Visual Form Agnosia Research Articles

The Anatomy of Object Recognition—Visual Form Agnosia Caused by Medial Occipitotemporal Stroke

The influential model on visual information processing by Milner and Goodale (1995) has suggested a dissociation between action- and perception-related processing in a dorsal versus ventral stream projection. It was inspired substantially by the observation of a double dissociation of disturbed visual action versus perception in patients with optic ataxia on the one hand and patients with visual form agnosia (VFA) on the other. Unfortunately, almost all cases with VFA reported so far suffered from inhalational intoxication, the majority with carbon monoxide (CO). Since CO induces a diffuse and widespread pattern of neuronal and white matter damage throughout the whole brain, precise conclusions from these patients with VFA on the selective role of ventral stream structures for shape and orientation perception were difficult. Here, we report patient J.S., who demonstrated VFA after a well circumscribed brain lesion due to stroke etiology. Like the famous patient D.F. with VFA after CO intoxication studied by Milner, Goodale, and coworkers (Goodale et al., 1991, 1994; Milner et al., 1991; Servos et al., 1995; Mon-Williams et al., 2001a,b; Wann et al., 2001; Westwood et al., 2002; McIntosh et al., 2004; Schenk and Milner, 2006), J.S. showed an obvious dissociation between disturbed visual perception of shape and orientation information on the one side and preserved visuomotor abilities based on the same information on the other. In both hemispheres, damage primarily affected the fusiform and the lingual gyri as well as the adjacent posterior cingulate gyrus. We conclude that these medial structures of the ventral occipitotemporal cortex are integral for the normal flow of shape and of contour information into the ventral stream system allowing to recognize objects.

Brain activation during immediate and delayed reaching in optic ataxia

Patients with optic ataxia after lesions of the occipito-parietal cortex demonstrate gross deviations of movements to visual targets in their peripheral visual field. When the same patients point to remembered target locations their accuracy improves considerably. Taking into account opposite findings in a single patient suffering from visual form agnosia due to bilateral occipito-temporal lesions (D.F.), this paradoxical improvement was attributed to brain structures outside the dorsal stream, and supposed to be specifically associated with delayed movement execution. This conclusion was based on the still unverified assumption that the dorsal system is almost completely lacking any localization function in patients with optic ataxia who demonstrate the paradoxical delay effect. We thus investigated brain activity associated with immediately executed and delayed movements in a patient with optic ataxia due to extensive bilateral lesions (I.G.) and in 16 healthy subjects using functional magnetic resonance imaging. Our analysis revealed robust and indistinguishable activation of intact dorsal occipital and parietal areas adjacent to the patient's lesions for both types of movements. In healthy subjects, we found the same visuomotor network activated during immediate and delayed movements as well as additionally higher signal increases for movements to visible targets than for delayed movements in bilateral occipito-parietal and occipito-temporal areas. Our results suggest that in healthy subjects as well as in the optic ataxia patient I.G. dorsal areas are not only involved in immediate but also in delayed reaching. This observation questions the hypothesis that residual visuospatial abilities in patients with optic ataxia could only be mediated by a system outside of the dorsal stream.

Hémianopsie latérale homonyme et atrophie corticale postérieure

Introduction Posterior cortical atrophy (PCA) is a clinically and radiologically defined syndrome, in which predominant symptoms focus on higher visual dysfunction with progressive course and association with cortical atrophy or hypometabolism that predominates in the posterior part of the hemispheres. Homonymous hemianopia (HH) has rarely been described in this syndrome. Methods We report on six patients (four females, two males, aged 63 to 80) referred for visual disorder which led to demonstration of HH using perimetry testing. These patients were followed for 1 to 5 years after discovery of HH. Brain imaging with MRI or CT scan was obtained in the six cases and a SPECT scan was performed in four cases. Results HH was left-sided in four cases and right-sided in two cases. Associated symptoms related to higher visual dysfunction were simultagnosia, alone or as part of a full Balint's syndrome, alexia, constructional apraxia, dressing apraxia, visual form agnosia, prosopagnosia and hemispatial neglect. These symptoms were mild at onset but invariably worsened with disease progression. Dementia eventually developed in all cases. The clinical diagnosis was probable Alzheimer's disease in five cases and corticobasal degeneration in one case. Radiology showed posterior cortex atrophy in all cases as well as reduced cerebral blood flow in the same region, with an asymmetrical pattern compatible with the side of HH. Conclusion Elementary cortical lesions in PCA can develop mainly in the associative visual areas and even in the primary visual area, resulting in HH. HH has rarely been documented in PCA, but its prevalence would probably be higher if systematic search was conducted. Apparently isolated HH of insidious onset should suggest PCA and lead to neuropsychological testing and search for discrete atrophic changes of the posterior cortex on MRI as well as for metabolic alterations with SPECT or PET.

