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Optic ataxia in Ba´lint-Holmes syndrome§ L. Pisella *, Y. Rossetti, G. Rode INSERM U1028 CNRS UMR 5292, ImpAct Team, Lyon Neuroscience Research Center (CRNL), 16, avenue du Doyen-Le´pine, 69676 Bron cedex, France
A R T I C L E I N F O
A B S T R A C T
Article history: Received 25 November 2015 Accepted 5 December 2015
The objective of this review is to reinstate the diversity of visual perception and visuomotor symptoms following lesions to the posterior parietal cortex (dorsal visual stream). This diversity was overshadowed for a long time and shows the contribution of the dorsal visual stream not only to action but also to perception. More precisely, we propose that the visuomotor deficit in optic ataxia stems from two distinct components: visual proprioceptive deficit (hand effect) and visual attentional deficit (field effect) also affecting the perception in peripheral vision. ß 2016 Elsevier Masson SAS. All rights reserved.
Keywords: Optic ataxia Posterior parietal cortex Dorsal attentional network
1. Introduction The issue of relationships between perception and action plays a key role in several exploration fields related to upper functions of the body, such as Philosophy, Human Sciences or Neurosciences. Neuroanatomy suggested the existence of several visual pathways connecting the retina to the cortex. Experiments conducted on monkeys showed the existence of two divergent visual pathways corresponding to two different functions: the processing of the ‘‘where’’ and ‘‘what’’. One of these pathways, the occipito-temporal or ventral stream, links the prestriate areas to the inferior temporal cortex. A lesion in the inferior temporal cortex abolishes the visual discrimination of objects without affecting the perception of spatial relationships between the objects themselves (relative positions). The other occipito-parietal pathway or dorsal stream reaches the posterior parietal cortex. A lesion in the posterior parietal cortex is responsible in monkeys of spatial disorientation characterized by a deficit in the perception of relative positions [1] and localization of objects during targeted actions [2]. In humans, the behavioral effects of neurological damage involving a limited part of the posterior parietal cortex were analyzed in this theoretical context [3,4]. Patients presented with difficulties in directing their actions towards objects positioned in their peripheral visual field, even though they did not have any difficulties in recognizing these objects. This neurological deficit called optic ataxia is observed after damage to the dorsal stream. The reverse dissociation was observed in patients with bilateral
§
This work was supported by the Labex ANR-11-LABX-0042. * Corresponding author. E-mail address: [email protected] (L. Pisella).
damage to the occipito-temporal cortex who showed visual agnosia [5]: patient DF could not recognize the size, shape or orientation of the objects, whether her response was verbal or indicated by a matching motor task. However, when she needed to reach objects with a natural grasping gesture, her maximal grip aperture, measured during movement, was correlated with the size of the object. These observations suggest that during her action she could process visual information on the objects metric properties that she could not consciously perceive. The confrontation of these results with those obtained in patients with optic ataxia, suggests that deficits in the visual recognition of objects and directed action can be clearly dissociated. Optic ataxia and visual agnosia were considered for a long time as the two components of a dorsal-ventral differentiation, which could in reality correspond to a dissociation between the perception of the ‘‘what’’ and the organization of the ‘‘how’’ when directing an action [6,7] rather than the dissociation proposed within the perception field [1] for processing the various properties of objects (‘‘where’’ vs. ‘‘what’’). To simplify, the parietal posterior cortex, with its associated optic ataxia deficit, was considered as the specific area for actions, leaving perception and visual consciousness to the occipitotemporal ventral stream. This dichotomous vision was proposed in a book [6] that had a major influence on neurosciences for a decade. However, in parallel, modern functional neuroimaging data evidenced a systematic activation of the parietal posterior cortex in all perception tasks performed without a motor response, and thus attributed it a major role in attentional phenomena. To reconcile these two views, one needs to refer to the first clinical descriptions of the consequences of parietal cortex damage (Ba´lint’s syndrome [8,9]) and modulate the truncated view of optic ataxia that was presented under the influence of the perception–action dissociation theory.
http://dx.doi.org/10.1016/j.rehab.2016.01.003 1877-0657/ß 2016 Elsevier Masson SAS. All rights reserved.
Please cite this article in press as: Pisella L, et al. Optic ataxia in Ba´lint-Holmes syndrome. Ann Phys Rehabil Med (2016), http:// dx.doi.org/10.1016/j.rehab.2016.01.003
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2. Ba´lint’s syndrome
3. Optic ataxia
Symptoms following bilateral damage of the parietal posterior cortex (dorsal stream) were initially described by Ba´lint in 1909 [8] and 10 years later by Holmes using other terms [9]. The syndrome described by Ba´lint includes a triad of symptoms described as such:
Optic ataxia corresponds to the difficulty in performing gestures located in the contralesional visual field (field effect) and/or with the contralesional hand (hand effect), in the absence of primary visual, proprioceptive or motor disorders. These two effects are additive, which already implies that they are independent: the most severe errors are observed when the patient directs a movement with the ataxic hand towards the ataxic field, intermediate severe errors are observed when the patient directs the healthy hand towards the ataxic field and the ataxic hand towards the healthy visual field, movements performed with the healthy hand towards the healthy visual field are normal (Fig. 1-open-loop).
