Ординатура / Офтальмология / Английские материалы / The Neuropsychology of Vision_Fahle, Greenlee_2003

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nevertheless lead to partial failures of visual analysis for certain stimuli, and examples will be given below. These results clearly demonstrate that the view that introspection gives us on visual perception as being one unified entity is incorrect. Even though seeing the world appears to be a simple unitary process, this process has separable elements that may be damaged individually, leaving a view of the world that more or less selectively lacks one or several specific dimension(s).

Unfortunately, however, our knowledge about the exact contributions of almost all of these cortical areas is sparse, for a number of reasons. To start with, earlier researchers in neuropsychology quite often did not know the exact location of lesions in their patients, and only in relatively few patients could this localization be clarified after the patients’ deaths. Today, this problem has been overcome by the improvements of imaging techniques that make possible to localize most cortical defects by recording the sum potentials reflecting brain activity (see Chapter 3, this volume), by computed tomography (CT), and especially by magnetic resonance imaging (MRI; see Figs 7.7 and 7.8, and Chapter 4, this volume). A second, still virulent problem is that we do not know exactly what and where the individual cortical areas lie that are homologous to the monkey’s areas shown in Fig. 7.9. After all, our brains differ substantially from those of monkeys (thank goodness!) not only regarding the size and number of folds, but also regarding the arrangement of areas. (For example, the foveal representation in man is far more medial than in monkey, where it is situated on the lateral occipital cortex.) A third problem is that lesions in humans usually destroy more than one area, even if some of them only partially, and that fibres of passage between neighbouring areas might be destroyed, too. Hence, it is not surprising that patients seldom present ‘pure’ symptoms and that the exact relationships between the structure and function of visual cortical areas are still largely unknown.

Visual information-processing in the cortex: parallel processing and feedback

Given the rich and extended pattern of cortical areas analysing the visual world, strokes and other cortical injuries quite often involve parts of the ‘visual’ cortex that makes up, according to some estimates, around one-third of the human cortex. As we just saw, different parts of this system subserve different aspects of visual analysis and on different levels of abstraction. Over the last century, a solid body of descriptions has accumulated describing the resulting symptoms, and several systems to categorize them and to associate symptoms to different levels of (failed) analysis have emerged. The one used in this chapter is firmly based on these earlier systems, with a few modifications.

A failure of adequate response to visual stimulation in the absence of absolute scotomata—and usually intact colour-, motion-, and stereovision, i.e. failure of object analysis without severe loss in contour detection—is usually called an agnosia. An oftenused distinction is between apperceptive and associative agnosias (Lissauer 1890 ‘Seelen blindheit’; cf. Chapter 10, this volume). In short, apperceptive agnosias describe problems on a more fundamental level of perception: patients are unable to form visual objects and to reliably segregate figure from ground (Benton and Tranel 1993). Patients

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suffering from associative agnosia, on the other hand, are able to perform this early step of pattern analysis, but fail to categorize the figure they segregated from its surround and hence fail to recognize the objects in spite of the fact that they are able to bind together the isolated features. These clinical syndromes will be described in detail in the section ‘Apperceptive and associative agnosias’, while some neuronal aspects are presented here.

Understanding neuropsychological symptoms in vision in full would require the understanding of the normal structure and function of the neuronal machinery that subserves visual perception. From the knowledge about this function outlined in Chapters 1, 2, and 5 in this volume, we now have a concept of cortical function quite different from that of a couple of decades ago. Cortical processing is no longer considered to be a one-way sequence of hierarchical levels of (increasingly complex and symbolic) information-processing, but rather a highly complex entity of feedforward and feedback projections (see especially Chapter 2). With such a view, which emphasizes the effects of top–down influences from ‘higher’ cortical areas to ‘lower’ ones, factors such as attention and expectation gain importance even for the very first steps of visual pattern analysis (e.g. Ullman 1995). A second important insight is the distributed and parallel processing of visual information in the cortex. Different aspects of stimuli are analysed in parallel processing streams (e.g. colour, motion; see Chapter 5, this volume), and we have good evidence for a partial separation between processing of contours versus (homogeneous) areas (see the next subsection and the later subsection ‘Neuronal mechanisms for contour and position detection’; Welpe et al. 1980; Grossberg 1991; Paradiso and Nakayama 1991).

