Impaired delayed but preserved immediate grasping in a neglect patient with parieto-occipital lesions

Patients with optic ataxia, a deficit in visually guided action, paradoxically improve when pantomiming an action towards memorized stimuli. Visual form agnosic patient D.F. shows the exact opposite pattern of results: although being able to grasp objects in real-time she loses grip scaling when grasping an object from memory. Here we explored the dissociation between immediate and delayed grasping in a patient (F.S.) who after a parietal-occipital stroke presented with severe left visual neglect, a loss of awareness of the contralesional side of space. Although F.S. had preserved grip scaling even in his neglected field, he was markedly impaired when asked to pretend to grasp a leftward object from memory. Critically, his deficit cannot be simply explained by the absence of continuous on-line visual feedback, as F.S. was also able to grasp leftward objects in real-time when vision was removed. We suggest that regions surrounding the parietal-occipital sulcus, typically damaged in patients with optic ataxia but spared in F.S., seem to be essential for real-time actions. On the other hand, our data indicates that regions in the ventral visual stream, damaged in D.F but intact in F.S., would appear to be necessary but not sufficient for memory-guided action.     

Visuomotor performance based on peripheral vision is impaired in the visual form agnostic patient DF

The perception-action model states that visual information is processed in different cortical areas depending on the purpose for which the information is acquired. Specifically, it was suggested that the ventral stream mediates visual perception, whereas the dorsal stream primarily processes visual information for the guidance of actions (Goodale & Milner, 1992). Evidence for the model comes from patient studies showing that patients with ventral stream damage (visual form agnosia) and patients with dorsal stream damage (optic ataxia) show divergent performance in action and perception tasks. Whereas DF, a patient suffering from visual form agnosia, was found to perform well in visuomotor tasks despite her inability to use vision for perceptual tasks, patients with optic ataxia show usually the opposite pattern, i.e. good perception but impaired visuomotor control. The finding that both disorders seem to provoke a mirror-reversed pattern of spared and impaired visual functions, led to the belief that optic ataxia and visual form agnosia can be considered as complementary disorders. However, the visuomotor performance of patients with optic ataxia is typically only impaired when they are tested in visual periphery while being often preserved when tested in central vision. Here, we show that DF's visuomotor performance is also only preserved when the target is presented centrally. Her reaching and grasping movements to targets in peripheral vision are abnormal. Our findings indicate that DF's visuomotor performance is quite similar to the visuomotor performance of patients with optic ataxia which undermines previous suggestions that the two disorders form a double-dissociation.     

Optic ataxia and the function of the dorsal stream: Contributions to perception and action

Optic ataxia (OA) is one of the symptoms pertaining to Bálint's Syndrome. It has been described clinically for nearly 80 years before it became a cornerstone of the most popular dual stream theory of the visual brain. Over the last 10 years a regain of interest for this neurological condition lead to a number of precise analyses of the deficits found in optic ataxia, giving rise to a renewed outline of its very definition and hence of the function(s) of the occipito-parietal (dorsal) stream.In absence of concomitant clinical symptoms, we review evidence that misreaching errors in central vision result from the “hand effect”: an erroneous dynamic spatial processing of proprioceptive information from the hand. When visual feedback of the hand is provided (closed-loop condition), pure optic ataxia is restricted to peripheral vision. This central versus peripheral vision distinction is repeatedly used to argue that action and perception are not unique and dissociated systems. New assessments of optic ataxia patients are provided, confirming on one hand that their visuomotor deficit is specific to peripheral vision (i.e. when the gaze and the hand goals are dissociated), on the other hand that they disclose perceptual deficits in peripheral vision. These results are coherent with the recent demonstration that optic ataxia patients exhibit a general contralesional deficit for dynamic visuo-spatial processing, affecting both hand and eye movements [Gaveau, V., Pélisson, D., Blangero, A., Urquizar, C., Prablanc, C.,Vighetto, A., et al. (2008). A common parietal module for saccade and reach: Eye-hand coordination and saccadic control in optic ataxia. Neuropsychologia, 46, 475–486]. Such module(s) within the dorsal stream could be used for both action and perception in the periphery.It is concluded that optic ataxia cannot be considered as a unitary and specific visuo-manual deficit, and that the modular organisation of the dorsal stream allows for numerous dorsal–ventral interactions for perception and action.     