Object-based attention and visual area LO

We investigated the neural basis of so-called “object-based attention” by examining patient D.F., who has visual form agnosia caused by bilateral damage to the lateral occipital (LO) area of the ventral visual stream. We tested D.F.’s object-based attention in two ways. In the first experiment, we used a spatial cueing procedure to compare the costs associated with shifting attention within versus between two separate outline figures. D.F. did not show the normal advantage of within-object over between-object attention shifts. In the second experiment, we used a complementary paradigm in which two separate stimuli, presented either on the same or on different objects, have to be identified as the same or different, We found no evidence for the normal pattern of superior performance for within versus between figure comparisons. In a third experiment, we checked that D.F. showed normal shift costs for invalid as opposed to valid cueing in a standard Posner spatial attention task. In a final experiment, we compared horizontal versus vertical attention shifting in group of healthy controls without the presence of outline rectangles, and found that their pattern of shift costs was indistinguishable from that seen in D.F. when the rectangles were present (Experiment 1). We conclude that whilst D.F. has a normal spatial orienting system this is completely uninfluenced by object structure. We suggest that area LO may mediate form processing precisely at the stage where visual representations normally influence the spread of attention.

Potentiation of action by undetected affordant objects

The physical attributes of objects that are relevant to motor behaviour, or action, are referred to as affordances (Gibson, 1979). Recent evidence has shown that an object's affordance can potentiate an unrelated motor response even when there is no intention to respond to it (e.g., Tucker & Ellis, 1998). In the five experiments, we examined whether conscious perception of an affordance is necessary to produce motor priming by presenting images of affordant objects (e.g., hammer) under conditions which cause them to be undetectable: Brief masked exposure (BME) and attentional blink (AB). We successfully demonstrated that conscious perception is not necessary for an object's affordance to produce motor priming. Since these findings are consistent with the abilities/disabilities of patients with blindsight and visual form agnosia, it is possible that processing accomplished by the dorsal stream produced this effect, though more research is needed to confirm this assertion.

Missing in action: the effect of obstacle position and size on avoidance while reaching

When reaching to objects, our hand and arm rarely collide with non-target objects, even if our workspace is cluttered. The simplicity of these actions hides what must be a relatively sophisticated obstacle avoidance system. Recent studies on patients with optic ataxia and visual form agnosia have demonstrated that obstacle avoidance is an automatic process, likely governed by the dorsal stream (Schindler et al. 2004; Rice et al. 2006). The current study sought to quantify how normal participants react to changes in the size and position of non-target objects in and around their workspace. In the first experiment, 13 right-handed subjects performed reaches to a target strip in the presence of two non-target objects, which varied in depth and horizontal configuration. We found that objects with horizontal alignments that were asymmetric about midline created systematic deviations in reach trajectory away from midline, with participants seeming to maximize the distance away from the two objects. These deviations were significantly greater for objects nearer in depth and nearly disappeared when the objects were placed beyond the target strip. Accompanying this pattern of deviation were other significant obstructing effects whereby reaches were executed more slowly when objects were close in depth and close to the participants reaching (right) hand. In the second experiment, we varied the height of the two objects, as well as the depth. Object pairs were now both tall, both short, or one-short/one-tall. We replicated the significant depth effects of the first experiment, extending the finding to include sensitivity to the size of the objects. Here the obstructing effect caused by short objects was similar to tall objects when those objects were placed at the depth of the reach target, but less than the tall objects when placed at mid-reach. Taken together, these experiments suggest that humans possess a sophisticated obstacle avoidance system that is extremely sensitive and conservative in evaluating potential obstacles and adjusting the reach accordingly.

