Neuropsychological dissociations between motion and form perception suggest functional organization in extrastriate cortical regions in the human brain

Brain and Cognition 74 (2010) 160–168

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Neuropsychological dissociations between motion and form perception suggest functional organization in extrastriate cortical regions in the human brain Heath E. Matheson *, Patricia A. McMullen Department of Psychology, Dalhousie University, Halifax Nova Scotia, Canada

a r t i c l e

i n f o

Article history: Accepted 28 July 2010 Available online 19 August 2010 Keywords: Neuropsychology Coherent motion perception Static form perception Form-from-motion perception Biological motion perception Dissociation

a b s t r a c t In this review of neuropsychological case studies, a number of dissociations are shown between different visual abilities including low-level motion perception, static form perception, form-from-motion perception and biological motion perception. These dissociations reveal counter-intuitive results. Specifically, higher level form-from-motion perception can persist despite deficits in low-level motion perception and static form perception. To account for these dissociations, we present a model of functional organization and identify future directions for investigations of higher order form-from-motion perception. Ó 2010 Elsevier Inc. All rights reserved.

1. Introduction To adaptively interact with and navigate through the environment humans need to visually process objects and their movements. Further, it is critically important that the visual system processes the motion information about an object in conjunction with the form information about that same object. For example, survival critically depends on the visual system’s ability to attribute the motion of a predator with the form of the same predator, and not to an incidental object in the environment like a tree. Most importantly, form and motion information needs to be coherently processed by other systems within the brain in order to judge the behavioural relevance of the object (‘‘Is this looming object dangerous?”), and prepare the most appropriate and adaptive response (‘‘Should I get out of the way?”). Because these processes are important for the survival of the species, it is no surprise that the human brain has evolved relatively specialized systems for analyzing form and motion information. Importantly, based on a large body of neuropsychological dissociation literature it has been suggested that the visual system is parsed into two streams, each with its own processing mandate (Milner & Goodale, 1995). The ventral stream, extending from primary visual cortex into the inferior temporal lobe, appears to be relatively specialized to process information about an object’s form, and participates in explicit form recognition. Conversely, the dorsal stream, extending from the primary visual cortex into the parietal lobe, appears to be specialized for analyzing the motion, location, and volumetric properties of an * Corresponding author. E-mail address: [email protected] (H.E. Matheson). 0278-2626/$ - see front matter Ó 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.bandc.2010.07.009

object and uses this information to guide grasping. Though the relative independence of these two streams has been questioned (e.g. Husain & Nachev, 2006), and though it is clear that each stream does not participate in form or motion processing exclusively (e.g. some regions in dorsal stream are sensitive to shape properties including depth structure, Durand et al. (2007), and depth from stereopsis, Georgieva, Peeters, Kolster, Todd, and Orban (2009), for a review see Orban et al. (2006); and there are occipitotemporal regions that appear to be sensitive to low-level motion, Sunaert, Hecke, Marchal, & Orban, 1999), Milner and Goodale (2008) have maintained that both streams receive similar early visual input and transform it to produce separate types of output for different purposes; specifically, the ventral stream is used to select possible objects for action, while the dorsal stream uses visual input (information about motion, location, and volumetric properties) to implement a desired action (Milner & Goodale, 2008). These proposed systems have been supported by investigations using functional magnetic resonance imaging (fMRI) and have consistently shown that form processing is associated with increased blood flow to ventral regions in the temporal lobes and movement information is associated with increases in the dorsal regions of the parietal lobes (see Grill-Spector & Malach, 2004). However, though imaging studies have implicated disparate brain regions in processing form and motion information, the way in which these specialized processes share information remains poorly understood. To date, a large number of studies have demonstrated that these systems interact (reviewed in McIntosh and Schenk (2009); see Adamo & Ferber, 2009; Bruno & Franz, 2009) and a number of suggestions have been made about how these interactions occur, though a coherent framework has yet to

H.E. Matheson, P.A. McMullen / Brain and Cognition 74 (2010) 160–168

surface. Each of the current accounts posit some mechanism by which the two streams exchange information, with some focusing on functional connections and ‘crosstalk’ between the two streams (e.g. Regan, Giaschi, Sharpe, & Hong, 1992; Zhuang, Peltier, He, LaConte, & Hu, 2008) and others suggesting a separate integrative mechanism responsible for combining information from the two streams; candidate integrative mechanisms have been proposed for the superior temporal sulcus (STS) (Baizer, Ungerleider, & Desimone, 1991; Peuskens, Vanerie, Verfaillie, & Orban, 2005) or regions within the parietal lobe (Regan et al., 1992). Other accounts share and combine features of the suggestions listed here (e.g. Kourtzi, Bulthoff, Erb, & Grodd, 2002), but it is clear that researchers are far from establishing a broadly accepted account of form and motion interactions within the visual system. Previous suggestions of how form and motion interact within the visual system are based on investigations using different brain imaging techniques (e.g. fMRI), psychophysical behavioural experiments, and/or neuropsychological case studies. Though these methods have led to many important findings, a complete and integrated review of even a single technique has not been conducted. We feel that a review of the neuropsychological literature will be a critical step in developing a coherent framework describing the interactions between form and motion processing within the human visual system, primarily because neuropsychological investigations are capable of revealing behavioural dissociations that are difficult to reveal using other methods. Though many useful descriptions of neuropsychological dissociations between form and motion processing have surfaced (as will be demonstrated below), we feel that a complete review of known dissociations will contribute to the development of neurocognitive models of the processing of form and motion information. As a result of this review, we present a tentative model that leads to a few critical predictions about the organization of form and motion processing and the integration of these two types of information within the visual system. 2. Neuropsychological dissociations To investigate the interactions between form and motion processing, we have reviewed a number of neuropsychological case and group studies that have employed different perceptual tasks. In these published reports, researchers have typically used tasks of: (a) static form perception, (b) low-level motion perception, (c) form-from-motion perception, and (d) biological motion perception. (Examples of such tests are described below and summarized in Table 1.) Though the tests used across studies are not identical, we have attempted to note the critical differences where appropriate. Below, we describe the general characteristics of each task. Static form perception is usually studied by showing patients line drawings or photographs of common objects and having them verbally name them or visually discriminate between two exemplars. Often the stimuli are line drawings, but greyscale photos of real objects appearing in conventional and unconventional views

