Visual object agnosia without prosopagnosia or alexia: Evidence for hierarchical theories of visual recognition

Abstract

A single case study is presented of a patient, Mr. W, with a selective deficit in recognizing pictures and real objects, linked to impaired stored visual knowledge about objects. Despite this, Mr. W maintained a preserved ability both to read aloud printed words and to recognize famous faces, when compared with age-matched control subjects. In addition, his access to semantic information from words was superior to that from pictures. The data provide evidence that visual agnosia can occur without alexia or prosopagnosia, contrary to recent proposals (Farah 1990, 1991). This finding is consistent with a hierarchical model of visual object recognition in which agnosia can reflect impaired stored knowledge of objects without accompanying perceptual deficits. The selective recognition deficit for objects further indicates that stored knowledge concerning different classes of visual stimuli (common objects, faces, and words) is separately represented in the brain.     

Visual Object Agnosia without Alexia or Prosopagnosia: Arguments for Separate Knowledge Stores

We review the points raised by Farah (this issue) in her discussion of the paper by Rumiati, Humphreys, Riddoch, and Bateman (1994), in which a case study was presented of a patient, Mr W., with visual object agnosia without either prosopagnosia or alexia. We reiterate the argument that Mr W. had impaired stored knowledge about the visual characteristics of objects, and that this was more severe than his deficit at a semantic level. In addition, we summarize supporting evidence from another patient (Humphreys & Rumiati, submitted), who showed the same pattern of breakdown as Mr W. We suggest that stored visual knowledge can be specific to the form of stimulus (words, objects, and faces), that these different forms of knowledge may be represented in distinct neural areas, and that agnosia can result after damage to stimulus-specific sites of knowledge representation.     

Optic aphasia, optic apraxia, and loss of dreaming

A 47-year-old man with a left temporo-occipital infarct in the area of the posterior cerebral artery is presented. The neuropsychological examination did not reveal aphasia or gross mental deficits. The patient presented with alexia without agraphia, color agnosia, but few visual perceptual deficits. The main impairment was in confrontation naming; he was incapable of naming objects and pictures, not from lack of recognition (excluding visual agnosia) but from lack of access to the appropriate word (optic aphasia). The patient also exhibited a deficit in the evocation of gesture from the visual presentation of an object (optic apraxia) and a difficulty in "conjuring up" visual images of objects (impaired visual imagery) and loss of dreams. The fundamental deficit of this patient is tentatively explained in terms of visuoverbal and visuogestural disconnection and a deficit of mental imagery.     

Prosopagnosia: a defect in visual configural processing

A patient with severe, lasting prosopagnosia could not get an immediate overview of a face sufficiently specific for successful identification. He also failed completely in tasks of visual closure despite adequate performances on numerous other tests of visual perception and memory. We conclude that prosopagnosia represents a loss of visual "configural processing"--a learned skill enabling immediate identification of individual members of a class without conscious visuospatial analysis or remembering. Prosopagnosia and agnosic alexia represent two distinct defects of configural processing: Alexics cannot identify items with distinctive features that are themselves identifiable. Prosopagnosics cannot identify objects whose critical distinguishing features have no independent identities.     

Object Recognition Difficulty in Visual Apperceptive Agnosia

Two patients with visual apperceptive agnosia were examined on tasks assessing the appreciation of visual material. Elementary visual functioning was relatively preserved, but they had profound difficulty recognizing and naming line drawings. More detailed evaluation revealed accurate recognition of regular geometric shapes and colors, but performance deteriorated when the shapes were made more complex visually, when multiple-choice arrays contained larger numbers of simple targets and foils, and when a mental manipulation such as a rotation was required. The recognition of letters and words was similarly compromised. Naming, recognition, and anomaly judgments of colored pictures and real objects were more accurate than similar decisions involving black-and-white line drawings. Visual imagery for shapes, letters, and objects appeared to be more accurate than visual perception of the same materials. We hypothesize that object recognition difficulty in visual apperceptive agnosia is due to two related factors: the impaired appreciation of the visual perceptual features that constitute objects, and a limitation in the cognitive resources that are available for processing demanding material within the visual modality.     