‘optische Ataxie’, imprecision of visually-guided movements characterized by spatial errors that were observed with the right hand (‘‘hand effect’’); ‘ra¨umliche Storung der Aufmerksamkeit’–lateralized attention deficit, it was described as attention being biased towards the right side of the extra-personal space, so left stimuli were neglected; ‘seelenla¨hmung des Schauens’–attention symptom different from the previous one described as an extreme restriction of visual attention, i.e. the inability of an individual to perceive more than a single object at a time (called ‘‘Simultanagnosia’’ later on in the literature) [10,11]). This third symptom was often referred as a ‘‘psychic paralysis of gaze’’ because it was described as a fixed gaze not stemming from oculomotor deficit but rather inattention for stimuli located in the peripheral visual field; In the description of the ‘‘disturbances of visual orientation’’ syndrome reported by Holmes [9,12] in World War I soldiers with bilateral parietal lesions, oculomotor disorders had a large impact: the author described a wandering gaze when visually looking for a target and difficulty in maintaining fixation. These disorganized eye movements (later on called ‘‘gaze ataxia’’ or ‘‘gaze apraxia’’ [13]) were associated with a complete inability to direct grasping movements (optic ataxia). Holmes considered that these visual-manual and oculomotor disorders were the consequence of a lower level impairment preventing to visually locate the targets. The major difference between the descriptions by Ba´lint [8] and Holmes [9] resides in their interpretation of visuomotor disorders. As a matter of fact for Ba´lint, oculomotor impairments are the consequences of attention disorders, and because of the ‘‘hand effect’’ observed in his patient, the optic ataxia could not simply be a vision-related disorder. In line with Ba´lint, following authors have defined optic ataxia following focal damage to the superior parietal lobule and the intraparietal sulcus as a specific disorder of the visual–manual processing of spatiotemporal object information (localization, but also orientation and size, all determining the exact gesture to grasp them), without comparable visual perception, attention or eye movement disorders [4,14]. However, this debate between visuospatial or purely visual-manual interpretation of ataxia has been refueled by neuroimaging that showed that the superior parietal lobule and intraparietal sulcus constituted the neural substrate of the ‘‘dorsal attention system’’ voluntary orienting the attention toward a location of interest in the peripheral vision [15]. In accordance with these neuroimaging data, attention deficits are systematically found when specifically screened in patients with unilateral [16–19] or bilateral optic ataxia [20]. In this chapter, we propose to explore these visual attention deficits and differentiate them from those in patients presenting with clinical hemispatial neglect. First, we will describe more precisely the combination of the two aspects of visualmanual deficits in optic ataxia: the hand effect, which prevented Ba´lint from concluding to a purely visual disorder that we view as a high-level spatiotemporal integration disorder for proprioceptive information; the field effect for which we are proposing an attentional-related interpretation.