Illusions, perception, and action: Where are we now?

Patient DF, an extensively-tested woman with visual form agnosia from ventral-stream damage, is able to scale her grip aperture to match a goal object's geometry when reaching out to pick it up, despite being unable to explicitly distinguish amongst objects on the basis of their different geometries. Using evidence from a range of sources, including functional MRI, we have proposed that she does this through a functionally intact visuomotor system housed within the dorsal stream of the posterior parietal lobe. More recently, however, Schenk (2012a). The Journal of Neuroscience, 32(6), 2013–2017; Schenk (2012b). Trends in Cognitive Sciences, 16(5), 258–259. has argued that DF performs well in visually guided grasping, not through spared and functioning visuomotor networks in the dorsal stream, but because haptic feedback about the locations of the edges of the target is available to calibrate her grasps in such tasks, whereas it is not available in standard visual perceptual tasks. We have tested this 'calibration hypothesis' directly, by presenting DF with a grasping task in which the visible width of a target varied from trial to trial while its actual width remained the same. According to the calibration hypothesis, because haptic feedback was completely uninformative, DF should be unable to calibrate her grip aperture in this task. Contrary to this prediction, we found that DF continued to scale her grip aperture to the visual width of the targets and did so well within the range of healthy controls. We also found that DF's inability to distinguish shapes perceptually is not improved by providing haptic feedback. These findings strengthen the notion that DF’s spared visuomotor abilities are driven largely by visual feedforward processing of the geometric properties of the target. Crucially, these findings also indicate that simple tactile contact with an object is needed for the visuomotor dorsal stream to be engaged, and accordingly enables DF to execute visually guided grasping successfully. This need for actions to have a tangible endpoint provides an important new modification of the Two Visual Systems theory.

Exaggerated Color Perception in a Patient with Visual Form Agnosia

Previous studies on visual form agnosic patients have shown that their color perception is relatively preserved when monochromatic figures are used. However, it is unclear whether their color perception remains normal when figures are composed of two parts in different colors. The results showed that patient X.F. had difficulty in naming both colors when the two colors were placed next to each other, and in discriminating the two-color figure from the figure presented in its larger color. In contrast, X.F. could name the two colors when they were physically separated. These data suggest that X.F. manifests exaggerated color perception, producing a color filling-in effect that may be mediated by her spared early visual area.

Visuomotor system uses target features unavailable to conscious awareness

After lesions to primary visual cortex, patients lack conscious awareness of visual stimuli. Interestingly, however, some retain the ability to make accurate judgments about the visual world (i.e., so-called blindsight). Similarly, damage to inferior occipitotemporal regions of cortex (e.g., lateral occipital cortex) can result in an inability to perceive object properties while retaining the ability to act on them (i.e., visual form agnosia). In the present work, we demonstrate that the ability to interact with objects in the absence of conscious awareness is not isolated to those with restricted neuropathologic conditions. Specifically, neurologically intact individuals are able to program and execute goal-directed reaching movements to a target object without awareness of extrinsic target properties; they accurately tune the dynamics of their movement and modulate it online without conscious access to features of the goal object. Thus, the planning and execution of actions are not dependent on conscious awareness of the environment, suggesting that the phenomenon of blindsight (and agnosia) reflect normal conditions of the visual system.

Concurrent visuomotor behaviour improves form discrimination in a patient with visual form agnosia

It is now well established that the visual brain is divided into two visual streams, the ventral and the dorsal stream. Milner and Goodale have suggested that the ventral stream is dedicated for processing vision for perception and the dorsal stream vision for action [A.D. Milner & M.A. Goodale (1995) The Visual Brain in Action, Oxford University Press, Oxford]. However, it is possible that ongoing processes in the visuomotor stream will nevertheless have an effect on perceptual processes. This possibility was examined in the present study. We have examined the visual form-discrimination performance of the form-agnosic patient D.F. with and without a concurrent visuomotor task, and found that her performance was significantly improved in the former condition. This suggests that the visuomotor behaviour provides cues that enhance her ability to recognize the form of the target object. In control experiments we have ruled out proprioceptive and efferent cues, and therefore propose that D.F. can, to a significant degree, access the object's visuomotor representation in the dorsal stream. Moreover, we show that the grasping-induced perceptual improvement disappears if the target objects only differ with respect to their shape but not their width. This suggests that shape information per se is not used for this grasping task.