On the other hand, the brain uses not maximally distributed processing—if it would, as Lashley thought (see Bach et al. 1960), there would not exist any specific losses for specific functions such as colour or form perception, and neither would agnosias exist. The brain obviously processes similar features, or objects in nearby locations, so we find (visual) retinotopy, (auditory) tonotopy, and (somatosensory) somatotopy in primary sensory areas, as well as some type of ‘object-topy’ in higher areas, e.g. all faces seem to be processed in adjacent parts of the cortex, enabling the syndrome of (isolated) prosopagnosia (failure to recognize faces; see the eponymous section). As a consequence of the feedback nature of the system, the identification of an object seems to occur usually in an iterative way. First, in a very fast process, a preliminary hypothesis is produced about what type of object might be present. Thorpe et al. (1996) demonstrated that cortical potentials evoked by presentation of natural scenes containing animals versus those not containing animals start to differ from each other as early as 150 ms after the start of stimulus presentation. This is to say that, after such short time, the brain has already made a hypothetical decision about a rather complex dichotomy, namely, between animate and inanimate scenes. However, the pattern recognition task is by no means finished by that time, but higher security and precision of analysis require extensive additional computation.

Given these facts, it is not surprising that the electrical activities evoked by a visual stimulus in ‘early’ and ‘higher’ visual areas overlap over quite a substantial time, as is

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evident from Fig. 2.9 in Chapter 2, and it has been argued that the failure of agnosic patients to correctly identify objects may be due to the fact that they stop too early during the iterative process of object synthesis in the visual brain (Zihl and von Cramon 1986). Both theoretical (e.g. Hinton 1981) and empirical findings (e.g. Fahle and Poggio 2002) indicate moreover that processing and storage of information are not strictly separated in the brain: changing perceptual memory is associated with changing perception.

To sum up, anatomical, electrophysiological, and computational evidence all support a view of cortical pattern analysis as an iterative process involving the simultaneous activity of many cortical areas that deal with visual information-processing on different levels of complexity. This new view poses some problems for a clear-cut discrimination between the effects of associative disturbances on one hand and apperceptive ones on the other, since not only do disturbances on the level of perception hinder association, but also the other way round! This view of cortical processing immediately explains why it may be difficult to discriminate between apperceptive and associative agnosias in patients (see the section ‘Apperceptive and associative agnosias’). Even if these defects involve different levels of information processing, the lower level will not function normally if the higher one is defective. Still, it seems fair to discriminate, not only computationally but also in the cortex, between different levels of processing in feature analysis and hence between different levels of defect. But we should always be aware that even lesions on ‘high’ levels of processing can have effects on performance on the ‘low’ levels, especially for difficult perceptual stimuli requiring iterative processing.

Different levels and separate channels of visual information-processing

In the following, I would like to propose an operational distinction between the different levels of visual analysis, loosely based on the modular structure of visual cortex as outlined in the subsection on ‘The modular structure of visual cortices’ and the parallel processing as outlined in the preceding subsection. The first level achieves predominantly the detection of contours, or boundaries between areas, supplying information about the type of edge, its position, orientation, sharpness, and contrast—similar to the primal sketch of visual scenes proposed by Marr (1982). The perceived quality of areas defined by these boundaries is to a large extent determined by the information collected at these contour boundaries. An example for a feature extracted at this level is a difference in luminance (hence a luminance contrast), the feature tested in conventional perimetry. But a large number of features can contribute to contour definition, such as differences in colour, stereo-depth, motion direction, or velocity, and many more, often based on differences in texture (see the beginning of the section on ‘Visual indiscriminations’).