3.1. Hand effect The hand effect prompted Ba´lint to dissociate optic ataxia from the other perception and attentional symptoms of the triad. Fig. 1 shows that this hand effect depends on the ability of patients to see their hand (closed-loop) or not (open-loop), since the effect is strongly reduced when patients can see their hand in the start position and during the movement, whereas this visual reafference does not significantly change errors made with the healthy hand in the contralesional field (i.e. the field effect errors). When there is no visual reafference for the hand position (in the open-loop condition), only proprioception can indicate this position. The resulting increased ‘‘hand effect’’ errors in the open-loop condition suggest that those are more severe when proprioceptive information are used to guide the action, and thus the hand effect is in fact a proprioceptive information processing deficit. To test this hypothesis, we had two patients with unilateral optic ataxia perform a proprioceptive pointing task [21]. Patients were in the dark and had to fixate at a fluorescent dot positioned in the frontal plane straight ahead of them. They had their arm placed under a board and the investigator positioned behind the board placed their hand on that frontal plane, on the right side or left side of their visual fixation point. They were instructed to use their other hand to point on the other side of the board where the hand was positioned by the investigator. Patients never received feedback on their performance regarding locating their hidden hand by pointing to it with their other hand. In a first experience, they had to point with their ataxic hand towards their healthy hand. We observed the combination of a field effect and hand effect equivalent to the pointing task of the ataxic hand towards the visual target illustrated in Fig. 1: errors from 3 to 5 cm occurred, and were more severe when the healthy hand (target) was positioned in the contralesional space. In a second experience (Fig. 2), patients had to point with their healthy hand towards their ataxic hand, positioned either in the left space or in the right space in regards to the visual fixation point. In a remarkable manner, we noted in this condition much wider errors, about 12 cm in average for the patient Can and 8 cm in average for the patient Ok, errors were slightly greater when the ataxic hand was positioned in the patient’s ataxic field. These errors were grossly directed towards the center of the board where the patient had to fixate the fluorescent dot, and were so severe that sometimes they could bring the patient Can to point to the ipsilesional field when the hand was presented in the ataxic field (Fig. 2. Middle images: positions where the ataxic hand was moved by the investigator are indicated by full squares [target positions], positions pointed by the patient with the healthy hand are indicated by circles and a motor error vector materialized the difference between these two positions). These considerable errors demonstrate that a major pathological element of optic ataxia is the inability to locate the ataxic hand when presented as a target in the extra-personal space. It is important to note that this disorder is not a primary proprioceptive disorder because this function remains intact as verified by the clinical
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Fig. 1. Pointing errors (in mm) exhibited by a unilateral optic ataxia patient when pointing with his contralesional or ipsilesional hand toward visual targets presented in his contralesional or ipsilesional visual field, with visual feedback of his hand (closed loop) or without (open loop). Errors made with the contralesional hand are significantly reduced when visual feedback of the hand is provided.
diagnosis of optic ataxia, and validated by asking the patient Can to reproduce with his healthy arm the position requested by the investigator, and vice versa, the patient completed the test with no difficulties (Fig. 2, lower images). It is in fact a high-level specific proprioceptive localization disorder, or in other terms a motorproprioceptive transformation for a directed movement, explaining the errors related to the hand effect, just like the field effect was evidenced as a high level visuomotor disorder for a directed movement [4]. 3.2. The field effect Field effect errors were also studied and represented in two dimensions via error vectors. Fig. 3 shows that these errors are similar to those of proprioceptive localization in Fig. 2, because they are also greater when the target is presented further from the visual fixation point and they are globally directed towards the gaze location, when the fixation point position is changed it affects the error vectors [21,22]. Our first observation reporting a deficit of peripheral vision detection in a patient with optic ataxia was in fact fortuitous. It was in the context of a task where we explored the visuomotor reaction of patients with optic ataxia, after allowing a delay for memorizing the target and at the time when the patients started the pointing gesture, the target could reappear in their peripheral vision but in a different position [23]. Results showed that in this condition controls directed their pointing movement towards the newly presented target, whereas patients started the movement towards the memorized previous target location and changed their pointing trajectory only during the movement towards the newly presented target (9 tests
out of 16 for patient AT and 13 tests out of 16 for patient IG). This visuomotor behavior backed up the arguments in favor of a deficit of visual information processing regarding real-time spatial localization in optic ataxia [24–27]. After the experiment, we asked the patients if they were aware that we sometimes moved the targets in their peripheral vision. Patient AT reported never having detected a change in position. Patient IG who spontaneously made some remarks regarding changes in the target position, accepted to do the experiment again, this time with a double task to point and tell us if the target had been moved or not. To our amazement, she produced a lot of false positives in her verbal response and sometimes performed trajectory corrections that took her hand further away from the targets really presented to her (corresponding to these false positives). This behavior showed that she did not always perceive the targets in her peripheral visual field when executing the movement! Finally, her perception performance to detect position changes in her peripheral vision appeared even more impaired than her visuomotor performance in reaction to these changes [23], whereas according to the model by Milner and Goodale [6] optic ataxia is an action-related deficit preserving perception. Furthermore, we explored in this patient and one age-matched control subject, the abilities to detect changes in peripheral and central vision for different visual characteristics. Her detection performance was similar to the control subject for the central vision. Regarding peripheral vision (at 208), her detection performance was greatly reduced, with an 80% decrease in performance for orientation changes, 70% for changes in size and 50% for changes in spatial location (Fig. 4 [28]). Her detection of shape changes was retained, probably because these were not metric attributes but rather categorical attributes of the object’s identity (e.g. Round, square,
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Fig. 2. Pointing errors (in mm) exhibited by two unilateral optic ataxia patients (Can and Ok) when pointing with their ipsilesional (non-ataxic) hand toward their contralesional (ataxic) hand presented in their contralesional or ipsilesional visual field in the dark (eyes were open and only a central fixation dot was visible). As illustrated by the error vectors drawn from the target positions (red squares) toward the corresponding endpoints (blue diamonds), the amplitude of the errors (length of the vectors) in this condition of proprioceptive pointing were very large, and larger when the ataxic hand was positioned in the contralesional hemifield. The pictures below show that the patient with eyes closed still could reproduce the posture of the ataxic arm with the ipilesional arm and vice versa, confirming that the deficit of proprioceptive pointing is not due to primary proprioceptive deficit.