Intact automatic avoidance of obstacles in patients with visual form agnosia

In everyday life our reaching behaviour has to be guided not only by the location and properties of the target object, but also by the presence of potential obstacles in the workspace. Recent evidence from neglect and optic ataxia patients has suggested that this automatic obstacle avoidance is mediated by the dorsal, rather than the ventral, stream of visual processing. We tested this idea in two studies involving patients with visual form agnosia resulting from bilateral ventral-stream damage. In the first study, we asked patient DF to reach out and pick up a target object in the presence of obstacles placed at varying distances to the left or right of the target. We found that both DF and controls shifted their trajectories away from the potential obstacles and adjusted their grip aperture in such a way as to minimize risk of collision. In a second study, we asked DF and a second patient, SB, to either reach between, or to bisect the space between, two cylinders presented at varying locations. We found that both patients adjusted their reach trajectories to account for shifts in cylinder location in the reaching task, despite showing significantly worse performance than control subjects when asked to make a bisection judgement. Taken together, these data indicate that automatic obstacle avoidance behaviour is spared in our patients with visual form agnosia. We attribute their ability to the functional intactness of the dorsal stream of visual processing, and argue that the ventral stream plays no important role in automatic obstacle avoidance.

Preservation of Emmert's Law in a Visual Form Agnosic

Size constancy was investigated in DF, a patient with visual form agnosia, using a technique based on Emmert's law of visual after-images. DF was first given a task in which she was asked to indicate the distance of a vertical surface and a task where she had to estimate the width of a series of squares (widths ranging from 5 cm to 35 cm) placed at varying distances and having a constant visual angle. In the distance estimation task, DF greatly overestimated the distance of the vertical surface placed in front of her. DF also had great difficulty performing the size estimation task. DF then performed a task in which she stared at a bright 5 cm square for a brief period of time at a distance of 30 cm followed by the presentation of a vertical surface which varied in distance and was asked to indicate the width of the after-image either verbally or manually. DF's after-images conformed to the size-distance relationship predicted by Emmert's law—as the distance of the vertical surface increased her perception of the size of the after-images also increased. These data demonstrate that although DF is rather impaired in tasks that require explicit estimates of size and distance, at some level, DF must have relatively intact size constancy mechanisms given that her estimates of the width of the after-image conform to Emmert's law. Thus, the processes underlying explicit judgements of size and distance appear to differ from those underlying the size and distance scaling of after-images. I thank Mel Goodale for allowing me to conduct this research in his laboratory at the University of Western Ontario. This work was supported by CIHR (MG) and NSERC (PS) grants. This work was also supported by the Canada Research Chairs program (PS).

Pointing to places and spaces in a patient with visual form agnosia

Previous investigations of visuospatial abilities in the visual form agnosic patient D.F. suggest that her egocentric sensorimotor processing is intact while her ‘allocentric’ judgments of spatial position are impaired. The current investigation extends these previous observations by comparing D.F.'s performance at pointing to a set of spatially distributed stimuli, either directly or by ‘pantomiming’ the responses in an adjacent homologous workspace. The results showed accurate sensorimotor localization when D.F. pointed directly to single targets or to sequences of targets, presumably as she could use egocentric visual coding. In spite of making relatively spared spatial judgments about the arrays, however, D.F. performed quite poorly when copying them and on the pantomimed pointing task. In this latter task good performance presumably depends on an ability to represent both the categorical and coordinate properties of the array (as does copying them), and to translate these into the effector-based coordinates required for accurate action. D.F.'s pantomimed pointing was similar to her copies of target arrays, as in both tasks there was evidence of spared (although somewhat degraded) appreciation of the relative spatial positions of the stimuli. Remarkably, her accuracy in this allocentric task was not worsened by longer pointing sequences. It is possible that D.F.'s degraded performance reflects a relative (though not complete) preservation of categorical coding within the ventral stream, despite a loss of coordinate coding there.