Damasio's error – Prosopagnosia with intact within‐category object recognition

The sudden inability to recognize individual faces following brain damage was first reported in a scientific journal 150 years ago and termed ‘prosopagnosia’ 70 years ago. While the term originally identified a face‐selective neurological condition, it is now obscured by a sequence of imprecisions. First, prosopagnosia is routinely used to define symptoms of individual face recognition (IFR) difficulties in the context of visual object agnosia or other neurological conditions, or even in the normal population. Second, this over‐expansive definition has lent support to a long‐standing within‐category recognition account of prosopagnosia, that is, that the impairment of IFR reflects a general impairment in recognizing within‐category objects. However, stringent experimental studies of classical cases of prosopagnosia following brain damage show that their core impairment is not in recognizing physically similar exemplars within non‐face object categories. Instead, the impairment presents specifically for recognizing exemplars of the category of faces. Moreover, compared to typical observers, the impairment appears even more severe for recognizing individual faces against physically dissimilar than similar distractors. Here, I argue that we need to limit accordingly our definition of prosopagnosia to a clinical (i.e., neurological) condition in which there is no basic‐level object recognition impairment. Other criteria for prosopagnosia are proposed, with the hope that this conservative definition enables the study of human IFR processes in isolation, and supports progress in understanding the nature of these processes.     

The role of sensory-motor information in object recognition: evidence from category-specific visual agnosia

The role of sensory-motor representations in object recognition was investigated in experiments involving AD, a patient with mild visual agnosia who was impaired in the recognition of visually presented living as compared to non-living entities. AD named visually presented items for which sensory-motor information was available significantly more reliably than items for which such information was not available; this was true when all items were non-living. Naming of objects from their associated sound was normal. These data suggest that both information about object form computed in the ventral visual system as well as sensory-motor information specifying the manner of manipulation contribute to object recognition.     

Is the Right Anterior Temporal Variant of Prosopagnosia a Form of ‘Associative Prosopagnosia’ or a Form of ‘Multimodal Person Recognition Disorder’?

The construct of associative prosopagnosia is strongly debated for two main reasons. The first is that, according to some authors, even patients with putative forms of associative visual agnosia necessarily present perceptual defects, that are the cause of their recognition impairment. The second is that in patients with right anterior temporal lobe (ATL) lesions (and sparing of the occipital and fusiform face areas), who can present a defect of familiar people recognition, with normal results on tests of face perception, the disorder is often multimodal, affecting voices (and to a lesser extent names) in addition to faces. The present review was prompted by the claim, recently advanced by some authors, that face recognition disorders observed in patients with right ATL lesions should be considered as an associative or amnestic form of prosopagnosia, because in them both face perception and retrieval of personal semantic knowledge from name are spared. In order to check this claim, we surveyed all the cases of patients who satisfied the criteria of associative prosopagnosia reported in the literature, to see if their defect was circumscribed to the visual modality or also affected other channels of people recognition. The review showed that in most patients the study had been limited to the visual modality, but that, when the other modalities of people recognition had been taken into account, the defect was often multimodal, affecting voice (and to a lesser extent name) in addition to face.     

Impaired holistic and analytic face processing in congenital prosopagnosia: Evidence from the eye-contingent mask/window paradigm

There is abundant evidence that face recognition, in comparison to the recognition of other objects, is based on holistic processing rather than analytic processing. One line of research that provides evidence for this hypothesis is based on the study of people who experience pronounced difficulties in visually identifying conspecifics on the basis of their face. Earlier, we developed a behavioural paradigm to directly test analytic vs. holistic face processing. In comparison to a to be remembered reference face stimulus, one of two test stimuli was either presented in full view, with an eye-contingently moving window (only showing the fixated face feature, and therefore only affording analytic processing), or with an eye-contingently moving mask or scotoma (masking the fixated face feature, but still allowing holistic processing). In the present study we use this paradigm (that we used earlier in acquired prosopagnosia) to study face perception in congenital prosopagnosia (people having difficulties recognizing faces from birth on, without demonstrable brain damage). We observe both holistic and analytic face processing deficits in people with congenital prosopagnosia. Implications for a better understanding, both of congenital prosopagnosia and of normal face perception, are discussed.     

Covert face recognition in prosopagnosia: A review

Prosopagnosia, a spectacular face agnosia, is generally detected and discussed on the basis of explicit or overt performance of the subjects. However, recent observations suggest that an overt response is probably not sufficient to determine what is and what is not preserved in the cognitive processing of faces by prosopagnosia. Indeed, signs of covert knowledge have been evidenced in some, but not all, subjects, indicating that they are still able to use representations they cannot use overtly. Empirical data, showing that the nature of prosopagnosia is a more complex phenomenon than has been thought and that the processing models should be adjusted accordingly, are reviewed.     