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Fig. 3. Error vectors (see legend of Fig. 2) and 95% confidence ellipses (variability) of pointing made toward peripheral visual targets (red squares) while keeping their eyes on central fixation (cross) by healthy controls (top panel), patients with right hemisphere lesion (middle panel) and left hemisphere lesion (bottom panel), with their left hand (left column) and their right hand (right column) separately.
triangle). We conclude that the functional difference between ventral and dorsal pathways is better explained by the type of visual attribute processed (categorical vs. metric) and central vs. peripheral vision, than by a role dedicated to perception vs. action [28]. The relationship between these fine perception deficits in the peripheral vision and spatial attention deficit could be due to the fact that spatial attention is a process improving spatial resolution and sensitivity to contrast in peripheral vision [29–32]. A spatial attention defect could in fact explain both fine perception deficits and visuomotor inaccuracy in peripheral vision (visual-manual, i.e. field effect and saccadic errors [33,34]).
This deficit in an effective orientation of attention towards the contralesional visual field (‘‘ataxic’’) in patients presenting with unilateral optic ataxia was validated by specific attention paradigms such as facilitation via spatial cueing to influence the speed of stimulus processing (Posner paradigm [35] applied to patients with a lesion of the intraparietal sulcus and the superior parietal lobule [16,19], see Fig. 5 image on the left) or the identification of a flashed letter in peripheral vision [17,18]. This matches with the functional neuroimaging data that showed that the superior parietal lobule and the intraparietal sulcus constituted the neural substrate of the ‘‘dorsal attention network’’ (DAN) voluntarily orienting the attention
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Fig. 4. Percentage of correct perception of change occurrence (forced choice verbal response: ‘‘change’’/‘‘no change’’) in stimulus shape, size, orientation or location (tested in blocked conditions), with stimulus presented in central or peripheral vision (tested in blocked conditions), in patient IG with bilateral optic ataxia and in an age-matched healthy control.
towards the peripheral vision, in the space contralateral to the activated hemisphere [15]. Note that in their study researching the neural substrates involved in the Posner paradigm [35], Corbetta et al. [15] also showed the existence of a ‘‘ventral attention network’’ (VAN) [37] involving the inferior parietal lobule of the right hemisphere. The VAN was activated when the targets to be detected did not appear on the cued side, and this regardless of the side (invalid cueing conditions). In other words, since the VAN was activated when the target appeared in the entire visual field, but outside of the ongoing attentional focus, it was activated when the patients had to disengage attention from a current location. Performance of hemineglect patients to this paradigm [36] showed a strong disengagement of attention deficit since their reaction time was slower in the two invalid cueing conditions (Fig. 5, image on the left: unilateral spatial neglect). This invalidity effect was interacting with the rightward attention bias of the patients. Patients with unilateral optic ataxia did not present with this disengagement of attention deficit but a simple right-left asymmetry in valid as well as in invalid cueing conditions (Fig. 5, image on the right side: optic ataxia). Thus, both optic ataxia and hemineglect patients show an engagement of attention deficit towards the contralesional space. The engagement of attention deficit may thus be caused by a functional impairment of the DAN (superior parietal lobule and intraparietal sulcus). In patients with hemineglect, the DAN would be affected either directly by a large lesion in the right hemisphere, or indirectly by under
activation of the DAN induced by the lesion to the VAN in the same right hemisphere as demonstrated by Corbetta et al. [38]. Following damage to the VAN, hemineglect patients thus exhibit additional deficits of disengagement, visuospatial working memory (Pisella et al. [in this issue]), sometimes executive control, aggravating the consequences of the contralesional engagement of attention deficit (towards the left side). Conclusion If, as we are supposing, these two effects (hand and field effects) are dissociated on an anatomical-functional level, then we are faced with a clinical context associating two symptoms of a different nature and could in fact have a dissociated clinical presentation. One could be able to observe in ataxic patients, the absence of hand effect but the presence of an attentional disorder for the contralesional field affecting the actions directed towards the objects presented in that field but also the localization and fine perception in peripheral vision in this space (subclinical neglect). Other ataxic patients would be free of the field effect, with an ocular-centered localization disorder of the contralesional hand, based on proprioception, easily evidenced by errors when the contralesional hand is directed towards the target in the entire space, even in central vision. Disclosure of interest The authors declare that they have no competing interest. References
Fig. 5. Reaction time (in ms) to targets presented in the ipsilesional (ipsi) or the contralesional (contra) visual fields, after a congruent central cueing (valid) or an incongruent central cueing (invalid) in patients with unilateral spatial neglect (NSU) and patients with unilateral optic ataxia (OA) separately.