Preserved implicit form perception and orientation adaptation in visual form agnosia

Visual form agnosia is mainly characterized by profound deficits in visual form and shape discrimination. Previous studies have shown that patients retain the capacity for coordinated motor behaviors, color naming and implicit letter perception. However, it is unknown to what extent other visual functions, such as implicit form and orientation perception, are preserved. To address these questions, we investigated a single visual form agnosic patient, X.F., in two distinct experiments. X.F.'s visual lesions were mainly localized in the bilateral occipitotemporal cortex, with the dorsal visual stream and early visual cortex largely spared. In Experiment 1, X.F. named the color of different forms across 12 blocks of trials. After the first six blocks, the combinations of a form with its color were changed and the new combination was presented for the remaining six blocks. X.F.'s reaction time increased during the switch block and was significantly greater than the overall RT changes between adjacent, non-switch blocks. This indicates that X.F. retained the ability to perceive changes in form despite her inability to discriminate the forms. In Experiment 2, X.F. showed selective orientation adaptation effects to different spatial frequencies; that is, her contrast threshold was significantly higher when the adapting and test orientations were the same than when they were orthogonal, although her orientation discrimination performance was severely impaired. These data provide evidence of a functional dissociation between explicit and implicit visual abilities, and suggest that the residual early visual cortex mediates form and orientation processing in the absence of awareness.

The fusiform face area is not sufficient for face recognition: Evidence from a patient with dense prosopagnosia and no occipital face area

We tested functional activation for faces in patient D.F., who following acquired brain damage has a profound deficit in object recognition based on form (visual form agnosia) and also prosopagnosia that is undocumented to date. Functional imaging demonstrated that like our control observers, D.F. shows significantly more activation when passively viewing face compared to scene images in an area that is consistent with the fusiform face area (FFA) ( p < 0.01). Control observers also show occipital face area (OFA) activation; however, whereas D.F.'s lesions appear to overlap the OFA bilaterally. We asked, given that D.F. shows FFA activation for faces, to what extent is she able to recognize faces? D.F. demonstrated a severe impairment in higher level face processing—she could not recognize face identity, gender or emotional expression. In contrast, she performed relatively normally on many face categorization tasks. D.F. can differentiate faces from non-faces given sufficient texture information and processing time, and she can do this is independent of color and illumination information. D.F. can use configural information for categorizing faces when they are presented in an upright but not a sideways orientation and given that she also cannot discriminate half-faces she may rely on a spatially symmetric feature arrangement. Faces appear to be a unique category, which she can classify even when she has no advance knowledge that she will be shown face images. Together, these imaging and behavioral data support the importance of the integrity of a complex network of regions for face identification, including more than just the FFA—in particular the OFA, a region believed to be associated with low-level processing.

Differential Impact of Parvocellular and Magnocellular Pathways on Visual Impairment in Apperceptive Agnosia?

The term “visual form agnosia” describes a disorder characterized by problems recognizing objects, poor copying, and distinguishing between simple geometric shapes despite normal intellectual abilities. Visual agnosia has been interpreted as a disorder of the magnocellular visual system, caused by an inability to separate figure from ground by sampling information from extended regions of space and to integrate it with fine-grain local information. However, this interpretation has hardly been tested with neuropsychological or functional brain imaging methods, mainly because the magnocellular and parvocellular structures are highly interconnected in the visual system. We studied a patient (AM) who had suffered a sudden heart arrest, causing hypoxic brain damage. He was/is severely agnosic, as apparent in both the Birmingham Object Recognition Battery and the Visual Object and Space Battery. First- and especially second-order motion perception was also impaired, but AM experienced no problems in grasping and navigating through space. The patient revealed a normal P100 in visual evoked potentials both with colored and fine-grained achromatic checkerboards. But the amplitude of the P100 was clearly decreased if a coarse achromatic checkerboard was presented. The physiological and neuropsychological findings indicate that AM experienced problems integrating information over extended regions of space and in detecting second-order motion. This may be interpreted as a disorder of the magnocellular system, with intact parvocellular system and therefore preserved ability to detect both local features and colors.

