Elsevier

Cortex

Volume 98, January 2018, Pages 102-113
Cortex

Special issue: Research report
Reachability judgement in optic ataxia: Effect of peripheral vision on hand and target perception in depth

https://doi.org/10.1016/j.cortex.2017.05.013Get rights and content

Abstract

The concept of peripersonal space was first proposed by Rizzolatti, Scandolara, Matelli, and Gentilucci (1981), who introduced the term to highlight the close links between somatosensory and visual processing for stimuli close to the body and suggested that this near-body space could in fact be characterized as an action space (Rizzolatti, Fadiga, Fogassi, & Gallese, 1997). Supporting this idea, patients with right hemisphere lesions have been described as impaired in performing actions towards objects and in perceiving their location − but only when the objects were presented within arm's reach (Bartolo, Carlier, Hassaini, Martin, & Coello, 2014; Brain, 1941). Whether the deficit of optic ataxia patients in processing target locations for action has an effect on the representation of peripersonal space has never been explored. The present study highlights optic ataxia patients' specific difficulties in processing hand-to-target distances in a motor task and in a perceptual task requiring identification of what is reachable in the visual environment. The difficulties are especially evident when both the target and the hand are perceived in the visual periphery. Indeed, when patient I.G. was able to fixate the target, her reaching accuracy and her perception of reachable space both largely improved. Furthermore, the difficulties were enhanced when the hand and the target were both in the lower visual field (in a fixed-far condition vs a fixed-near condition). This novel up-down dimension of optic ataxia fits with the larger representation of the lower visual field in the posterior parietal cortex (Pitzalis et al., 2013; Previc, 1990).

Introduction

Specifying appropriate interactions with the physical or social world requires accurate localisation of objects or individuals in space, as well as anticipation of which action is feasible depending on the situation and the body properties (Coello and Iachini, 2015, Delevoye-Turrell et al., 2010). This is particularly true when one intends to reach for and grasp an object to move it to a new location. The distance, size and orientation of the object must be evaluated so that, by appropriately anticipating the object's physical characteristics (Jeannerod, 1997, Morsella et al., 2009) and selecting an accurate final posture (Rosenbaum, van Heugten, & Caldwell, 1996), the hand will conform to those characteristics and successfully manipulate it. Neuroimaging (Chao and Martin, 2000, Iacoboni, 2006) as well as animal (Sakata et al., 1995, Sakata et al., 1997) studies have shown that posterior parietal cortex is specifically involved in the encoding of 3D features of visual objects in the environment such that it is useful for visual guidance of hand action. For instance, monkey studies have revealed that the neurons in the anterior intraparietal sulcus (AIP) respond to the shape, orientation or size of manipulative objects (Murata et al., 2000, Sakata et al., 1995). As a consequence, behavioural studies have supported the idea that when an individual observes an object, its functional attributes are processed automatically (Culham et al., 2008, Kalénine et al., 2016) through activation of motor regions of the brain (Grezes and Decety, 2002, Proverbio, 2012, Wamain et al., 2015). However, the combination of sensory and motor information in object processing has been shown to be modulated by the egocentric distance of the object according to the body, essentially in relation to the representation of peripersonal space (Gallivan et al., 2009, Previc, 1998, Quinlan and Culham, 2007, Rizzolatti et al., 1981, Wamain et al., 2015).

The concept of peripersonal space was first proposed by Rizzolatti et al. (1981), who introduced the term to highlight the close links between somatosensory and visual processing of stimuli close to the body, and suggested that the near-body space was indeed an action space (Rizzolatti et al., 1997). Objects in peripersonal space can be reached and manipulated immediately, whereas objects in extra-personal space are not immediately accessible and require moving the body to a new location (Coello and Delevoye-Turrell, 2007, Holmes and Spence, 2004, Rizzolatti et al., 1981, de Vignemont and Iannetti, 2015). In a study investigating brain electrical activity associated with object perception in peri- and extra-personal spaces, Wamain et al. (2015) reported that motor-related brain activity, registered through time-frequency analysis of the μ rhythm (8 Hz–13 Hz) in the EEG signals, was observed only for manipulable (compared to non-manipulable) objects when presented in peripersonal (compared to extra-personal) space. Furthermore, Quesque et al. (2016) found that peripersonal space not only contains objects for immediate action, but also specifies our private area in social interactions. Thus, the current view of peripersonal space is that of an abstract representation of a safe space anchored to the body, which moves with the body, and in which the allocation of attention is multisensorial (di Pellegrino and Làdavas, 2015), and objects are represented in terms of deployable actions (Coello & Iachini, 2015, for a review).