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Optic ataxia in Ba´lint-Holmes syndrome§ L. Pisella *, Y. Rossetti, G. Rode INSERM U1028 CNRS UMR 5292, ImpAct Team, Lyon Neuroscience Research Center (CRNL), 16, avenue du Doyen-Le´pine, 69676 Bron cedex, France
A R T I C L E I N F O
A B S T R A C T
Article history: Received 25 November 2015 Accepted 5 December 2015
The objective of this review is to reinstate the diversity of visual perception and visuomotor symptoms following lesions to the posterior parietal cortex (dorsal visual stream). This diversity was overshadowed for a long time and shows the contribution of the dorsal visual stream not only to action but also to perception. More precisely, we propose that the visuomotor deficit in optic ataxia stems from two distinct components: visual proprioceptive deficit (hand effect) and visual attentional deficit (field effect) also affecting the perception in peripheral vision. ß 2016 Elsevier Masson SAS. All rights reserved.
Keywords: Optic ataxia Posterior parietal cortex Dorsal attentional network
1. Introduction The issue of relationships between perception and action plays a key role in several exploration fields related to upper functions of the body, such as Philosophy, Human Sciences or Neurosciences. Neuroanatomy suggested the existence of several visual pathways connecting the retina to the cortex. Experiments conducted on monkeys showed the existence of two divergent visual pathways corresponding to two different functions: the processing of the ‘‘where’’ and ‘‘what’’. One of these pathways, the occipito-temporal or ventral stream, links the prestriate areas to the inferior temporal cortex. A lesion in the inferior temporal cortex abolishes the visual discrimination of objects without affecting the perception of spatial relationships between the objects themselves (relative positions). The other occipito-parietal pathway or dorsal stream reaches the posterior parietal cortex. A lesion in the posterior parietal cortex is responsible in monkeys of spatial disorientation characterized by a deficit in the perception of relative positions [1] and localization of objects during targeted actions [2]. In humans, the behavioral effects of neurological damage involving a limited part of the posterior parietal cortex were analyzed in this theoretical context [3,4]. Patients presented with difficulties in directing their actions towards objects positioned in their peripheral visual field, even though they did not have any difficulties in recognizing these objects. This neurological deficit called optic ataxia is observed after damage to the dorsal stream. The reverse dissociation was observed in patients with bilateral
§
This work was supported by the Labex ANR-11-LABX-0042. * Corresponding author. E-mail address: [email protected] (L. Pisella).
damage to the occipito-temporal cortex who showed visual agnosia [5]: patient DF could not recognize the size, shape or orientation of the objects, whether her response was verbal or indicated by a matching motor task. However, when she needed to reach objects with a natural grasping gesture, her maximal grip aperture, measured during movement, was correlated with the size of the object. These observations suggest that during her action she could process visual information on the objects metric properties that she could not consciously perceive. The confrontation of these results with those obtained in patients with optic ataxia, suggests that deficits in the visual recognition of objects and directed action can be clearly dissociated. Optic ataxia and visual agnosia were considered for a long time as the two components of a dorsal-ventral differentiation, which could in reality correspond to a dissociation between the perception of the ‘‘what’’ and the organization of the ‘‘how’’ when directing an action [6,7] rather than the dissociation proposed within the perception field [1] for processing the various properties of objects (‘‘where’’ vs. ‘‘what’’). To simplify, the parietal posterior cortex, with its associated optic ataxia deficit, was considered as the specific area for actions, leaving perception and visual consciousness to the occipitotemporal ventral stream. This dichotomous vision was proposed in a book [6] that had a major influence on neurosciences for a decade. However, in parallel, modern functional neuroimaging data evidenced a systematic activation of the parietal posterior cortex in all perception tasks performed without a motor response, and thus attributed it a major role in attentional phenomena. To reconcile these two views, one needs to refer to the first clinical descriptions of the consequences of parietal cortex damage (Ba´lint’s syndrome [8,9]) and modulate the truncated view of optic ataxia that was presented under the influence of the perception–action dissociation theory.
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2. Ba´lint’s syndrome
3. Optic ataxia
Symptoms following bilateral damage of the parietal posterior cortex (dorsal stream) were initially described by Ba´lint in 1909 [8] and 10 years later by Holmes using other terms [9]. The syndrome described by Ba´lint includes a triad of symptoms described as such:
Optic ataxia corresponds to the difficulty in performing gestures located in the contralesional visual field (field effect) and/or with the contralesional hand (hand effect), in the absence of primary visual, proprioceptive or motor disorders. These two effects are additive, which already implies that they are independent: the most severe errors are observed when the patient directs a movement with the ataxic hand towards the ataxic field, intermediate severe errors are observed when the patient directs the healthy hand towards the ataxic field and the ataxic hand towards the healthy visual field, movements performed with the healthy hand towards the healthy visual field are normal (Fig. 1-open-loop).