Deficits in peripheral visual attention in patients with optic ataxia

Earlier research has suggested that optic ataxia, a deficit in reaching in peripheral vision, can be isolated from Balint's syndrome as it is primarily a visuomotor disorder, independent of perceptual or attentional deficits. Yet almost no research has examined the attentional abilities of these patients. We examined peripheral visual attention in two patients with unilateral optic ataxia. Results indicated that both patients were slower to respond to targets in their ataxic visual field, irrespective of cuing condition (i.e. validly, invalidly, and no cue conditions), consistent with an overall decrease in the salience of stimuli in the ataxic field. Attentional deficits in peripheral vision are therefore an important factor to consider when examining visuomotor control deficits in optic ataxia.     

Balint syndrome as a result of a biparietal infarct. Neuropsychological analysis

A case of Balint syndrome with bilateral parietal infarction is presented. Analysis shows the tight intrication of visual inattention and psychic gaze palsy. The deficit of visuo-manual adjustment is characterized by a fixed divergence between the target and the point where the patient places his hand, either in ballistic movements (classical optic ataxia), either in pursuit movements; for this reason, a simple disconnexion should not explain the classic optic ataxia. The discretion of aphasia allows the individualization of an anterograde and partially retrograde amnesia.     

Attention for action?: Examining the link between attention and visuomotor control deficits in a patient with optic ataxia

The classic definition of ‘pure’ optic ataxia suggests that these patients’ visuomotor impairments are independent of perceptual or attentional deficits. More recent work suggests that some patients with optic ataxia also have difficulty attending to targets in their ataxic field. Thus, an important question is whether these attentional deficits might be related to the well-known problems in visuomotor control evident in these patients. To investigate this question we had controls (N = 5) and CF, a patient with optic ataxia in his left visual field, perform tasks that required them to detect or reach towards targets presented in either central vision, or at different target eccentricities in the periphery. As expected, CF was less accurate than controls when reaching to targets in his ataxic (left) visual field, and was much slower than controls to detect the presence of targets in his ataxic field. The reaction times to lift the hand in the pointing and the detecting conditions were correlated in the ataxic field of patient CF, suggesting a common attentional deficit in both tasks. Importantly, although CF was slower to detect targets in the ataxic field, and less accurate to reach towards those same targets, the two deficits did not follow the same pattern. Specifically, only reaching errors in the ataxic field were strongly modulated by target eccentricity. These results suggest that dorsal posterior parietal lesions result in attention and visuomotor control problems in optic ataxia that arise from damage to independent mechanisms.     

Attention in action: evidence from on-line corrections in left visual neglect

It is widely accepted that the posterior parietal cortex is critical for the on-line control of action and optic ataxia patients are unable to correct their movements in-flight to changes in target position. The current study investigated on-line correction in patients with left visual neglect, right brain damaged patients without neglect and healthy controls. Participants were asked to reach towards a central target that could jump unexpectedly, at movement onset, to the right or left sides of space. In response to the jump, participants were asked either to follow the target or to stop their movement. Neglect patients were able to correct their ongoing movements smoothly and accurately towards right and left target jumps. They did so even when told to stop their movement, indicating that these corrections occurred automatically (i.e., without instruction). However, the timing of corrections to the left was delayed in neglect patients and this produced a drastic increase in movement time. To our surprise, we also found that neglect patients were impaired at stopping their ongoing reaches, when compared to the control groups, in response to either left or right jump trials. We suggest that the 'automatic pilot' system for the hand is spared in neglect, but its processing speed is unilaterally slowed due to a deficit in orienting of attention to the contralesional side. We relate these findings to the breakdown of a system that combines information for attention, perception and action. Damage to this system may not only slow corrective movements to the contralesional side, but also produce non-lateralized deficits in interrupting an ongoing reach.     

