postural cues in patients presenting with optic ataxia.

Introduction

The posterior parietal cortex (PPC) is believed to play a key role in the representation of corporeal and peripersonal space and in the sensorimotor transformations associated with the planning and control of movement. Consistent with this viewpoint, damage to the PPC in humans frequently leads to disorders in the representation of space (e.g., hemispatial neglect) and to impairments in the planning and control of goal-directed movements (e.g., optic ataxia). While much is already known about the visuomotor functions of the PPC; understanding the nature of the sensorimotor transformations carried out within human PPC remains a fundamental and largely unresolved problem for neuroscience and important clinically in treating the consequences of brain injury and brain disease (see Jackson & Husain, 2006 for recent reviews).

Optic ataxia (OA) is most often characterised as a disorder of visually guided reaching movements that cannot be attributed to a basic motor or sensory deficit (Bálint, 1909; Rizzo & Vecera, 2002). The disorder was described initially by Reszö Bálint as one of a triad of visuospatial symptoms that can result from bilateral damage to the occipital-parietal cortex in humans, and which has since become known as Balint-Holmes or Balint's syndrome (Rizzo & Vecera, 2002). More recent studies have confirmed that optic ataxia can also occur in isolation from other symptoms associated with Balint's syndrome and can follow unilateral damage to the parietal cortex of either hemisphere; most frequently involving the intraparietal sulcus and superior parietal lobule (SPL) or white matter underlying these areas (Perenin & Vighetto, 1988). The anatomical loci associated with optic ataxia following unilateral brain damage are reviewed later in this article.

OA is generally thought to be a high-level visuomotor impairment that arises as a consequence of a failure within successive stages of the sensorimotor transformation process strongly associated with the PPC (e.g., Buxbaum & Coslett, 1997), and several lines of evidence provide support for the view that OA cannot be explained by a simple motor deficit as OA patients can be shown to reach accurately under some circumstances but not others. First, a number of studies have reported OA patients who present with so-called ‘field’ effects, in which they misreach (often with both upper limbs) only when reaching for visual targets presented within specific regions of the visual field (most typically in patients with unilateral brain damage this region is contralateral to the site of their lesion) (e.g., Perenin & Vighetto, 1988). Second, as originally noted by Bálint (1909), the misreaching errors exhibited by patients with OA are most often modality specific. That is, while patients will misreach when reaching toward visual targets, they can often reach accurately when pointing without vision toward the location of auditory targets or toward somatosensory stimuli located upon their body (e.g., Bálint, 1909). Third, the magnitude of the misreaching errors exhibited by OA patients has often been shown to be capable of being modulated by task context. For instance, David Milner and colleagues demonstrated that the misreaching errors of an OA patient (AT) were substantively reduced if a 5 s delay was introduced between viewing a visual target and executing a reaching toward that target (Milner, Paulignan, Dijkerman, Michel, & Jeannerod, 1999). This group also demonstrated that reaching accuracy improved when an OA patient (IG) was required to pantomime a reach-to-grasp movement to a visual object (i.e., reach and pretend to grasp a previously visable object) rather than execute a reach-to-grasp movement to the object directly (Milner et al., 2001). Jackson and colleagues also demonstrated, in an OA patient (MU), that removing on-line vision immediately prior to movement onset (triggered coincident with the instruction to reach using a set of PLATO spectacles, see Jackson, Jackson, & Hindle, 2000 for details) substantially improved reaching accuracy (Jackson, Newport, Mort, Husain, Jackson, et al., 2005). More importantly, this group showed that MU's misreaching impairment could be significantly modulated by attentional factors. They demonstrated that MU's non-foveal misreaching impairment could be substantially improved by placing the fixation and target objects on a continuous plinth so that these objects appeared, perceptually, to be more like two components of a single object than two separate objects (Jackson, Newport, Mort, Husain, Jackson, et al., 2005). A similar manipulation has been shown previously to improve perceptual reporting in Balint's syndrome (Humphreys & Riddoch, 1995) and to influence grip aperture scaling in bimanual reach-to-grasp movements (Jackson, German, & Peacock, 2002).

We interpreted these findings as broadly consistent with the idea that visuospatial information about the target and fixation object might compete for limited processing resources, and that this competition is reduced if visual information is removed, or the target and fixation objects are ‘unified’ to form a single visuospatial object. We also suggested that a key aspect of non-foveal OA might be an inability to de-couple reach direction from gaze direction—i.e., to represent simultaneously the spatial coordinates of a reaching movement that differs from the current direction of gaze (Jackson, Newport, Mort, Husain, Jackson, et al., 2005). This idea will be expanded upon below and new data will be introduced to support and expand upon this idea.