‘optische Ataxie’, imprecision of visually-guided movements characterized by spatial errors that were observed with the right hand (‘‘hand effect’’); ‘ra¨umliche Storung der Aufmerksamkeit’–lateralized attention deficit, it was described as attention being biased towards the right side of the extra-personal space, so left stimuli were neglected; ‘seelenla¨hmung des Schauens’–attention symptom different from the previous one described as an extreme restriction of visual attention, i.e. the inability of an individual to perceive more than a single object at a time (called ‘‘Simultanagnosia’’ later on in the literature) [10,11]). This third symptom was often referred as a ‘‘psychic paralysis of gaze’’ because it was described as a fixed gaze not stemming from oculomotor deficit but rather inattention for stimuli located in the peripheral visual field; In the description of the ‘‘disturbances of visual orientation’’ syndrome reported by Holmes [9,12] in World War I soldiers with bilateral parietal lesions, oculomotor disorders had a large impact: the author described a wandering gaze when visually looking for a target and difficulty in maintaining fixation. These disorganized eye movements (later on called ‘‘gaze ataxia’’ or ‘‘gaze apraxia’’ [13]) were associated with a complete inability to direct grasping movements (optic ataxia). Holmes considered that these visual-manual and oculomotor disorders were the consequence of a lower level impairment preventing to visually locate the targets. The major difference between the descriptions by Ba´lint [8] and Holmes [9] resides in their interpretation of visuomotor disorders. As a matter of fact for Ba´lint, oculomotor impairments are the consequences of attention disorders, and because of the ‘‘hand effect’’ observed in his patient, the optic ataxia could not simply be a vision-related disorder. In line with Ba´lint, following authors have defined optic ataxia following focal damage to the superior parietal lobule and the intraparietal sulcus as a specific disorder of the visual–manual processing of spatiotemporal object information (localization, but also orientation and size, all determining the exact gesture to grasp them), without comparable visual perception, attention or eye movement disorders [4,14]. However, this debate between visuospatial or purely visual-manual interpretation of ataxia has been refueled by neuroimaging that showed that the superior parietal lobule and intraparietal sulcus constituted the neural substrate of the ‘‘dorsal attention system’’ voluntary orienting the attention toward a location of interest in the peripheral vision [15]. In accordance with these neuroimaging data, attention deficits are systematically found when specifically screened in patients with unilateral [16–19] or bilateral optic ataxia [20]. In this chapter, we propose to explore these visual attention deficits and differentiate them from those in patients presenting with clinical hemispatial neglect. First, we will describe more precisely the combination of the two aspects of visualmanual deficits in optic ataxia: the hand effect, which prevented Ba´lint from concluding to a purely visual disorder that we view as a high-level spatiotemporal integration disorder for proprioceptive information; the field effect for which we are proposing an attentional-related interpretation.
3.1. Hand effect The hand effect prompted Ba´lint to dissociate optic ataxia from the other perception and attentional symptoms of the triad. Fig. 1 shows that this hand effect depends on the ability of patients to see their hand (closed-loop) or not (open-loop), since the effect is strongly reduced when patients can see their hand in the start position and during the movement, whereas this visual reafference does not significantly change errors made with the healthy hand in the contralesional field (i.e. the field effect errors). When there is no visual reafference for the hand position (in the open-loop condition), only proprioception can indicate this position. The resulting increased ‘‘hand effect’’ errors in the open-loop condition suggest that those are more severe when proprioceptive information are used to guide the action, and thus the hand effect is in fact a proprioceptive information processing deficit. To test this hypothesis, we had two patients with unilateral optic ataxia perform a proprioceptive pointing task [21]. Patients were in the dark and had to fixate at a fluorescent dot positioned in the frontal plane straight ahead of them. They had their arm placed under a board and the investigator positioned behind the board placed their hand on that frontal plane, on the right side or left side of their visual fixation point. They were instructed to use their other hand to point on the other side of the board where the hand was positioned by the investigator. Patients never received feedback on their performance regarding locating their hidden hand by pointing to it with their other hand. In a first experience, they had to point with their ataxic hand towards their healthy hand. We observed the combination of a field effect and hand effect equivalent to the pointing task of the ataxic hand towards the visual target illustrated in Fig. 1: errors from 3 to 5 cm occurred, and were more severe when the healthy hand (target) was positioned in the contralesional space. In a second experience (Fig. 2), patients had to point with their healthy hand towards their ataxic hand, positioned either in the left space or in the right space in regards to the visual fixation point. In a remarkable manner, we noted in this condition much wider errors, about 12 cm in average for the patient Can and 8 cm in average for the patient Ok, errors were slightly greater when the ataxic hand was positioned in the patient’s ataxic field. These errors were grossly directed towards the center of the board where the patient had to fixate the fluorescent dot, and were so severe that sometimes they could bring the patient Can to point to the ipsilesional field when the hand was presented in the ataxic field (Fig. 2. Middle images: positions where the ataxic hand was moved by the investigator are indicated by full squares [target positions], positions pointed by the patient with the healthy hand are indicated by circles and a motor error vector materialized the difference between these two positions). These considerable errors demonstrate that a major pathological element of optic ataxia is the inability to locate the ataxic hand when presented as a target in the extra-personal space. It is important to note that this disorder is not a primary proprioceptive disorder because this function remains intact as verified by the clinical
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Fig. 1. Pointing errors (in mm) exhibited by a unilateral optic ataxia patient when pointing with his contralesional or ipsilesional hand toward visual targets presented in his contralesional or ipsilesional visual field, with visual feedback of his hand (closed loop) or without (open loop). Errors made with the contralesional hand are significantly reduced when visual feedback of the hand is provided.