Two parallel systems seem to exist—one detecting boundaries (e.g. by means of spatial bandpass–filtering) and the other one representing (larger) areas (spatial

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Fig. 7.10 Craik-O’Brian-Cornsweet illusion. While the areas on both far ends of the divide have exactly the same luminance (cover the middle part of the figure and you will see for yourself), they appear at different brightness. The reason is the sharp transition between high and low intensity which is clearly perceived by the visual system. The information on intensity collected at this border is extrapolated towards the adjacent area, while the slow gradient of luminosity that brings both areas back to identical intensity levels is largely ignored by the early stages of the visual system and is eventually eliminated. (From Fahle (2003a).)

lowpass-filter). Features such as colour, luminance, and texture, represented partly by an area-system, seem to be filled in into the areas delineated by the contours, and starting from the contours (Welpe et al. 1980; Paradiso and Nakayama 1991; Grossberg 1991). One striking demonstration is the Craik-O’Brien-Cornsweet illusion, where two fields of identical luminance appear in quite different brightness due to the fact that the areas close to the borders between the two fields have different contrast polarity (Fig. 7.10).

Another forceful argument for the pre-eminent importance of borders is the so-called stabilized image. Our eyes constantly perform irregular high-frequency, low-amplitude motions that move the retinal image of the outer world over short distances on the retina. If the image of the outer world is stabilized on the retina (say by immobilizing the eye), the world fades within a few dozens of seconds. Note that the stabilization will have no influence on those photoreceptors illuminated by homogeneous areas—their input stays constant anyway. The only receptors that will experience a difference between a stabilized and an unstabilized image are the ones at boundaries. While the moving contour prevents local adaptation of the underlying photoreceptors, this changes as soon as the boundaries are stabilized and local adaptation takes its toll.

While the boundary system is certainly the most important channel for visual information-processing, a second independent system probably exists which conveys information about areas (cf. the subsection ‘Neuronal mechanisms for contour and position detection’; Welpe et al. 1980). Moreover, a second categorization is important: between a system analysing primarily colour and fine detail (P-system) and another one dealing primarily with motion signals and important for action (M-system; see

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Ungerleider and Mishkin 1982; Milner and Goodale 1995; Westwood et al. 2002; Patla and Goodale 1996; Goodale et al. 1991; cf. also Ettlinger 1990; Vaina 1994).

The results of single-cell recordings in animals, mostly macaque monkeys, indicate that the striate cortex as well as early extrastriate areas subserve fundamental visual operations such as detection of contours, as well as analysis of orientation and spatial frequency (plus some forms of grouping and figure-ground segmentation, see below; Peterhans and von der Heydt 1991). Disturbances on this level of image processing, i.e. failures to detect and identify contours and borders, and to fill in the adjacent areas, are not usually called agnosias, but rather scotomata or visual field defects, or cerebral achromatopsia, or motion blindness, depending on the individual type of defect. As a general name for this class, and to stress the fact that they share a defect on the same

Semantic storage

Stored visual representation (pseudo(?) 3D-maps)

Grouping/ binding to surfaces/ objects

Retinal input

Fig. 7.11 Schematic overview of the levels of cortical information-processing and the symptoms arising from disturbances on the different levels. On the first level, boundaries are detected based on transitions in luminance, hue, (stereoscopic) depth, motion direction or speed, texture, or other cues, e.g. second-order features in these submodalities. Defects on this level lead to symptoms that are called indiscriminations. On the next level, contours, or boundaries are combined and bound together to form objects. Defects on this level lead to apperceptive agnosias. On a third level, the objects are compared with stored representations of objects encountered earlier, i.e. the present object is categorized and hence recognized. Defects on this level lead to associative agnosias, e.g. to prosopagnosia if only recognition of faces is defective, or alexia if the defect concerns words. The recognized object is usually linked to a noun (semantic storage). Missing of this link leads to optic aphasia.

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level of processing—between complete blindness on one side and the intact detection of contours and areas without the ability to form objects on the other side (apperceptive agnosia; see the beginning of the section ‘Apperceptive and associative agnosias’)—I would propose the term ‘indiscriminations’ (see Fig. 7.11). These indiscriminations will be dealt with in detail in the first two subsections of ‘Visual indiscriminations’, while the third subsection presents methods to test these functions.