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are often used. Low-level motion perception is generally studied by using coherent motion stimuli. In these stimuli, random dots (e.g. ‘‘snow”) are presented with each dot moving in a random direction. The participant sees nothing but random flicker. However, when a certain proportion of dots move together in the same direction (i.e. coherent motion) a sense of directional motion is perceived. The threshold (minimum proportion of moving dots needed to induce perception of overall coherent motion in one direction) is usually taken as an index of sensitivity to basic motion. With these types of stimuli and tasks it is thought that basic form and motion processing can be studied relatively independently. To study interactions between form and motion processing two other types of stimuli have been used which combine these attributes. They are 2-D and 3-D form-from-motion stimuli. In 2-D form-from-motion stimuli, a proportion of background dots in a random-dot display move in one direction (or at a certain velocity) making up the background. The rest of the dots, making up a foreground object (such as a letter), move in another direction (or at a different velocity). When the image is static, observers see nothing but a collection of random dots (i.e. ‘‘snow”) because there is no contour information available in the stimulus (i.e. no differences in luminance, texture, or depth between the background and foreground). However, once the foreground dots move relative to the background dots the hidden form is immediately perceived. This type of stimulus is important because the visual system extracts form information from motion cues alone. A second type of stimulus, a 3-D form-from-motion stimulus, is created by placing dots on the surface of an invisible 3-D structure. When the display is stationary, the observer sees a collection of random dots. However, when the dots move, a rotating three-dimensional object is perceived (such as a sphere or cube). Here too, the visual system extracts form information based on motion cues. Though both types of stimuli are considered form-from-motion, there is an important distinction between the two. Vaina (1989) suggests that 2-D form-from-motion relies on processes of ‘segregation’, that is, perceptually differentiating between figure and ground, whereas 3-D form-from-motion relies on processes of ‘integration’ over time, or perceptually integrating the motion of individual dots as they move through time and space. This suggests that 2-D and 3D form-from-motion stimuli may be processed by functionally distinct mechanism (and evidence for this is provided below). Finally, interactions between form and motion are investigated with another type of stimulus, known as a biological motion stimulus (or Johansson point-light walker stimulus, Johansson, 1973). To create these stimuli, points of light are placed on the major articulating joints of a human actor while the actor is filmed in a dark room. Observers can immediately identify the isolated moving points as a human figure despite the fact that there is no contour information in the stimulus. When the stimulus is static, scrambled, or inverted, observers fail to report seeing a human actor (Sumi, 1984). In these more complex stimuli, object form is extracted based on the global movement of the elements in the display, despite the lack of contour information in the stimulus.

Table 1 Brief descriptions of tasks typically used to investigate form and motion processing in neuropsychological investigations. Process

Task

Description

Basic form processing Basic motion processing Form-from-motion processing

Static form Coherent motion 2-D form-frommotion 3-D form-frommotion Point-light walkers

Object naming of static line drawings, discrimination of different silhouettes Proportion of dots moves coherently against a background of random dots Kinetic boundaries define shape

Biological motion processing

Contour defined by positioning and motion of imaginary points of light on the surface of an object (e.g. rotating in three dimensions) Points of light are placed on the articulating joints of a moving human actor filmed in the dark

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Together, 2-D and 3-D form-from-motion and biological motion stimuli provide a means to investigate interactions between the processing of form and motion. Few reported studies have tested any single patient using all four of these tasks. Thus, this review is separated into five parts based on the patterns of intact and impaired perceptual abilities displayed in different subgroups of patients who have been tested with a combination of these tests. Within each section, we highlight the areas of brain damage common to each group (as described by the authors of each study). However, the use of different imaging techniques and nomenclature, and the fact that there is often wide-spread damage in many of these patients, makes it difficult to compare lesions across studies and therefore our conclusions are based on more gross anatomical organization (areas listed in each patient) that likely reflects the critical functional areas for the abilities we describe. To support our claims, neuroimaging results are also provided. Importantly, it is assumed that even a single reported dissociation between two perceptual abilities provides an ‘existence proof’ that the two abilities are dissociable (Farah, Wilson, Drain, & Tanaka, 1995). Using this approach, we were able to show double dissociations between all but one pair of the four perceptual abilities. In addition to this, we reveal counter-intuitive dissociations between pairs of perceptual abilities. By counter-intuitive, we mean that intuitive assumptions of functional dependence of more complex abilities (e.g. perceiving form-from-motion) on more basic abilities (e.g. perceiving static form) and are not supported. Rather, counter-intuitively impairment of these basic abilities does not necessarily impair complex abilities. For example, the impairment of static form perception does not always impair form-from-motion perception. Finally, we develop a testable neurocognitive model that accounts for the patterns of double dissociation and resolves a number of counter-intuitive results. 2.1. Impaired static form perception with preserved low-level motion, form-from-motion, or biological motion perception Impairments of static form perception and recognition, typically referred to as visual agnosia, have been extensively reported (see Farah (1990) for a comprehensive review). Although, low-level motion perception is rarely studied in such patients, Vaina (1994) provided convincing evidence from a visual agnostic (EW) that static form perception can be impaired independently of low-level motion perception. EW was impaired at Efron shape discrimination, face recognition, and could not recognize common objects from conventional and unusual views. These are all tasks that require static form perception. Importantly, his low-level motion perception was intact (i.e. normal motion coherence thresholds). This patient also reveals our first striking counter-intuitive dissociation: despite impairments in static form perception this patient can perceive form-from-motion and biological motion displays. Specifically, he showed relatively intact 2-D form-from-motion perception, with normal ability to detect kinetic boundaries defined by differences in motion direction and to detect a form (i.e. square, triangle, etc.) defined by differences in speed. 3-D structure from motion was also relatively intact (i.e. the ability to detect a spinning cylinder). Finally, EW was able to discriminate point-light walkers and identify their actions. Overall, these results demonstrate that patient EW had difficulties perceiving static forms (i.e. agnosia), but could still extract 2-D and 3-D forms when they were primarily defined by movement. Impairments in static form perception are usually a consequence of damage to the ventral occipito-temporal cortex, as was the case with EW. Specifically, he suffered from bilateral occipital lesions (with more extensive damage on the right), extending ventrally into medial temporal areas including hippocampus and para-