A general deficit of the 'automatic pilot' with posterior parietal cortex lesions?

Lesions of the parieto-occipital junction (POJ) in humans cause gross deviations of reaching movements and impaired grip formation if the targets are located in the subjects' peripheral visual field. Movements to central targets are typically less impaired. This disorder has been termed "optic ataxia". It has been suggested that a general deficit of online corrections under central as well as peripheral viewing conditions might be sufficient to explain this discrepancy. According to this hypothesis, patients with optic ataxia should demonstrate an impaired online correction of grip aperture under central viewing conditions if the target object changes its size during the grasping movement. We investigated this prediction in a patient with optic ataxia (I.G.) in a virtual visuo-haptic grasping task. We imposed an isolated need for online corrections of the hand aperture independently of positional changes of the target object. While we found some general inaccuracies of her grasping movements, the patient did not show a specific impairment of online adjustment of grip aperture. On the contrary, I.G. smoothly adjusted her grip aperture comparable to healthy subjects. A general deficit of fast movement correction affecting targets in peripheral as well as central visual fields thus does not appear to account for the overt visuomotor deficits in optic ataxia. Rather, it seems more likely that an anatomical dissociation between visuomotor pathways related to actions in the central and in the peripheral visual field underlies the dissociation of visuomotor performance depending on the retinotopic target position in optic ataxia.     

Optic ataxia: clinical-radiological correlations with the EMIscan.

After coronary by-pass surgery, a 47 year old, right-handed man developed Gerstmann's syndrome, a visual-spatial perceptual deficit, and a gross impairment of movememt under visual guidance ("optic ataxia"). Visual fields and extraocular movements were intact; he had a left hemiparesis. The EMIscan showed three lesions: a left parietal-occipital lesion; a posterior callosal lesion, and a right frontal lesion. It is hypothesized that optic ataxia in both visual fields requires bilateral lesions which, in the present case, were strategically placed so as to effectively disconnect motor cortex from visual input.     

Atypical, perhaps under-recognized? An unusual phenotype of Friedreich ataxia

Friedreich ataxia (FRDA) is typically characterized by slowly progressive ataxia, depressed tendon reflexes, dysarthria, pyramidal signs, and loss of position and vibration sense with onset before 25 years. While several atypical forms of FRDA are recognized, profound vision deficit is rare. We describe here a 41-year-old man with profound vision deficit and episodic complete blindness associated with marked optic atrophy, spastic paraparesis, and sensory neuropathy without ataxia whose diagnostic evaluation revealed compound heterozygosity for two frataxin mutations, a 994 GAA repeat intronic expansion and c.389G > T (p.G130V) missense mutation. This case emphasizes that FRDA should be considered for individuals with significant vision deficit with optic atrophy and sensory neuropathy, even in the absence of ataxia. This case also raises the additional, related concern that prior studies may underestimate the frequency and varieties of variant forms of FRDA.     

Mirror agnosia and mirror ataxia constitute different parietal lobe disorders.

We describe two new clinical syndromes, mirror agnosia and mirror ataxia, both characterized by the deficit of reaching for an object through a mirror in association with a lesion of either parietal lobe. Clinical investigation of 13 patients demonstrated that the impairments affected both sides of the body. In mirror agnosia, the patients always reached toward the virtual object in the mirror and they were not capable of changing their behavior even after presentation of the position of the object in real visual space. In mirror ataxia (resembling optic ataxia) although some patients initially tended to reach for the virtual object in the mirror, they soon learned to guide their arms toward the real object, all of them producing many directional errors. Both patient groups performed poorly on mental rotation, but only the patients with mirror agnosia were impaired in line orientation. Only 1 of the patients suffered from neglect and 3 from apraxia. Magnetic resonance imaging showed that in mirror agnosia the common zone of lesion overlap was scattered around the posterior angular gyrus/superior temporal gyrus and in mirror ataxia around the postcentral sulcus. We propose that both these clinical syndromes may represent different types of dissociation of retinotopic space and body scheme, or likewise, of allocentric and egocentric space normally adjusted in the parietal lobe.     