Establishing visual category boundaries between objects: a PET study

Individuals with Alzheimer's disease (AD) often have problems in recognizing common objects. This visual agnosia may stem from difficulties in establishing appropriate visual boundaries between visually similar objects. In support of this hypothesis, showed that AD subjects have difficulties in establishing visual category boundaries between continuously graded shapes. In an attempt to investigate the neural basis of these impairments, the current study required a group of neurologically healthy elderly participants to categorically classify a series of ellipses varying in width while regional blood flow changes were measured using positron emission tomography (PET). Two categorization conditions were compared in order to isolate changes in cortical activity that dissociated the categorization of shapes situated either near or far from a category boundary that divided the width continuum. The participants produced a discontinuity in the probability and speed of categorizing the shapes at some point along the continuum, suggesting that the objects were classified into distinct categories. Moreover, a comparison of the PET scans obtained while the subjects were categorizing the shapes situated near vs. far form the category boundary revealed significant differences in cortical activity in the parietal and frontal brain areas. These findings suggest that both visuo-spatial and decision making mechanisms may be involved in establishing categorical distinctions between continuously graded stimuli. It is proposed that the functional role of the parietal and frontal cortical regions in establishing visual boundaries between categories of objects may be relevant for understanding object recognition impairments in AD.     

Perceptual functions in prosopagnosia

Some patients with prosopagnosia may have an apperceptive basis to their recognition defect. Perceptual abnormalities have been reported in single cases or small series, but the causal link of such deficits to prosopagnosia is unclear. Our goal was to identify candidate perceptual processes that might contribute to prosopagnosia, by subjecting several prosopagnosic patients to a battery of functions that may be necessary for accurate facial perception. We tested seven prosopagnosic patients. Three had unilateral right occipitotemporal lesions, two had bilateral posterior occipitotemporal lesions, and one had right anterior-to-occipital temporal damage along with a small left temporal lesion. These lesions all included the fusiform face area, in contrast to one patient with bilateral anterior temporal lesions. Most patients had impaired performance on face-matching tests and difficulty with subcategory judgments for non-face objects. The most consistent deficits in patients with lesions involving the fusiform face area were impaired perception of spatial relations in dot patterns and reduced contrast sensitivity in the 4 to 8 cycles deg(-1) range. Patients with bilateral lesions were impaired in saturation discrimination. Luminance discrimination was normal in all but two patients, and spatial resolution was uniformly spared. Curvature and line-orientation discrimination were impaired in only one patient, who also had the most difficulty with more basic-level object recognition. We conclude that deficits in luminance, spatial resolution, curvature, line orientation, and contrast at low spatial frequencies are unlikely to contribute to apperceptive prosopagnosia. More relevant may be contrast sensitivity at higher spatial frequencies and the analysis of object spatial structure. Deficits in these functions may impair perception of subtle variations in object shape, and may be one mechanism by which the recognition defect in prosopagnosia can extend to other classes of object subcategorization.     

Further observations on the nature of prosopagnosia

Two new cases of prosopagnosia are described and compared with pertinent clinical material from the English language literature. The interpretation of this disorder most compatible with the clinical data appears to us to be that there is an underspecification of visuoperceptive information preventing both the formation of significant face images and the retrieval of well-known face memoranda existing within a relatively intact visual remote memory store. Failure of formation of immediate memoranda of similarly complex visual images is also commonly observed but does not seem to be a requirement for the symptom of prosopagnosia. Conceptualizing this abnormality as simply a material specific visual agnosia of images beyond the classifier level would still appear to be acceptable if less informative.     

Shape Integration for Visual Object Recognition and Its Implication in Category-Specific Visual Agnosia

A series of experiments was conducted on a patient (ELM) with bilateral inferior temporal lobe damage and category-specific visual agnosia in order to specify the nature of his functional impairment. In Experiment 1, ELM performed a task of picture/word matching that used line drawings of fruits and vegetables as stimuli. The pattern of confusions exhibited by the patient suggested a failure in processing the full range of shape features necessary for the unique specification of the target relative to other structurally related items. This hypothesis of a shape integration impairment was tested and verified by subsequent visual recognition experiments (Experiments 2-4), which used synthetic stimuli with shapes precisely defined on the dimensions of elongation, curvature, and tapering. Furthermore, it was determined (Experiment 5) that the integration deficit is specific to the retrieval of shape knowledge from memory and does not affect the encoding of the properties of visual stimuli. It is argued that these findings have critical implications for cognitive theories of visual object recognition and for an interpretation of the visual function of the inferior temporal cortex. Finally, it was shown that the patient's deficit for structural knowledge integration is modulated by the semantic properties of the objects (Experiment 6), thereby demonstrating the applicability of the present findings to an explanation of category-specific visual agnosia.     