Grasping What is Graspable: Evidence from Visual form Agnosia

Patient DF has profound visual form agnosia. Despite this, she has no problem adjusting her finger-thumb grip aperture to the width of objects when reaching to grasp them. In a previous study, however, she was found to have great difficulty in scaling her grip aperture when attempting to grasp a transparent disc through two holes cut into it. This problem was attributed to a putative difference between the visual processing of size and distance in the brain, whereby DF retained the capacity for processing object size but not the separation between distinct elements such as holes. In the present study we have tested this idea more directly, and found no evidence to support such a distinction. Nonetheless, we replicated our earlier finding that DF is unable to produce normal prehension movements when attempting to grasp transparent stimuli by placing her digits into holes. We suggest that, whilst some simple objects offer themselves directly to the dorsal stream for grasping, an intact ventral stream is required to respond appropriately to more complex stimuli.

Covert processing of visual form in the absence of area LO

The patient D.F., who suffers from severe visual form agnosia, has been found to have a bilateral lesion of area LO, an area known to be intimately involved in the perception of object shape. Despite her perceptual impairment, however, D.F. retains residual form processing abilities that can provide distal visuomotor control, for example in the configuration of her grasp when reaching to pick up objects of different shapes and sizes. This dissociation has been interpreted as reflecting the sparing of a dedicated system for processing the physical properties of objects solely for purposes of guiding action. Here we test this hypothesis in two studies designed to examine whether or not spared shape processing capacities might be revealed under other kinds of indirect test conditions. First, we exploited the fact that a redundant shape cue will speed search for a coloured stimulus within an array, and vice versa. Unlike our control subjects, D.F. showed no facilitation effect of either kind. Second, we used two Stroop tasks in which single coloured uppercase letters were presented. Our intention was to determine (a) whether naming the colour would be influenced by whether the letter was the initial letter of the correct or incorrect colour name (e.g. ‘R’ or ‘G’); and (b) whether the reverse might be true, that is that D.F.’s guesses at letter identity might be influenced by their colour. We found no evidence for a Stroop effect of the former (standard) kind in D.F., but we did find evidence for reverse-Stroop effects. This result may reflect a partial sparing of ventral stream areas specialised for letter-form processing.

Dynamic visual speech perception in a patient with visual form agnosia.

To examine the role of dynamic cues in visual speech perception, a patient with visual form agnosia (DF) was tested with a set of static and dynamic visual displays of three vowels. Five conditions were tested: (1) auditory only which provided only vocal pitch information, (2) dynamic visual only, (3) dynamic audiovisual with vocal pitch information, (4) dynamic audiovisual with full voice information and (5) static visual only images of postures during vowel production. DF showed normal performance in all conditions except the static visual only condition in which she scored at chance. Control subjects scored close to ceiling in this condition. The results suggest that spatiotemporal signatures for objects and events are processed separately from static form cues.

Dissociating ‘what’ and ‘how’ in visual form agnosia: a computational investigation

Patients with visual form agnosia exhibit a profound impairment in shape perception (what an object is) coupled with intact visuomotor functions (how to act on an object), demonstrating a dissociation between visual perception and action. How can these patients act on objects that they cannot perceive? Although two explanations of this ‘what–how’ dissociation have been offered, each explanation has shortcomings. A ‘pathway information’ account of the ‘what–how’ dissociation is presented in this paper. This account hypothesizes that ‘where’ and ‘how’ tasks require less information than ‘what’ tasks, thereby allowing ‘where/how’ to remain relatively spared in the face of neurological damage. Simulations with a neural network model test the predictions of the pathway information account. Following damage to an input layer common to the ‘what’ and ‘where/how’ pathways, the model performs object identification more poorly than spatial localization. Thus, the model offers a parsimonious explanation of differential ‘what–how’ performance in visual form agnosia. The simulation results are discussed in terms of their implications for visual form agnosia and other neuropsychological syndromes.