Action control in visual neglect

Patients with unilateral neglect show a variety of impairments when reaching towards objects in contralesional space. The basis of these deficits could be perceptual, motor or at one of the intermediate stages linking these processes. Here, we review studies of visually guided reaching in neglect and integrate these results with findings from normal human and monkey action control. We consider evidence which shows that neglect patients can be slow to initiate or execute reaches particularly to a contralesional target. We discuss the directional and spatial deficits that may interact to contribute to such reaching abnormalities and highlight the importance of effective target selection and on-line guidance, exploring the idea that deficits in these mechanisms underlie increased susceptibility to ipsilesional visual distraction in neglect. We also examine the relationship between optic ataxia and neglect by considering two illustrative cases, one with pure optic ataxia and the other with optic ataxia plus neglect, which reveal differences in the anatomical substrates of the two syndromes. We conclude that many patients with neglect make abnormal visually guided reaches, but the pattern of reaching deficits is highly variable, most likely reflecting heterogeneity of lesion location across subjects. Rather than being specific to the neglect syndrome, abnormalities of reaching in these patients may correspond to the extent of damage to the visuomotor control system which involves critical regions in both the parietal and frontal cortex, the white matter tracts connecting them and subcortical regions. Thus, the action control deficits in neglect may be conceptualised as a range of impairments affecting multiple stages in the visuomotor control process.     

Recovery of function after brain damage: The motivational specificity of spared neural traces

The present research was concerned with how neural traces spared by a visual ablation may participate in or influence the recovery of visual behaviors. In particular, the question was asked whether these spared neural traces influence only the recovery of those behaviors with which they were specifically associated or whether they may influence the recovery of a range of different behaviors. The procedure which we used to address this problem involved distinguishing particular behaviors on the basis of the motivational state under which they were acquired. The results indicate that if the pre-operative and postoperative motivational states are the same, then the neural traces spared by a visual lesion can influence the postoperative recovery of a brightness discrimination. However, if the preoperative and postoperative motivational states are not the same, then the spared neural traces have very little influence on the postoperative recovery of a brightness discrimination.     

How humans reach: distinct cortical systems for central and peripheral vision.

Lesions of the posterior parietal cortex in humans can produce a specific disruption of visually guided hand movements termed optic ataxia. The fact that the deficit mainly occurs in peripheral vision suggests that reaching in foveal and extrafoveal vision relies on two different anatomical substrates. Using fMRI in healthy subjects, the authors demonstrated the existence of two systems, differently modulated by the two reaching conditions. Reaching in central vision involves a restricted network, including the medial intraparietal sulcus (mIPS) and the caudal part of the dorsal premotor cortex (PMd). Reaching in peripheral vision engages a more extensive network, including the parieto-occipital junction (POJ). Interestingly, POJ corresponds to the site of the lesion overlap that the authors recently found to be responsible for optic ataxia. These two sets of results converge to show that there is not a unique cortical network for reaching control but instead two systems engaged in reaching to targets in the central and peripheral visual field.     

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

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.     

A hand and a field effect in on-line motor control in unilateral optic ataxia

Patients with bilateral optic ataxia fail to show rapid perturbation-induced corrections during manual aiming movements. Based on this, it has been proposed that this pathology results from a disruption of processes of on-line motor control in the posterior parietal cortex (PPC). Here, we show that on-line motor control performance in a patient with unilateral optic ataxia is similar to that of pointing towards stationary targets in peripheral vision, showing the same combination of hand and field effects. We also show that in the patient, manual correction towards his ataxic field was possible only when a preceding saccade (100msec earlier) rapidly provides foveal information about the new target location. In control subjects, manual correction was often, but not necessarily preceded by a saccade. These results allow us to put forward a model of visuo-manual transformation, which involves updating of the reach plan based on the target-eye error, and rely upon two dissociated spatial representations (of the hand and of the target, respectively) within the PPC.     