That OA is not simply a consequence of a visual impairment such as hemispatial neglect is supported by many reports that OA patients often present with a so-called ‘hand’ effect in which the patient errs when reaching toward visual targets (typically for targets presented in either visual field) only when reaching with one limb but not when reaching with the other (e.g., Bálint, 1909; Jackson, Newport, Mort, & Husain, 2005; Perenin & Vighetto, 1988). Pisella, Binkofski, Lasek, Toni, and Rossetti (2006) review recent evidence suggesting that OA may reflect a functional dissociation between central and peripheral vision: they propose that reaching errors associated with ‘field’ effects are linked to eye-centred representations of visual targets within the PPC whereas errors associated with ‘hand’ effects most likely result from a mislocalisation of the contralesional (ataxic) limb, arising due to an impairment in the processing of proprioceptive information. Below we consider further the nature of the misreaching errors observed in OA.

Section snippets

A problem with the standard view of optic ataxia

As noted above, OA is almost always characterised as an impairment of visually guided reaching movements that cannot be attributed to a basic motor or sensory deficit (Bálint, 1909). Unfortunately while this characterisation is widely accepted it is nevertheless rather misleading as it misrepresents the pattern of reaching errors exhibited by the vast majority of OA patients who present at the clinic, or are described in the literature. The majority of patients who present with OA do not in

Importance of eye-centred coding in understanding non-foveal optic ataxia

Visually guided movements, such as reaching out to grasp an object, ordinarily involve translating visual information that is coded initially in retinotopic coordinates into a motor plan that specifies the sequence of postural changes required to bring the hand to the object. More specifically, information coded in extrinsic (spatial) coordinates must be transformed into a motor plan that can be expressed within intrinsic (motor) coordinates. Key issues are the exact role played by the PPC in

Human POJ and eye-hand coordination: evidence from brain imaging studies

Several recent brain imaging studies have confirmed the importance of the human POJ region for the planning and control of eye and reaching movements in healthy individuals (e.g., Astafiev et al., 2003; Connolly, Andersen, & Goodale, 2003; Medendorp, Goltz, Vilis, & Crawford, 2003; Prado et al., 2005).

Connolly et al. (2003) conducted an fMRI study that compared BOLD activations associated with memory-guided saccadic eye movements and memory-guided reaching movements. These authors identified a

Intrinsic coding of reaching movements in PPC

To execute reaching movements, information specified in extrinsic (spatial) coordinates must be transformed into a motor plan that can be expressed within intrinsic (postural) coordinates. For reaching movements directed to visually defined targets, this will involve translating visual information that is coded initially in retinotopic coordinates, into a motor plan that specifies the sequence of postural changes required to bring the hand to the target. It is currently unclear whether the PPC

Experiment: non-foveal OA patient reaching to visual and non-visual targets

One prediction of the scheme outlined above is that damage to the POJ region in humans might be expected to lead to an impairment in performing reaching movements in circumstances in which information in different coordinates need to be combined. In particular, in circumstances where extrinsic, eye-centred, information needs to be combined with intrinsic, postural, information—such as is the case during reaching movements to extra-foveal targets.

We have sought to test this prediction over

Brief overview of task and procedure

The procedure used was similar to that reported previously. Participants were seated at wooden table upon which rested a raised matt black wooden board containing two sets of two target holes, each 6 mm in diameter. Participants executed pointing movements, using the index finger of each hand, from one of two starting positions located close to the patient's midsaggital axis toward one of two target locations in each case (Fig. 3B). Each pair of target holes were 22° apart, and each target was

Case JJ

JJ was a right-handed male who had suffered recurrent cerebral haemorrhages over a period of 6 years. This patient was studied by our group over a 7-year period and has been the subject of several previous publications which describe in detail aspects of his Balint's syndrome (e.g., Jackson, Newport, Mort, & Husain, 2005; Jackson, Newport, Mort, Husain, Jackson, et al., 2005; Jackson, Shepherd, Mueller, Husain, & Jackson, 2006; Newport & Jackson, 2006). At the time of testing he was 70 years

Results

Reaching movements were recorded and quantified using a minibird magnetic motion tracking device. Movements were also recorded using digital video and direction of gaze was monitored throughout. Previous studies by our group using this task have demonstrated that healthy adults make very accurate reaching movements, even when reaching to proprioceptively defined target locations without vision. Jackson and Newport (2001) reported that reaching movements directed to visually defined targets, to

Discussion

Our data from JJ confirm and extend the original observation made by Buxbaum and Coslett (1997) that OA patients most typically exhibit misreaching errors only when reaching to extra-foveal target locations. Our data demonstrate that misreaching errors are larger when patients are required to reach to visually defined extra-foveal targets as previously reported (e.g., Jackson, Newport, Mort, & Husain, 2005), and more importantly, when reaching toward proprioceptively defined target locations

Conclusion

This paper presents our current perspective on non-foveal OA. It is largely based upon our observation of patients presenting with Balint's syndrome following bilateral damage to the PPC, and builds upon recent electrophysiological studies of monkey PPC and brain imaging studies of the role played by human PPC during reaching movements. Our perspective stresses the importance of the SPL and POJ regions of the human PPC for representing reaching movements in both extrinsic (eye-centred) and

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