Independent representation of parts and the relations between them: evidence from integrative agnosia

Whether objects are represented as a collection of parts whose relations are coded independently remains a topic of ongoing discussion among theorists in the domain of shape perception. S. M., an individual with integrative agnosia, and neurologically intact ("normal") individuals learned initially to identify 4 target objects constructed of 2 simple volumetric parts. At test, the targets were mixed with distractors, some of which could be discriminated from the targets on the basis of a mismatching part, whereas the rest could be discriminated only on the basis of the altered spatial arrangements of parts. S. M. learned to identify the target objects, although at a rate slower than that of the normal participants. At test, he correctly rejected distractors on the basis of mismatching parts but was profoundly impaired at rejecting distractors made of the same local components but with mismatching spatial arrangements. These results suggest that encoding the spatial arrangements of parts of an object requires a mechanism that is different from that required for encoding the shape of individual parts, with the former selectively compromised in integrative agnosia.     

A double dissociation between action and perception in the context of visual illusions: opposite effects of real and illusory size

The idea that there are two distinct cortical visual pathways, a dorsal action stream and a ventral perception stream, is supported by neuroimaging and neuropsychological evidence. Yet there is an ongoing debate as to whether or not the action system is resistant to pictorial illusions in healthy participants. In the present study, we disentangled the effects of real and illusory object size on action and perception by pitting real size against illusory size. In our task, two objects that differed slightly in length were placed within a version of the Ponzo illusion. Even though participants erroneously perceived the physically longer object as the shorter one (or vice versa), their grasping was remarkably tuned to the real size difference between the objects. These results provide the first demonstration of a double dissociation between action and perception in the context of visual illusions and together with previous findings converge on the idea that visually guided action and visual perception make use of different metrics and frames of reference.     

Visual object agnosia as a problem in integrating parts and part relations

Current models of vision generally assume that the recognition of visual objects is achieved by encoding their component parts, as well as the spatial relations among parts. The current study examined how the processing of parts and their configurations may be affected in visual agnosia due to brain damage. Both a visual agnosic patient (AR) and healthy control subjects performed a visual search task in which they had to discriminate between targets and distractors that varied according to whether they shared their parts and/or their configuration. The results show that AR's visual search rates are disproportionally slow when targets and distractors share the same configuration than when they have different configurations. AR is also found to be disproportionately slow in discriminating targets and distractors that share identical parts when the targets and distractors share the same configuration. With differently configured targets and distractors, AR shows no part sharing effect. For controls, in contrast, the part and configuration sharing effects occur independently of one another. It is concluded that AR's object recognition deficit arises from difficulties in discriminating objects that share their configuration, and from an abnormal dependency of part information processing upon object configuration.     

Visually Controlled Locomotion and Visual Orientation in Animals

A general theory of locomotor behavior in relation to physical objects is presented. Since the controlling stimulation for such behavior is mainly optical, this involves novel assumptions about object perception and about what is called visual kinaesthesis. Evidence for these assumptions is cited. On the basis of this theory it is possible to suppose that animals are visually oriented to the surfaces of their environment, not merely to light as such. In short, it is possible to explain why they seem to have space perception. Implications of this approach for maze-learning are pointed out.     

Visuo-haptic integration in object identification using novel objects

Although some studies have shown that haptic and visual identification seem to rely on similar processes, few studies have directly compared the two. We investigated haptic and visual object identification by asking participants to learn to recognize (Experiments 1, and 3), or to match (Experiment 2) novel objects that varied only in shape. Participants explored objects haptically, visually, or bimodally, and were then asked to identify objects haptically and/or visually. We demonstrated that patterns of identification errors were similar across identification modality, independently of learning and testing condition, suggesting that the haptic and visual representations in memory were similar. We also demonstrated that identification performance depended on both learning and testing conditions: visual identification surpassed haptic identification only when participants explored the objects visually or bimodally. When participants explored the objects haptically, haptic and visual identification were equivalent. Interestingly, when participants were simultaneously presented with two objects (one was presented haptically, and one was presented visually), object similarity only influenced performance when participants were asked to indicate whether the two objects were the same, or when participants had learned about the objects visually—without any haptic input. The results suggest that haptic and visual object representations rely on similar processes, that they may be shared, and that visual processing may not always lead to the best performance.