hippocampal cortex. Further, some damage extended into the parietal lobe, posterior to the trigone of the lateral ventricle (Vaina, 1994). The ventral occipitotemporal area’s importance for static object recognition has been corroborated by fMRI studies in neurologically intact participants (e.g. Ishai, Ungerleider, Martin, & Haxby, 2000; see Grill-Spector, 2003). With this pattern of brain damage and behavioural performance it is clear that static form perception can be selectively impaired relative to the perception of low-level motion, form-from-motion or biological motion. Again, the counter-intuitive finding here is that despite extensive damage, particularly to ventral visual cortex, an object’s form can still be perceived when derived from motion cues. 2.2. Impaired low-level motion perception with preserved static form, form-from-motion, and biological motion perception ‘‘Motion blindness”, or akinetopsia, is associated with impaired low-level motion detection and can be dissociated from static form perception. Patient LM (McLeod, Dittrich, Driver, Perrett, & Zihl, 1996), though able to identify objects in daily life, was severely impaired on tasks of motion perception (Zihl, Von Cramon, & Mai, 1983). Consistent with her anecdotal reports of impaired motion perception in everyday life, her motion coherence thresholds were elevated across a range in which normal subjects perform flawlessly (Baker, Hess, & Zihl, 1991). Importantly however, and despite her difficulties on low-level motion tasks and self-reported ‘motion blindness’, she was successful on a variety of form-from-motion tasks. First, LM could identify 3-D form-from-motion, (e.g. a cube; Rizzo, NAwrot, & Zihl, 1995) or could at the very least describe their motions (e.g. the motions of a point-light door opening and closing). Further she could perform a number of biological motion tasks including: (a) detecting human actors and identifying their actions, (b) discriminating between intact and scrambled point-light walkers, and (c) discriminating point-light walkers and cyclists from non-meaningful movement (McLeod et al., 1996). This demonstrates that LM was able to use motion to recover both biological and non-biological form information despite her limited ability to perform the coherent motion task and to process basic motion. Though adding noise to the motion display reduced her ability to perform the biological motion tasks, the overall performance from this patient shows that low-level motion perception is dissociable from biological motion. LM was not tested on a 2-D motion task. Evidence that 2-D form-from-motion perception can be dissociated from basic motion perception was provided by another patient with impaired low-level visual motion perception (as measured with the motion coherence task), BC, (Vaina, Cowey, LeMay, Bienfang, & Kikinis, 2002). BC showed normal 2-D form-from-motion perception when the motion-defined form (e.g. square) moved against a static background and she could detect boundaries when they were defined by differences in motion direction. BC also showed intact static form perception (object recognition from conventional views), and was unimpaired on identification of the action in biological motion displays. These results are complimented by two other patients. First, another clear example of impaired low-level motion wither preserved biological motion perception was shown in patient WK (Billino, Braun, Bohm, Bremmer, & Gegenfurter, 2009), and studies of patient AF, who also showed elevated motion coherence thresholds (Vaina, Lemay, Bienfang, Choi, & Nakayama, 1990) showed intact 3-D structure from motion some aspects of biological motion (see also Vaina, 1994). All of these patients showed deficits in low-level motion perception as measured by coherent motion tasks (i.e. elevated thresholds). Common to each of these patients was damage to area hMT+/V5 (LM bilateral lesions, BC right hemisphere, WK right hemisphere, AF bilateral damage but larger on the right), a region

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that has been implicated in studies of low-level motion perception in fMRI studies (e.g. Tootell et al., 1995). (Though note that WK had a focal lesion just posterior to this in stereotaxic space, indicating intersubject variability.) Importantly, the studies reviewed here demonstrate our second counter-intuitive result: in some patients, deficient perception of low-level motion does not limit their use of motion information when it defines a biological or non-biological form/boundary. This suggests that the processing that underlies low-level motion perception in hMT+/V5 is not necessary for processing these more complex stimuli. 2.2.1. Impaired biological motion perception with preserved static form, form-from-motion and low-level motion perception from damage to superior temporal sulcus The perception of biological motion can be disrupted independently of static form, low-level motion, and form-from-motion. It appears that this can occur as a result of two distinct types of brain lesions, each discussed separately below. First, we will discuss dissociations after damage to regions in the superior temporal sulcus. In the next section, we will discuss a similar impairment after damage to regions of the parietal lobe. In one study (Vaina & Gross, 2004), patients JR, RJ, LH and IF were severely impaired at biological motion tasks, unable to identify human walkers in the displays. However, they were able to discriminate static shapes (i.e. they did not showing visual agnosia), and they could either (a) detect 2-D boundaries defined by motion (JR, RJ, LH and IF), (b) discriminate 2-D form-from-motion (i.e. squares and triangles) defined by direction (JR, RJ, LH), (c) discriminate 2-D form-from-motion defined by differences in speed (RJ, LH) and/or (d) identify 3-D form-from-motion (RJ). These patients were not tested on a motion coherence task so we have no information about their low-level motion perception. However, Billino et al. (2009) have recently reported two patients, AB and EB, who showed deficits in biological motion but not the low-level motion coherence tasks described above. Overall, these patients demonstrate that biological motion can be dissociated separately from static form, low-level motion, and non-biological form-from-motion (both 2-D and 3-D). In the patients described here, all have damage to lateral posterior and/or anterior temporal lobes, (including regions of superior temporal gyrus and the superior temporal sulcus), though damage is not exclusive to these areas in any case and there is wide-spread damage in some of the patients (see Table 2). Though this region is active in many cognitive tasks (including speech processing, face processing, audio visual integration, and reasoning about other people’s minds; Hein & Knight, 2008), this pattern strongly implicates the STS as the site of a specialized mechanism for processing biological motion. (Indeed the ability to process and represent human motion may be necessary for performing the diverse set of tasks listed above.) Supporting this conjecture are fMRI studies that have shown that the lateral superior temporal sulcus is preferentially active to biological motion stimuli compared to other motion stimuli (e.g. the motion of tools; Beauchamp, Lee, Haxby, & Martin, 2002; scrambled biological motion, Grossman & Blake, 2002; motion of point-light geometric forms, Bonda, Petrides, Ostry, & Evans, 1996). Further, electrodes over this region record differential brain activity to biological motion displays and random motion displays (Hirai, Fukushima, & Hiraki, 2003; Jokisch, Daum, Suchan, & Troje, 2005). Also, and perhaps most importantly, reverse lesioning of the posterior STS using repetitive transcranial magnetic stimulation impairs the perception of biological motion while stimulation of hMT+ does not (Grossman, Battelli, & Pascual-Leone, 2005). This finding is consistent with fMRI results showing distinct neural activity in superior temporal sulcus for biological motion stimuli (while hMT+ does not seem to discrimi-