The second level is the binding together of individual contour elements to coherent objects. This is by no means an easy task in natural environments due to partial overlap between objects, shadows adding contours that do not represent object borders, and motion blur, to name a few problems. Disturbances on this level usually receive the label ‘apperceptive agnosias’. The third level then would be recognition of the objects formed on the second level, mainly on the basis of the contour information collected on the first level. Disorders on this level are generally called associative agnosias (see the last two subsections of ‘Apperceptive and associative agnosias’), since the association between the visual image and its stored representation has been lost. One may or may not continue to discriminate a fourth level that connects the recognized object with the appropriate noun, but this level may not be specific for visual neuropsychology. Disturbances on this fourth level are called optic aphasias (see the eponymous subsection), reflecting the fact that the object can be identified, but the connection to its name is lost (while the person still knows the correct noun; compare Mendola et al. 1999). As mentioned above, these levels cannot be separated during normal operation. They do not work sequentially but at least partly in synchrony, so defects on each of the levels will necessarily influence the operation of the other levels, even the ‘lower’ ones, at least when extremely difficult perceptual tasks have to be solved.

The above distinction of levels will serve as a useful way to categorize the symptoms of patients in visual neuropsychology, even if the levels cannot be separated from each other as precisely as one would like. Deficits on the level of binding together of contours, i.e. of object formation and object identification, will be discussed in the section ‘Apperceptive and associative agnosias’.

Visual indiscriminations and failures of space representation

Visual indiscriminations: failures to extract (object) boundaries in visual scenes

Defects of detecting luminance and colour contrasts

There appears to be no unique role for luminance contrast in the detection of contours. Contours between objects can be defined by differences in hue, saturation, reflectance, stereoscopic depth, texture, motion velocity or motion direction of elements, time of appearance of elements, and quite a number of other, more complex features, such as the amount of variation in any of these domains over space and/or time (so-called secondorder features; e.g. Zanker et al. 1998; Chapter 4, this book). But luminance contrast is

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the only feature contributing to contour detection that is routinely tested in clinical practice, mostly due to the fact that this test is technically easy to perform and that virtually all contours in natural environments have a contrast component—hence patients suffering from defects in detecting luminance contrast are most severely handicapped. Defects anywhere in the retina and along the visual pathways up to the primary visual cortex will produce defects in contrast detection as well as in all other submodalities that can contribute to contour detection. Hence, testing one dimension is sufficient to assess the damage. After all, detecting a luminance (or colour) contrast is a prerequisite for most other processes of feature analysis such as stereovision and orientation discrimination. But just testing patients’ ability to detect luminance contrast is not sufficient for lesions that involve cortical areas beyond the primary visual cortex. Injuries of cortical areas beyond V1, the primary visual area receiving the bulk of the afferent fibres from the retina via the lateral geniculate nucleus, often do not result in absolute scotomata as detected by conventional perimetry.

An example of such an incomplete defect is a condition called ‘cerebral amblyopia’ where the perceptions of form and of colour are defective in the contralesional hemifield while luminance detection is preserved (see below; Mauthner 1881; Gelpke 1899; Poppelreuter 1917; Teuber et al. 1960; Zihl and von Cramon 1986). A number of patients have been described as suffering from relatively isolated defects of abilities such as detecting motion or colour. Examples for defects of colour processing caused by cortical injury are discussed in detail in Chapter 8, this volume (see also Samelsohn 1881; Scotti and Spinnler 1970; Tzavaras et al. 1971; Assal et al. 1969; Damasio et al. 1980a; Green and Lesell 1977; Lewandowsky 1908; Lhermitte et al. 1969; Pearlman et al. 1975; Mendola and Corkin 1999; Cronin-Golomb et al. 1993; Troscianko et al. 1996). In short, bilateral destruction of several cortical areas, including Area V4, can lead to the so-called cortical achromatopsia. Patients suffering from this type of ‘indiscrimination’ lose the ability to discriminate between colours on the basis of hue or saturation. They only perceive shades of grey, in spite of intact retinal ganglion cells of all three types and in spite of the fact that they can still faintly perceive borders between directly adjoining coloured patches if the differences are sufficiently large. Object colour can no longer be ‘filled in’ from the borders, and the patients are unable to find an object on the basis of its colour. Moreover, patients may be unable to name the colour that is characteristic of an object (Zihl and von Cramon 1986) or to correctly sort colours (de Renzi et al. 1972; cf. also de Renzi and Spinnler 1967). The defect of colour perception may be present in only a part of the visual field—most often, one of the upper quadrants—and often is associated with problems in identifying faces (prosopagnosia; see the eponymous subsection). Lesions usually are located in the medial and lateral occipitotemporal gyri.