diagnosis of optic ataxia, and validated by asking the patient Can to reproduce with his healthy arm the position requested by the investigator, and vice versa, the patient completed the test with no difficulties (Fig. 2, lower images). It is in fact a high-level specific proprioceptive localization disorder, or in other terms a motorproprioceptive transformation for a directed movement, explaining the errors related to the hand effect, just like the field effect was evidenced as a high level visuomotor disorder for a directed movement [4]. 3.2. The field effect Field effect errors were also studied and represented in two dimensions via error vectors. Fig. 3 shows that these errors are similar to those of proprioceptive localization in Fig. 2, because they are also greater when the target is presented further from the visual fixation point and they are globally directed towards the gaze location, when the fixation point position is changed it affects the error vectors [21,22]. Our first observation reporting a deficit of peripheral vision detection in a patient with optic ataxia was in fact fortuitous. It was in the context of a task where we explored the visuomotor reaction of patients with optic ataxia, after allowing a delay for memorizing the target and at the time when the patients started the pointing gesture, the target could reappear in their peripheral vision but in a different position [23]. Results showed that in this condition controls directed their pointing movement towards the newly presented target, whereas patients started the movement towards the memorized previous target location and changed their pointing trajectory only during the movement towards the newly presented target (9 tests
out of 16 for patient AT and 13 tests out of 16 for patient IG). This visuomotor behavior backed up the arguments in favor of a deficit of visual information processing regarding real-time spatial localization in optic ataxia [24–27]. After the experiment, we asked the patients if they were aware that we sometimes moved the targets in their peripheral vision. Patient AT reported never having detected a change in position. Patient IG who spontaneously made some remarks regarding changes in the target position, accepted to do the experiment again, this time with a double task to point and tell us if the target had been moved or not. To our amazement, she produced a lot of false positives in her verbal response and sometimes performed trajectory corrections that took her hand further away from the targets really presented to her (corresponding to these false positives). This behavior showed that she did not always perceive the targets in her peripheral visual field when executing the movement! Finally, her perception performance to detect position changes in her peripheral vision appeared even more impaired than her visuomotor performance in reaction to these changes [23], whereas according to the model by Milner and Goodale [6] optic ataxia is an action-related deficit preserving perception. Furthermore, we explored in this patient and one age-matched control subject, the abilities to detect changes in peripheral and central vision for different visual characteristics. Her detection performance was similar to the control subject for the central vision. Regarding peripheral vision (at 208), her detection performance was greatly reduced, with an 80% decrease in performance for orientation changes, 70% for changes in size and 50% for changes in spatial location (Fig. 4 [28]). Her detection of shape changes was retained, probably because these were not metric attributes but rather categorical attributes of the object’s identity (e.g. Round, square,
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Fig. 2. Pointing errors (in mm) exhibited by two unilateral optic ataxia patients (Can and Ok) when pointing with their ipsilesional (non-ataxic) hand toward their contralesional (ataxic) hand presented in their contralesional or ipsilesional visual field in the dark (eyes were open and only a central fixation dot was visible). As illustrated by the error vectors drawn from the target positions (red squares) toward the corresponding endpoints (blue diamonds), the amplitude of the errors (length of the vectors) in this condition of proprioceptive pointing were very large, and larger when the ataxic hand was positioned in the contralesional hemifield. The pictures below show that the patient with eyes closed still could reproduce the posture of the ataxic arm with the ipilesional arm and vice versa, confirming that the deficit of proprioceptive pointing is not due to primary proprioceptive deficit.