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nate coherent motion stimuli vs. biological motion stimuli; Grossman et al., 2000). Together, the findings with patients suffering from low-level motion deficits and the findings of patients with impaired biological motion deficits demonstrate that the process underlying biological motion perception can be damaged selectively even when the perception of static form, low-level motion, and 2-D formfrom-motion remains intact. Further, this suggests that the processes underlying low-level motion perception are not necessary for efficient biological motion perception (see Billino et al., 2009 for similar conclusion). Indeed, though the low-level motion sensitive region hMT+ responds to biological motion, it does not seem to preferentially respond to biological motion vs. scrambled motion, nor does it discriminate between coherent motion and kinetic boundaries (Grossman et al., 2000; although see Vanduffel et al. (2002), for evidence that it discriminates between 2-D and 3-D motion). This suggests only a correlated relationship between the two in the healthy human brain. In addition to this, because damage in this region is not always associated with deficits in non-human form-from-motion perception, these patients show that the integrated form and motion information processed here might be specific to human forms in particular, and not object forms more generally. 2.2.2. Impaired biological motion perception with preserved low-level visual motion and static form, and form-from-motion perception from damage to regions of the parietal lobe As alluded to in the previous section, the perception of biological motion can be impaired with damage to regions other than the superior temporal lobe. In some patients, damage to regions of the parietal lobe (superior or inferior parietal lobe) seems to be sufficient to disrupt biological motion perception while sparing performance on the other perceptual tasks looked at here. Two patients, 34FM1 and 34FM2 (bilateral parietal lesions affecting supramarginal gyrus and superior parietal lobule; Schenk & Zihl, 1997) showed normal static form and low-level motion perception but could not identify point-light walkers on static or dynamic random-dot backgrounds. Tests of coherent motion, and static form perception were normal in these patients. Similarly, LL (right frontoparietal lesion) and UJ (left parietal lesion) (Billino et al., 2009) showed intact motion coherence thresholds but impaired biological motion discrimination. Further, patients JS (left angular and supramarginal gyrus) and JL (right superior parietal lobule) (Battelli, Cavanagh, & Thorton, 2003) were tested with form-from-motion and biological motion stimuli, and though both patients could perform a 2-D form-from-motion task in which they discriminated the orientation of a rectangle, they showed abnormal performance on either: (a) distinguishing gait direction (JS) or (b) discriminating between normal and scrambled point-light walkers (JL) in biological motion displays. Common to these patients is wide-spread damage that includes regions of the parietal lobe. Because parietal damage can lead to impairments of biological motion perception, we suggest that the superior/inferior parietal lobe remains a likely candidate for the integration of form and motion information in biological (and perhaps 3-D form-from-motion, to be described below) stimuli. There are a number of reasons we suggest this. First, though damage to the STS seems to impair biological motion perception, damage to the temporal lobes does not always lead to impairments in 3-D form-from-motion perception (though both of these tasks require perceptual integration of dots over space and time). In contrast, parietal damage seems to consistently impair biological motion and is also shown to impair 3-D form-from-motion. Therefore, it is likely that the STS does not take part in the integration process itself, but simply represents the human form derived from

Lowlevel motion

Static form

2-D formfrommotion

3-D formfrommotion

Biological motion

Ventral occipital cortex

O

X

O

O

O

MT/V5+ MT/V5+ Occipito-temporo-parietal junction (just posterior to MT/V5+) RH

X X X

O

O O O

Primary impairment

Patient ID

Reference

Reported damage

Static form

EW

Vaina (1994)

Basic motion

LM BC WK

McLeod et al. (1996) Vaina et al. (2002) Billino et al. (2009)

JR

Vaina & Gross (2004)

Biological motion (after temporal lesions)

RJ

Biological motion (after parietal lesions)

JS

JL 34FM1 34FM2 LL UJ Form-from-motion (3-D)

Form-from-motion (2-D)

AL

Billino et al. (2009) Battelli et al. (2003)

Schenk & Zihl, 1997) Billino et al. (2009) Cowey & Vaina (2000)

4 Patients

(Vaina, 1989)

1

Regan et al. (1992)

2 3 4 9 10 12 A-1 A-2 A-8 A-3 A-4 A-5 A-6 A-7 5 Patients

Blake et al. (2007)

O

RH lateral/anterior temporal lobe, extending into parietal lobe (also basal ganglia and globus pallidus)

O

O

X

X

RH convexity of temporal lobe (extension into basal ganglia, posterior-lateral frontal and parietal lobes) RH anterior portion of the temporal lobe (posterior portion of internal capsule) RH, anterior portion of superior temporal lobe RH posterior temporal RH vicinity of STS

O

O

O

X

O O

O X

X X

X X X X

O O

LH angular and supramarginal gyrus

RH superior parietal lobule BL supramarginal gyrus, superior parietal lobule BL supramarginal gyrus, superior parietal lobule RH parietal LH parietal

O

X

O

X X X X X

O O O O

O O

LH medial inferior temporal lobe, hippocampus, parahippocampal gyrus extending into posterior parietal lobe and into the medial temporal lobe, thalamus, and posterior internal capsule RH occipitoparietal lesions

O*

O

X

X

O

X

Wide spread lesions in ventral occipital cortex; overlap in parieto-temporal white matter underlying fusiform gyrus RH LH RH LH RH LH RH Basal temporo-occipital cortex; overlap in lingual, parahippocampal, posterior fusiform, underlying white matter; LH RH RH RH LH RH RH LH RH occipitotemporal lesions

O

O

X

O O O O O O O

O O O O O O

X X X X X X X

X

O O O O O O O O

X X X X X X X X 

X

O

Abbreviations: LH – left hemisphere; RH – right hemisphere; hMT+/V5 – human homologue V5/posterior middle temporal gyrus; STS – superior temporal sulcus; ( ) – indicates that no direct test of the perceptual ability was performed but could be inferred from observation.

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LH IF AB EB

O

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Table 2 Summary of neuropsychological dissociations. ‘O’ indicates intact ability, ‘X’ indicates impaired ability. If the patient was not tested the field has been left blank. The reported damage includes major sites of impairment. In some cases, more detailed information was provided for the patient(s) and is provided here.