Defects of detecting and discriminating motionor time-defined boundaries

Another submodality of visual perception that has been reported as being defective in patients without distinct scotomata as revealed by perimetry is motion detection.

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Already the gestalt psychologists knew that an object could be defined by ‘common fate’, e.g. common direction of motion. We must first clarify how motion information can contribute to the detection of boundaries between areas and hence define an object before dealing with deficits of this ability.

The case is similar to that of visual perception in general, which to introspection appears as a unitary entity while it consists of many partly independent submodalities (see the subsection on ‘The modular structure of visual cortices’). Similarly, introspection tends to create the wrong impression regarding the sequence of events when it comes to analysing moving objects. I expect that most people not familiar with neurophysiology would suppose that our brains first detect objects and subsequently analyse their movements. A number of experiments show that this is not the case, at least not always. On the lowest level of motion analysis, the elementary motion detector signals that a contrast edge has moved, usually from one position in space to a nearby position. The detector is so simple (Fig. 7.12) that it cannot discriminate between moving versus appropriately flickering targets. It just differentiates between dynamic versus stationary stimuli as well as between different directions of motion.

The local motion signals from many motion detectors, each with a spatially restricted receptive visual field, are combined with each other. They thus create an object, defined, e.g. by common motion relative to a stationary background, by a difference in the speed of element motion, or else by a difference in the direction of element motion. In this way, motion information can contribute to the detection of borders in the visual field, and can by itself define an object. Low-level motion information, such as differences in the speed of moving dots (one special case being stationary dots) can serve as input for the contour detection system, thus defining an object that would otherwise be invisible. (The same is true for stereoscopic depth perception: an object may be defined purely by disparity differences between the object and its surround, the principle underlying the so-called random-dot stereograms (Julesz 1971; see the next subsection), and even differences in the presentation times of identical elements in different areas of the visual field can lead to the perception of contours between these areas (Fahle 1993).)

It seems that there are only very few reports in the literature on patients suffering from relatively isolated but severe disturbances of motion perception. In all cases, the patient’s detection or discrimination of moving stimuli had deteriorated rather selectively (Pötzl and Redlich 1911; Goldstein and Gelb 1918; Zihl et al. 1983; Greenlee and Smith 1997; cf. also Smith et al. 1998; Vaina et al. 1999; Braun et al. 1998; Vaina et al. 1990, 2000, 2001a; Cowey and Vaina 2000; Vaina and Rushton 2000; Clifford and Vaina 1999; Vaina 1989, 1998; Vaina and Cowey 1996; and Vaina et al. 2001b for fMRI-correlates of different levels of motion processing in humans). Patients with severe symptoms typically see the object both at the start and the end of its trajectory, but not in-between, and some who had been tested for the perception of apparent motion did not experience any motion impression. A number of additional patients described in the literature suffered from disturbances of motion perception that were either due to the so-called cerebral amblyopia which is not specific for motion perception (cf. Zihl and