Neuropsychological investigations have provided further arguments for dissociation between peripersonal and extra-personal space at the neural level. Brain (1941) reported the first cases of neurological patients impaired in perceptual tasks performed in either peripersonal or extra-personal space. One of the patients for example, suffering a right hemisphere glioblastoma, was impaired in perceiving objects' locations and performing actions towards them, but only when the objects were presented within arm's reach. Because he also observed patients specifically impaired in localising objects in far space, Brain (1941) hypothesised specific brain representation for processing in ‘grasping distance’ within arm's reach and ‘walking distance’ beyond arm's reach (see also Grüsser, 1983, for a similar description). Further studies validated this first observation by showing that patients with an insult to the right parietal cortex show signs of neglect in the contralesional space but predominantly in either peripersonal (Berti and Frassinetti, 2000, Costantini et al., 2014, Halligan and Marshall, 1991, Mennemeier et al., 1992) or extra-personal space (Bjoertomt et al., 2002, Cowey et al., 1994, Shelton et al., 1990, Vuilleumier et al., 1998). In a recent study, Bartolo, Carlier, Hassaini, Martin, and Coello (2014) analysed the encoding of peripersonal space in neurological hemiplegic patients with brain damage localised in either the right or the left hemisphere. Patients were tested in a sequential motor control task (healthy hand) and a reachability judgement task. Interestingly, while patients with left brain lesion did not differ from controls in either task, right brain lesion patients showed a specific deficit in both the sequential motor task and the reachability judgement task, suggesting that motor planning processes specifically involve the right hemisphere (Haaland and Delaney, 1981, Sainburg, 2005, Sainburg and Kalakanis, 2000, Schaefer et al., 2007, Schaefer et al., 2009, Winstein and Pohl, 1995) and contribute to the encoding of peripersonal space (Bartolo et al., 2014, Coello and Iachini, 2015).

Patients with pure optic ataxia (OA) resulting from insult to the superior parietal lobe, are characterised by specific difficulties in reaching and grasping visual targets in the absence of any “clinical” perceptual and oculo-motor disorders (Garcin et al., 1967, Perenin and Vighetto, 1988, Pisella et al., 2009, Pisella et al., 2015, Pisella et al., 2016, Rossetti and Pisella, 2002, Rossetti and Pisella, 2016). Binocular vision as well as motor abilities are preserved, and the deficit itself lacks proprioceptive defect (Garcin et al., 1967, Perenin and Vighetto, 1988). Impaired visuo-motor accuracy in OA is strikingly predominant for targets located in the visual periphery (Bálint, 1909, Jeannerod, 1986, Revol et al., 2003, Rossetti et al., 2005, Vighetto and Perenin, 1981), and reaching and/or grasping objects in central vision are preserved, providing that both the arm and the target objects are visible before movement onset (Coello et al., 2007, Grea et al., 2002, Perenin and Vighetto, 1988, Pisella et al., 2009, Vighetto, 1980). In the presence of a unilateral lesion, the affected peripheral field is contralesional, and one observes the field effect characterised by reaching movements' end-points that are systematically biased towards the central fixation point (Blangero et al., 2010, Pisella et al., 2009, Vindras et al., 2016). Systematic spatial errors can also occur in the healthy visual field when reaching movements are performed using the contralesional hand, a pattern called hand effect (Blangero et al., 2008, Granek et al., 2012, Perenin and Vighetto, 1988, Pisella et al., 2006, Pisella et al., 2009). These effects are consistent with a gaze-centred representation of the target in visuomotor tasks (Batista et al., 1999, Blangero et al., 2005, Henriques et al., 1998a, Henriques et al., 1998b, Khan et al., 2005, Medendorp et al., 2003, Poljac and van der Berg, 2003, Pouget et al., 2002). In agreement with this, the non-alignment of the direction of gaze and the visual target magnifies visuomotor deficits in AO (Khan et al., 2007). As a result, unilateral AO patients show reaching errors that are larger when the visual target is in the visual field contralateral to the lesioned hemisphere, thus supporting a gaze-centred representation of space (Dijkerman et al., 2006, Khan et al., 2005). However, whether this deficit in processing the target location for action affects the representation of peripersonal space has never been explored in patients with OA, and is thus the aim of the present study. To assess the link between peripersonal space representation and visuo-motor deficits in OA, we compared manual reaching performances to perceptual reachability assessment in patient IG, who was characterised by bilateral OA, in conditions of alignment and non-alignment of gaze direction in the near-far dimension.

Section snippets

Case report

Patient I.G. was a 33-year-old suffering from an ischaemic stroke related to acute vasospastic angiopathy in the posterior cerebral arteries established by angiogram. Magnetic resonance imaging revealed a hyperintense signal on T2 sequencing that was fairly symmetrically located in the posterior parietal and upper and lateral occipital cortico-subcortical regions. Reconstruction of the lesion (Talairach & Tournoux, 1988) indicated that it involved mainly Brodmann's areas 19, 18, 7, a limited

Reaction time

In the HC group, RT averaged 417 msec and was not influenced by Gaze condition (F2,18 = .41, p = .67, ns.) or Target location (F2,18 = .528, p = .59, ns.), nor was their interaction significant (F4,36 = 1.30, p = .29, ns., Fig. 2A). I.G.'s RT averaged 700 msec and was significantly affected by Gaze condition and by Target location.

Discussion

The aim of this study was to evaluate the effect of optic ataxia on both manual reaching and the perception of reachable space. In these two tasks, performances were assessed while the patient (I.G.) or the healthy controls (HC) were free to move their eyes or were constrained to fixate a near or far point.

Concerning the motor task, HC showed no sharp effect of target distance or gaze condition on RT or spatial accuracy. The rather consistent spatio-temporal performances observed in HC can be

Acknowledgements

The authors wish to thank I.G. for her time and patience as well as for fruitful discussions, and also all the control participants. We also thank George Michael (University of Lyon) for assisting with the case-controls statistics, and we are grateful to John M. Belmont, Ph.D., for his helpful comments on the manuscript. We are most grateful to Frédéric Volland for his skillful help with the experimental devices. This work was supported by funds from Inserm, CNRS, Hospices Civils de Lyon and

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