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Fig. 3. Error vectors (see legend of Fig. 2) and 95% confidence ellipses (variability) of pointing made toward peripheral visual targets (red squares) while keeping their eyes on central fixation (cross) by healthy controls (top panel), patients with right hemisphere lesion (middle panel) and left hemisphere lesion (bottom panel), with their left hand (left column) and their right hand (right column) separately.
triangle). We conclude that the functional difference between ventral and dorsal pathways is better explained by the type of visual attribute processed (categorical vs. metric) and central vs. peripheral vision, than by a role dedicated to perception vs. action [28]. The relationship between these fine perception deficits in the peripheral vision and spatial attention deficit could be due to the fact that spatial attention is a process improving spatial resolution and sensitivity to contrast in peripheral vision [29–32]. A spatial attention defect could in fact explain both fine perception deficits and visuomotor inaccuracy in peripheral vision (visual-manual, i.e. field effect and saccadic errors [33,34]).
This deficit in an effective orientation of attention towards the contralesional visual field (‘‘ataxic’’) in patients presenting with unilateral optic ataxia was validated by specific attention paradigms such as facilitation via spatial cueing to influence the speed of stimulus processing (Posner paradigm [35] applied to patients with a lesion of the intraparietal sulcus and the superior parietal lobule [16,19], see Fig. 5 image on the left) or the identification of a flashed letter in peripheral vision [17,18]. This matches with the functional neuroimaging data that showed that the superior parietal lobule and the intraparietal sulcus constituted the neural substrate of the ‘‘dorsal attention network’’ (DAN) voluntarily orienting the attention
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Fig. 4. Percentage of correct perception of change occurrence (forced choice verbal response: ‘‘change’’/‘‘no change’’) in stimulus shape, size, orientation or location (tested in blocked conditions), with stimulus presented in central or peripheral vision (tested in blocked conditions), in patient IG with bilateral optic ataxia and in an age-matched healthy control.
towards the peripheral vision, in the space contralateral to the activated hemisphere [15]. Note that in their study researching the neural substrates involved in the Posner paradigm [35], Corbetta et al. [15] also showed the existence of a ‘‘ventral attention network’’ (VAN) [37] involving the inferior parietal lobule of the right hemisphere. The VAN was activated when the targets to be detected did not appear on the cued side, and this regardless of the side (invalid cueing conditions). In other words, since the VAN was activated when the target appeared in the entire visual field, but outside of the ongoing attentional focus, it was activated when the patients had to disengage attention from a current location. Performance of hemineglect patients to this paradigm [36] showed a strong disengagement of attention deficit since their reaction time was slower in the two invalid cueing conditions (Fig. 5, image on the left: unilateral spatial neglect). This invalidity effect was interacting with the rightward attention bias of the patients. Patients with unilateral optic ataxia did not present with this disengagement of attention deficit but a simple right-left asymmetry in valid as well as in invalid cueing conditions (Fig. 5, image on the right side: optic ataxia). Thus, both optic ataxia and hemineglect patients show an engagement of attention deficit towards the contralesional space. The engagement of attention deficit may thus be caused by a functional impairment of the DAN (superior parietal lobule and intraparietal sulcus). In patients with hemineglect, the DAN would be affected either directly by a large lesion in the right hemisphere, or indirectly by under
activation of the DAN induced by the lesion to the VAN in the same right hemisphere as demonstrated by Corbetta et al. [38]. Following damage to the VAN, hemineglect patients thus exhibit additional deficits of disengagement, visuospatial working memory (Pisella et al. [in this issue]), sometimes executive control, aggravating the consequences of the contralesional engagement of attention deficit (towards the left side). Conclusion If, as we are supposing, these two effects (hand and field effects) are dissociated on an anatomical-functional level, then we are faced with a clinical context associating two symptoms of a different nature and could in fact have a dissociated clinical presentation. One could be able to observe in ataxic patients, the absence of hand effect but the presence of an attentional disorder for the contralesional field affecting the actions directed towards the objects presented in that field but also the localization and fine perception in peripheral vision in this space (subclinical neglect). Other ataxic patients would be free of the field effect, with an ocular-centered localization disorder of the contralesional hand, based on proprioception, easily evidenced by errors when the contralesional hand is directed towards the target in the entire space, even in central vision. Disclosure of interest The authors declare that they have no competing interest. References
Fig. 5. Reaction time (in ms) to targets presented in the ipsilesional (ipsi) or the contralesional (contra) visual fields, after a congruent central cueing (valid) or an incongruent central cueing (invalid) in patients with unilateral spatial neglect (NSU) and patients with unilateral optic ataxia (OA) separately.
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