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**

+_

Fig. 7.12 The elementary motion detector. A stimulus moving from left to right (solid horizontal line) will first activate the left receptor and, after a delay depending on the speed of motion, will subsequently activate the right receptor. (a) During that interval, the activation of the left receptor has passed through the delay line and arrived at the multiplication unit where it meets the activation from the right receptor which does not have to cross a delay line. Hence, the multiplication unit produces an output. Leftward motion (interrupted horizontal line), on the other hand, will first activate the right receptor and subsequently, after a delay, the left detector. When the activation from the right detector arrives at the multiplication unit,

the other factor, coming from the left detector, is zero, and thus will be the result of the multiplication. The same is true when the activation from the left receptor finally arrives at the multiplication unit. By that time, the activation from the right receptor has long decayed, one of the factors is zero, and the multiplication unit signals ‘no movement’. (b) A delay line at the output of the other i.e. right receptor, creates a motion detector for the opposite direction, i.e. leftwards. Both detectors can be activated by repetitive, i.e. flicker stimulation.

von Cramon 1986), or due to loss of perception of motion-in-depth associated with a loss of depth perception (see the next subsection).

The best-studied and most pronounced case of ‘motion-blindness’ is that of a 43-year-old patient who had suffered from a bilateral occlusion of the parieto-occipital

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superior cerebral veins. Her visual fields were intact on both sides. The patient experienced all moving objects as jumping from one position to the next, rather than as in smooth motion, and had problems even in judging the speed at which a cup filled with coffee or in perceiving the mimics of her conversational counterpart. Crossing the street was dangerous for her since she could not estimate the speed of approaching cars, and she had problems navigating in crowded places due to an inability to anticipate the paths of other pedestrians. Interestingly, her ability to perform visually guided pursuit eye movements was also defective. The most probable cause for the defects was a bilateral injury to the medial temporal as well as the occipital gyri (cf. Fig. 7.3). In addition, a disconnection between striate cortex and some prestriate cortical areas may have played an important role (Zihl et al. 1983).

Defects to detect or discriminate contours defined by depth, by orientation differences, and ‘cerebral amblyopia’

A defect of stereoscopic depth perception, and hence the ability to detect boundaries based on depth differences, that is not linked to oculomotor abnormalities occurs in a relatively low proportion of patients after head trauma (Hart 1969). Usually, loss of fusion, i.e. of the ability to direct both eyes to exactly the same direction and to superimpose both retinal images, will lead to loss of stereoscopic vision in these trauma patients (Danta et al. 1978). The small phorias that almost all of us have and that lead to a small squint in the dark when a fusional impulse is missing might express themselves if fusion is defective. Relatively isolated defects of stereoscopic depth perception have been described as well as those combined with scotomata (Anton 1899; Pick 1901; Poppelreuter 1917; Holmes 1918a,b ; Birkmayer 1951; Benton and Hécaen 1970; Hamsher 1978; Lehmann and Walchi 1975; Rizzo and Damasio 1985; Rizzo 1989; Rothstein and Sacks 1972; cf. also Servos et al. 1995).

Depth perception not only relies on binocular disparities between the two retinal images, but also on several distinct cues (e.g. Fahle and Troscianko 1991). It seems that the ability to make use of at least several of these cues can be disrupted independently, usually after bilateral injuries (Danta et al. 1978; Birkmayer 1951; Kramer 1907; Holmes and Horax 1919; Gloning 1965). Complete loss of (not only stereoscopic) depth perception is often associated with the patient’s inability to appreciate the third dimension of perception: the world appears like the image on a monitor-screen (Riddoch 1917; Holmes and Horrax 1919; Faust 1947; Gloning 1965; cf. also Vaina 1989). This complete loss of the third dimension, at least in some patients, disrupts one of the important constancies, namely size constancy (see the subsection ‘Failures to achieve object constancy’). Retinal signals contain information about location of objects (direction, distance), their size, and speed that have to be converted from retinal space into egocentric space that is independent of eyeand head-movements in order for subjects to be able to navigate through their visual world.

There have been only a few reports on an isolated inability to perform figure–ground discrimination—and hence to detect boundaries—on the basis of orientation differences,