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information that has already been integrated by parietal mechanisms. A similar suggestion has been made by other authors (Regan et al., 1992). Importantly, fMRI studies have revealed activity in the parietal cortex during passive viewing of biological motion displays (Peuskens et al., 2005). Before we leave this issue, it is important to note that, though parietal regions may take part integrating form and motion information for the perception of biological motion, it is clear that this region does not participate in this task exclusively. Indeed, it has been shown that parietal regions participate in processing object location, as well as object shape information (e.g. Denys et al., 2004), especially when it is defined by binocular cues (e.g. see Orban et al., 2006). When taken together, it seems that the parietal region may be capable of integrating form and motion information because of its involvement in directing visuomotor behaviour, a task that requires analyzing the volumetric properties of objects and integrating the motion of form information over time (both of the hand and of the visual target). The idea that the inferior or superior parietal lobes are important for integrating motion signals in higher order visual tasks has been suggested before. For instance Battelli, Pascual-Leone, and Cavanagh (2007) suggest that this region is important for specifying the elements of a visual display and the order of their appearance within different regions of space. Though the damage to the parietal regions of the patients reviewed here is non-specific, and though it is clear that these regions are involved in a diverse set of processing tasks, we suggest that the regions of the parietal lobe also participate in integrating the form and motion information in biological motion displays (and perhaps 3-D form-from-motion displays). 2.3. Impaired form-from-motion perception (2-D or 3-D) with preserved static form and low-level motion perception Many patients demonstrate a dissociation between static form perception and 2-D form-from-motion, or a dissociation between low-level motion and 2-D form-from-motion. Specifically, seven patients (three left hemisphere, four right) (Regan et al., 1992) showed normal motion detection and static form perception but impaired detection and/or recognition of motion-defined letters. Eight other patients (Blake et al., 2007) showed normal thresholds in a coherence motion task but elevated thresholds on a 2-D formfrom-motion task. None of these patients were tested on 3-D form-from-motion tasks. However, impaired 3-D form-from-motion with intact low-level motion and static form was shown in patient AL (Cowey & Vaina, 2000).1 However this patient also showed impairments in biological motion displays. Though 2-D and 3-D form-from-motion can be spared despite impaired biological motion perception (see Section 2.2.1), the opposite pattern has not been reported; specifically, no patient with impaired 2-D or 3-D form-from-motion but spared biological motion appears in the literature reviewed here. In fact, few patients with clear deficits in form-from-motion perception have been tested with biological motion displays. As far as we know, there are no reports in the literature of a patient who shows impaired form-from-motion perception but spared biological motion perception. Thus, the relationship between formfrom-motion perception and biological motion perception remains unclear within this neuropsychological literature and is one of the most important avenues for future research. This ambiguity is highlighted in the discussion of possible neurocognitive models below.

1 Patient AL shows wide-spread damage and demonstrates deficits in all formfrom-motion displays (2-D, 3-D, and biological), making it difficult to classify her. For simplicity, we have included her in form-from-motion group.

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Though there is wide-spread damage in many of the cases of impaired form-from-motion processing, common to the patients is damage to ventral occipito-temporal cortex, involving regions associated with the lateral occipital complex (i.e. LOC, overlap in posterior regions of fusiform gyrus, although the damage is often extensive, commonly involving underlying white matter). Other areas listed include the lingual and parahippocampal cortices and parieto-temporal white matter. Consistent with this are fMRI results that reveal increased activation of LOC and other ventral occipitotemporal sites to form-from-motion stimuli (e.g. Dupont et al., 1997; Grezes et al., 2001). Importantly, this increase in activity is not necessarily seen in the STS, where biological motion displays increase activity. Also, within this region there seems to be little overlap of activation to static form stimuli (defined by colour) and form-from-motion (Gulyas, Heywood, Popplewell, Roland, & Cowey, 1994), suggesting that, though these perceptual abilities rely on processing in anatomical regions of the ventral temporal lobes, including LOC, performance on discriminating or detecting non-human static form and non-human form-from-motion relies on functionally distinct regions. Though it is difficult to make strong conclusions about the anatomical basis of deficits in 2-D and 3-D form-from-motion, the dissociations identified above do support the notion that the ability to explicitly identify or discriminate form-from-motion does not rely on the ability to discriminate low-level motion or static form. Again this is supported by a small body of fMRI results showing that hMT+/V5 may only have a correlational role form-from-motion perception. First, it has been shown that though hMT+ is activated to kinetic and luminance defined gratings it does not discriminate between them; also, the cortical regions that respond to kinetic contours and those that respond to uniform dot motion are different (Orban et al., 1995), providing some evidence that they are specializing in different tasks (and dissociable). Further, in a form-from-motion illusion, in which the subjective experience of a form defined by motion persists momentarily after the motion in the display has stopped, two different patterns of activity are observed in hMT+ and LOC; hMT+ is active only when motion is present in the display, whereas the LOC remains active while the subjective experience of a form continues. This has been taken as evidence that the LOC can represent form-from-motion in the absence of ongoing activity in hMT+ (Ferber, Humphrey, & Vilis, 2003). Finally, an investigation of the relationship between activation of area hMT+ and ventral temporal cortex to form-from-motion stimuli using both event related potentials and fMRI has shown that both regions are activated simultaneously at approximately 200–260 ms (Wang et al., 1999) suggesting that neither area depends on the other during this task, but instead receives information in parallel from earlier processing stages. Overall, it appears that regions of LOC process integrated form and motion information when they signal a non-human form (2-D and 3-D), and this region may be able to do so without input from ventral temporal regions necessary for explicit static form recognition or input from dorsal regions necessary for explicit low-level motion perception. There is at least one important unresolved question that arises from the literature with patients showing impairments in 2-D and 3-D form-from-motion perception. The dissociations reported here show that some patients with damage to the parietal lobe are impaired with biological motion stimuli but not 2-D form-from-motion stimuli. We have suggested that the parietal lobe serves to functionally integrate the motion of dots over time and space in the biological motion display. If this is so, the dissociation between biological motion and 2-D form-from-motion in parietal patients suggests that parietal areas may not integrate information for 2-D form-from-motion stimuli in the same way as it does for biological motion. Importantly, Vaina (1989) has shown a double