Correlated deficits of perception and action in optic ataxia

Optic ataxia, following dorsal stream lesions, is characterised by impaired visuomotor guidance. Recent studies have found concurrent perceptual deficits, but it is unclear whether these are functionally related to the visuomotor symptoms. We studied the ability of a well-documented patient (IG) with bilateral optic ataxia to react to sudden target jumps by correcting ongoing reaches or by explicitly reporting the jump direction. IG showed deficient reach corrections, especially for target jumps to the visual periphery, and was similarly slow to discriminate the same jumps perceptually. Across six test conditions, in which the retinal locations of target jumps were varied, her perceptual slowing mirrored her reaching deficit precisely. These findings confirm perceptual impairments after dorsal stream lesions, and imply a shared functional basis with the classical visuomotor symptoms of optic ataxia. Additionally, we show that the online correction deficit is determined dually by the retinal location to which the reach must be diverted, and the location to which it is initially directed. We suggest that this deficit, and its perceptual counterpart, can be traced to a slowed contralesional orienting of attention in optic ataxia.     

No double-dissociation between optic ataxia and visual agnosia: multiple sub-streams for multiple visuo-manual integrations

The current dominant view of the visual system is marked by the functional and anatomical dissociation between a ventral stream specialised for perception and a dorsal stream specialised for action. The "double-dissociation" between visual agnosia (VA), a deficit of visual recognition, and optic ataxia (OA), a deficit of visuo-manual guidance, considered as consecutive to ventral and dorsal damage, respectively, has provided the main argument for this dichotomic view. In the first part of this paper, we show that the currently available empirical data do not suffice to support a double-dissociation between OA and VA. In the second part, we review evidence coming from human neuropsychology and monkey data, which cast further doubts on the validity of a simple double-dissociation between perception and action because they argue for a far more complex organisation with multiple parallel visual-to-motor connections: 1. A dorso-dorsal pathway (involving the most dorsal part of the parietal and pre-motor cortices): for immediate visuo-motor control--with OA as typical disturbance. The latest research about OA is reviewed, showing how these patients exhibit deficits restricted to the most direct and fast visuo-motor transformations. We also propose that mild mirror ataxia, consisting of misreaching errors when the controlesional hand is guided to a visual goal though a mirror, could correspond to OA with an isolated "hand effect". 2. A ventral stream-prefrontal pathway (connections from the ventral visual stream to pre-frontal areas, by-passing the parietal areas): for "mediate" control (involving spatial or temporal transpositions [Rossetti, Y., & Pisella, L. (2003). Mediate responses as direct evidence for intention: Neuropsychology of Not to-, Not now- and Not there-tasks. In S. Johnson (Ed.), Cognitive Neuroscience perspectives on the problem of intentional action (pp. 67-105). MIT Press.])--with VA as typical disturbance. Preserved visuo-manual guidance in patients with VA is restricted to immediate goal-directed guidance, they exhibit deficits for delayed or pantomimed actions. 3. A ventro-dorsal pathway (involving the more ventral part of the parietal lobe and the pre-motor and pre-frontal areas): for complex planning and programming relying on high representational levels with a more bilateral organisation or an hemispheric lateralisation--with mirror apraxia, limb apraxia and spatial neglect as representatives. Mirror apraxia is a deficit that affects both hands after unilateral inferior parietal lesion with the patients reaching systematically and repeatedly toward the virtual image in the mirror. Limb apraxia is localized on a more advanced conceptual level of object-related actions and results from deficient integrative, computational and "working memory" capacities of the left inferior parietal lobule. A component of spatial working memory has recently been revealed also in spatial neglect consecutive to lesion involving the network of the right inferior parietal lobule and the right frontal areas. We conclude by pointing to the differential temporal constraints and integrative capabilities of these parallel visuo-motor pathways as keys to interpret the neuropsychological deficits.