There may be more to reaching than meets the eye: Re-thinking 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
References (52)
- et al.
Neuropsychologia
(2006) - et al.
Optic ataxia is not only ‘optic’: Impaired spatial integration of proprioceptive information
NeuroImage
(2007) - et al.
The posterior parietal cortex: Sensorimotor interface for the planning and online control of visually guided movements
Neuropsychologia
(2006) - et al.
Action control in visual neglect
Neuropsychologia
(2006) - et al.
Reaching errors in optic ataxia are linked to eye position rather than head or body position
Neuropsychologia
(2006) - et al.
Merging the senses into a robust concept
Trends in Cognitive Sciences
(2004) - et al.
Functional coupling between the limbs during bimanual reach-to-grasp movements
Human Movement Science
(2002) - et al.
Dorsal simultanagnosia: An impairment of visual processing or visual awareness?
Cortex
(2006) ‘Action binding’: Dynamic interactions between vision and touch
Trends in Cognitive Sciences
(2001)- et al.
Visuomotor functions of the posterior parietal cortex
Neuropsychologia
(2006)
Prism adaptation produces neglect-like patterns of hand path curvature in healthy adults
Neuropsychologia
Reaching movements may reveal the distorted topography of spatial representations after neglect
Neuropsychologia
Where the eye looks, the hand follows: Limb-dependent magnetic misreaching in optic ataxia
Current Biology
Grasping the past: Delay can improve visuomotor performance
Current Biology
The role of the posterior parietal lobe in prism adaptation: failure to adapt to optical prisms in a patient with bilateral damage to posterior parietal cortex
Cortex
Vision can improve the felt position of the unseen hand: Neurological evidence for links between vision and somatosensation in humans
Current Biology
The posterior parietal cortex and prism adaptation
Neuropsychologia
Parietal updating of limb posture: An event-related fMRI study
Neuropsychologia
No double-dissociation between optic ataxia and visual agnosia: Multiple sub-streams for multiple visuo-manual integrations
Neuropsychologia
Two cortical systems for reaching in central and peripheral vision
Neuron
Coordinate transformations for eye and arm
Current Opinion in Neurobiology
Annual Review Neuroscience
Functional organization of human intraparietal and frontal cortex for attending, looking, and pointing
Journal of Neuroscience
Seelenlähmung des ‘schauens’, optische ataxie, räumliche störung der aufmerksamkeit
Monattsschrifte für Psychiatrische Neurologie
Reach plans in eye-centred coordinates
Science
Optic ataxia as a result of the breakdown of the global tuning fields of parietal neurones
Brain
Cited by (55)
1.33 - Visual-Motor Integration in the Primate Brain
2020, The Senses: A Comprehensive Reference: Volume 1-7, Second EditionEvolved Mechanisms of High-Level Visual Perception in Primates
2020, Evolutionary NeuroscienceAwake craniotomy and bedside cognitive mapping in neurosurgery
2018, Neurosurgical Neuropsychology: The Practical Application of Neuropsychology in the Neurosurgical Practice