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dissociation between 2-D and 3-D form-from-motion. As mentioned earlier she suggests that 2-D form-from-motion relies on processes of ‘segregation’ (perceptually segregating foreground from background using local motion cues), and is disrupted after damage to the temporal lobe, whereas 3-D form-from-motion relies on processes of ‘integration’ (perceptually integrating the motion of dots over time and space) which is disrupted after damage to the parietal lobe. This dissociation strongly suggests that 2-D and 3-D form-from-motion stimuli are processed by functionally distinct mechanisms, perhaps with 3-D form-from-motion stimuli relying more on parietal ‘integration’ than 2-D stimuli. Overall, there is enough evidence to suggest that 2-D and 3-D form-frommotion may be processed by functionally distinct mechanisms. This has important consequences for understanding the organization of the visual cortices and is addressed in the discussion of the neurocognitive model presented in the next section. 3. Summary, model, and predictions A summary of the dissociations reviewed here is presented in Table 2. As can be seen across all of the patients discussed, every dissociation is shown except double dissociation between form-frommotion perception and biological motion perception. As mentioned throughout the review, these dissociations lead to a number of counter-intuitive conclusions that have important consequences for neurocognitive models of form and motion processing within the human visual system. Specifically, the perception of formfrom-motion (both 2-D and 3-D) and biological motion can persist despite deficits in low-level motion perception or static form perception. These dissociations are counter-intuitive because it is often assumed that form-from-motion perception and biological motion perception should depend on the interaction between low-level motion and static form processes, and it is surprising that visual forms can be derived from motion cues in visual agnosics, (see Farah, 1990, pp. 14–15) and some motion information can be used in akinetopsics. Indeed, this assumption is fostered by fMRI studies showing that the areas of the brain known to process basic motion – hMT+ – and static form – LOC – are active when formfrom-motion is processed (e.g. Ferber et al., 2003). Further, as described in Section 1, current theories posit that ventral visual areas sensitive to form and dorsal visual areas sensitive to motion either share information or send information to separate brain regions that both integrate and represent the two types of information. However, the dissociations reviewed here suggest a more complicated functional relationship between areas that process motion and form within the visual system, as discussed below. Using the neuropsychological and functional imaging results reviewed here we can attempt a simple functional neurocognitive description like the one in Fig. 1. In this model, the boxes represent functionally distinct mechanisms responsible for processing a particular type of visual information, or performing some transformation on it. The arrows represent functional connections (not necessarily anatomical) between these mechanisms and therefore separate boxes in the model may be processed within the same broadly defined anatomical regions (e.g. LOC; see shaded area). We identify anatomical candidates for the various mechanisms based on the gross lesions reported in the neuropsychological literature, fMRI studies of various perceptual abilities, and what is known from neurophysiological studies in the non-human primate; however, we emphasize that the mapping of the functional relationships between these processes and the associated neuroanatomy is only coarse and tentative, as we are unable to draw anatomically specific conclusions based on the neuropsychological literature here. We would also like to emphasize that the relationships highlighted here are functional, and we recognize that in the

healthy human brain all of these mechanisms are likely involved in processing a moving object. Before elaborating on this model, we will highlight the features common to previous descriptions of the human visual system (e.g. the two-streams hypothesis; Milner & Goodale, 1995) and models of the neuroanatomy of the non-human primate visual system known from histological studies (e.g. Felleman & van Essen, 1991; Van Essen, Anderson, & Felleman, 1992). Functionally, the visual system is parsed into two relatively independent streams (white boxes and connections 1a and 1b). As mentioned previously, the relative independence of these two streams is of ongoing debate (see Husain & Nachev, 2006; McIntosh & Schenk, 2009), and we recognize that form and motion processing are not the exclusive enterprises of either visual stream. To avoid this contentious issue, the presented model highlights only the gross functional relationships associated with particular visual deficits. Two main features of the presented model are consistent with neuropsychological literature and have been known for some time. First, early processing of form and motion takes place relatively independently, likely in areas V4 and V3/V3a (see Goodale & Milner, 1992). These modules have slightly more elaborate processing characteristics than the simple edge/line and motion/direction detection of V1, for example, sensitivity to complex shapes and global motion, respectively (see Grill-Spector & Malach, 2004; Livingstone & Hubel, 1988). From there, motion analysis continues in higher motion centers such as hMT+/V5 and is necessary normal coherence motion detection (and perhaps conscious access to the perception of motion – as damage to this area results in the ‘‘motion blind” phenomena described earlier, McLeod et al., 1996). Further, information about the static form of an object seems to continue into the ventral temporal cortex. Regions here are necessary for the successful perception of static form (and perhaps conscious access to the perception of static form – as damage to this area results in deficits in static form perception and object recognition, i.e. agnosia). However, the presented model needs to account for the findings that form-from-motion and biological motion perception can persist in the absence of static form or low-level motion perception (grey boxes). In the organization of Fig. 1, we suggest that separate, parallel pathways (connections 2a and 2b) feed into a mechanism that integrates the motion of the dots over time and space. Damage to regions of the parietal lobe eliminate the ability to perceive biological motion and sometimes 3-D form-from-motion, as in patient AL (though whether this is the case consistently remains unclear) and therefore this region is a likely candidate for the site of integration. We suggest however, that the parietal region does not represent the information about biological or 3-D forms. This is supported by the finding that biological motion perception can be impaired with damage to the STS, a candidate implicated in fMRI, and that forms activate regions of LOC. This suggests that the STS and the LOC receive functional connections from the parietal lobe (connections 3a and 3b), and represent the information in biological motion and 3-D form-from-motion stimuli, respectively. The separation of 3-D form-from-motion and biological motion processing is supported by the finding that they are not always impaired together (as damage to the STS does not necessarily impair 3-D form-from-motion). It appears that the STS is particularly sensitive to whether the form-from-motion stimulus signals the presence of a human actor, and may participate in representing human form-from-motion but not non-human forms; LOC on the other hand, seems to signal the presence of object form in general. Importantly, the suggested role of the parietal lobe for integrating the motion of the dots over time and space in these displays is consistent with the more recent conclusion that regions of the parietal lobe are responsible for more general integration of visual information over time and space and, in particular, its importance

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Biological Motion (STS/STG)

Low-level Motion (hMT+)

3-D FFM 3a

(LOC)

3b

Explicit Form

Integration (SPL/IPL)

1a

2a

Motion (V3)

1b

2b

Form (V4)

4

1a

(LOC)

2-D FFM (LOC)

1b

Low Level Analysis (V1)

Fig. 1. Proposed functional connections of modules processing different types of visual information that support successful discrimination or identification of low-level motion, static form, 2-D and 3-D form-from-motion, and biological motion. All proposed connections are functional. Based on the neuropsychological dissociations reviewed here, we list the sites of gross cortical damage common to patients that show impairments in associated tasks. Highlighted in grey are primary dissociations revealed by the attached review.

for keeping track of the order of events (Battelli et al., 2007). Future research should address this issue by investigating the parietal lobes involvement in tasks of biological and 3-D form-from-motion perception. The present model also needs to account for the finding that 2-D and 3-D form-from-motion are dissociated. Assuming that the perception of 2-D and 3-D form-from-motion require different types of analyses, the model in Fig. 1 treats 2-D and 3-D form-from-motion perception separately. This is done for a number of reasons. First, biological motion has been dissociated 2-D from formfrom-motion, and 2-D and 3-D form-from-motion have been dissociated from each other (Vaina, 1989). Because 3-D form-from-motion displays and biological motion displays both require perceptual integration of the dots over time and space, we have hypothesized that the integration mechanism of the parietal lobe functionally participates in tasks of 3-D and biological motion perception; however, because 2-D form-from-motion likely depends on a mechanism responsible for segregating foreground from background, the parietal integration mechanism likely does not participate in this task; further, parietal damage does not necessarily impair 2-D form-from-motion perception. Again, this is consistent with Vaina’s (1989) suggestion that 3-D form-from-motion stimuli (and we can extend this to biological motion stimuli) require integration of dots over time, whereas 2-D requires visual segregation. The importance of this distinction needs to be emphasized. This could suggest that 2-D form-from-motion may actually depend on ‘crosstalk’ between the ventral and dorsal streams (connection 4), though it would not rely on crosstalk between regions important for ‘conscious’ perception of static form or low-level motion (this has been demonstrated by the lack of direct functional connection between the two). Overall, the neuropsychological evidence suggests that, though non-human form is processed by regions of the LOC and other temporal sites, there are functional dissociations between the static form, 2-D and 3-D form-from-motion. Our model makes these functional divisions explicit, though the scope of the review limits our ability to describe the functional neuroanatomy of the subregions within LOC.

Though the neurocognitive model presented here is based on imperfect simplifications from a diverse set of reported case studies, it is important to note that the proposed connections are physiologically plausible. Indeed, histological studies in non-human primates have shown that most early visual areas are reciprocally connected, and early visual areas like V3 and V4 project to regions of the parietal lobe (see Felleman & Van Essen, 1991). Further, though regions of the parietal lobe are sparsely directly connected to the temporal lobe, they are widely connected with frontal regions which are reciprocally connected with regions of the temporal lobe. This is important because some of the connections highlighted in the model may be functional rather than directly anatomical (i.e. two disparate regions with processes that are engaged simultaneously and together form an associative network). The organization we present here lends itself to further investigation with neuropsychological patients and imaging techniques. The types of investigations we highlight here will be critical in determining the relationships between higher order visual areas that are responsible for form and motion processing. First, a double dissociation between form-from-motion and biological motion has not been shown, so the relationship between the two processes remains speculative. The model we present here suggests that integration mechanisms of the parietal lobes are involved in 3-D form-from-motion and biological motion separately, but more direct tests of this are needed. Further, it is necessary to determine in more detail the relationship between 2-D and 3-D form-from-motion processing and their relationship to biological motion processing. Can biological motion processing persist despite impairments in 2-D or 3-D form-from-motion, or both? Finally, future work can explore the suggested functional relationships between these areas using new analysis techniques for fMRI data sets (e.g. the structural equation modeling procedures of Zhuang et al. (2008)). 4. Conclusions Studies with neuropsychological patients that have investigated form and motion perception with the use of different static form, coherence motion, form-from-motion, and biological motion

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stimuli reveal a complex pattern of impairments that implicate dissociable processes within the ventral and dorsal streams. Counter-intuitively, it appears that intact perception of higher-order form-from-motion stimuli can persist despite altered perception of low-level motion and static form. The neurocognitive model presented here attempts to account for these dissociations and present directions for future research and should assist in further neuropsychological investigations. References Adamo, M., & Ferber, S. (2009). A picture says more than a thousand words: Behavioural and ERP evidence for attentional enhancements due to action affordances. Neuropsychologia, 47, 1600–1608. Baizer, J. S., Ungerleider, L. G., & Desimone, R. (1991). Organization of visual inputs to the inferior temporal and posterior parietal cortex in macaques. The Journal of Neuroscience, 1(11), 168–190. Baker, C. L., Hess, R. F., & Zihl, J. (1991). Residual motion perception in a ‘motionblind’ patient, assessed with limited-lifetime random dot stimuli. The Journal of Neuroscience, 11(2), 454–461. Battelli, L., Cavanagh, P., & Thornton, I. M. (2003). Perception of biological motion in parietal patients. Neuropsychologia, 41, 1808–1816. Battelli, L., Pascual-Leone, A., & Cavanagh, P. (2007). The ‘when’ pathway of the right parietal lobe. Trends in Cognitive Sciences, 11(5), 204–210. Beauchamp, M. S., Lee, K. E., Haxby, J. V., & Martin, A. (2002). FMRI responses to video and point-light displays of moving humans and manipulable objects. Journal of Cognitive Neuroscience, 15(7), 991–1001. Billino, J., Braun, D. L., Bohm, K.-D., Bremmer, F., & Gegenfurter, K. R. (2009). Cortical networks for motion processing: Effects of focal brain lesions on perception of different motion types. Neuropsychologia, 47(10), 2133–2144. Blake, O., Brooks, A., Mercier, M., Spinelli, L., Adriani, M., Lavanchi, L., et al. (2007). Distinct mechanisms of form-from-motion perception in human extrastriate cortex. Neuropsychologia, 45, 644–653. Bonda, E., Petrides, M., Ostry, D., & Evans, A. (1996). Specific involvement of human parietal systems and the amygdale in the perception of biological motion. The Journal of Neuroscience, 16(11), 3737–3744. Bruno, N., & Franz, V. H. (2009). When is grasping affected by the Muller–Lyer illusion? A quantitative review. Neuropsychologia, 47, 1421–1433. Cowey, A., & Vaina, LM. (2000). Blindness to form from motion despite intact static form perception and motion detection. Neuropsychologia, 38, 566–578. Denys, K., Vanduffel, W., Fize, D., Nelissen, K., Peuskens, H., Van Essen, D., et al. (2004). The processing of visual shape in the cerebral cortex of human and nonhuman primates: A functional magnetic resonance imaging study. The Journal of Neuroscience, 24(10), 2551–2565. Durand, J.-B., Nelissen, K., Joly, O., Wardak, C., Todd, J. T., Norman, J. F., et al. (2007). Anterior regions of monkey parietal cortex process visual 3D shape. Neuron, 55, 493–505. Dupont, P., de Bruyn, B., Vandenberghe, R., Rosier, A.-M., Michiels, J., Marchal, G., et al. (1997). The kinetic occipital region in human visual cortex. Cerebral Cortex, 7, 283–292. Farah, M. J. (1990). Visual agnosia: Disorders of object recognition and what they tell us about normal vision. Cambridge, MA: MIT Press/Bradford Books. Farah, M. J., Wilson, K. D., Drain, H. M., & Tanaka, J. R. (1995). The inverted face inversion effect in prosopagnosia: Evidence for mandatory, face-specific perceptual mechanisms. Vision Research, 35(14), 2089–2093. Felleman, D. J., & Van Essen, D. C. (1991). Distributed hierarchical processing in the primate cerebral cortex. Cerebral cortex, 1, 1047–3211. Ferber, S., Humphrey, K. J., & Vilis, T. (2003). The lateral occipital complex subserves the perceptual persistence of motion-defined groupings. Cerebral Cortex, 13, 716–721. Georgieva, S., Peeters, R., Kolster, H., Todd, J. T., & Orban, G. A. (2009). The processing of three-dimensional shape from disparity in the human brain. The Journal of Neuroscience, 29(3), 727–742. Goodale, M. A., & Milner, A. D. (1992). Separate visual pathways for perception and action. Trends in Neurosciences, 15, 20–25. Grezes, J., Fonlupt, P., Bertenthal, B., Delon-Martin, C., Segebarth, C., & Decety, J. (2001). Does perception of biological motion rely on specific brain regions. NeuroImage, 13, 775–785. Grill-Spector (2003). The neural basis of object perception. Current Opinion in Neurobiology, 13, 1–8. Grill-Spector, K., & Malach, R. (2004). The human visual cortex. Annual Reviews of Neuroscience, 27, 649–677. Grossman, E. D., Battelli, L., & Pascual-Leone, A. (2005). Repetitive TMS over posterior STS disrupts perception of biological motion. Vision Research, 45, 2847–2853. Grossman, E. D., & Blake, R. (2002). Brain areas active during visual perception of biological motion. Neuron, 35, 1167–1175. Grossman, E., Donnelly, M., Price, R., Pickens, D., Morgan, V., Neighbor, G., et al. (2000). Brain areas involved in the perception of biological motion. Journal of Cognitive Neuroscience, 12(5), 711–720.

Gulyas, B., Heywood, C. A., Popplewell, D. A., Roland, P. E., & Cowey, A. (1994). Visual form discrimination from color or motion cues: Functional anatomy by positron emission tomography. Proceedings of the National Academy of Science, 91, 9965–9969. Hein, G., & Knight, R. T. (2008). Superior temporal sulcus – It’s my area: Or is it? Journal of Cognitive Neuroscience, 20(12), 2125–2136. Hirai, M., Fukushima, H., & Hiraki, K. (2003). An event-related potentials study of biological motion perception in humans. Neuroscience Letters, 41, 44. Husain, M., & Nachev, P. (2006). Space and the parietal cortex. Trends in Cognitive Science, 11(1), 30–36. Ishai, A., Ungerleider, L. G., Martin, A., & Haxby, J. V. (2000). The representation of objects in the human occipital and temporal cortex. Journal of Cognitive Neuroscience, 12(Suppl. 2), 35–51. Johansson, G. (1973). Visual perception of biological motion and a model of its analysis. Perception and Psychophysics, 14, 202–211. Jokisch, D., Daum, I., Suchan, B., & Troje, N. F. (2005). Structural encoding and recognition of biological motion: Evidence from event-related potentials and source analysis. Behavioural Brain Research, 157, 195–204. Kourtzi, Z., Bulthoff, H. H., Erb, M., & Grodd, W. (2002). Object-selective responses in the human motion area MT/MST. Nature Neuroscience, 5(1), 17–18. Livingstone, M., & Hubel, D. (1988). Segregation of from, color, movement, and depth: Anatomy, physiology, and perception. Science, 240(4853), 740–749. McIntosh, R. D., & Schenk, T. (2009). Two visual streams for perception and action: Current trends. Neuropsychologia, 47, 1391–1396. McLeod, P., Dittrich, W., Driver, J., Perrett, D., & Zihl, J. (1996). Preserved and impaired detection of structure from motion by a ‘motion-blind’ patient. Visual Cognition, 3(4), 363–391. Milner, A. D., & Goodale, M. A. (1995). The visual brain in action. Oxford: Oxford University Press. Milner, A. D., & Goodale, M. A. (2008). Two visual systems re-viewed. Neuropsychologia, 46, 774–785. Orban, G. A., Claeys, K., Nelissen, K., Smans, R., Sunaert, S., Todd, J. T., et al. (2006). Mapping the parietal cortex of human and non-human primates. Neuropsychologia, 44, 2647–2667. Orban, G. A., Dupont, P., De Bruyn, B., Vogels, R., Vandenberghe, R., & Mortelmans, L. (1995). A motion area in human visual cortex. Proceedings of the National Academy of Sciences, 92, 993–997. Peuskens, H., Vanerie, J., Verfaillie, K., & Orban, G. A. (2005). Specificity of regions processing biological motion. European Journal of Neuroscience, 21, 2864–2875. Rizzo, M., NAwrot, M., & Zihl, J. (1995). Motion and shape perception in cerebral akinetopsia. Brain, 118, 1105–1127. Schenk, T., & Zihl, J. (1997). Visual motion perception after brain damage: I. Deficits in global motion perception. Neuropsychologia, 35(9), 1289–1297. Sumi, S. (1984). Upside-down presentation of the Johansson moving light-spot pattern. Perception, 13, 283–286. Sunaert, S., Hecke, P. V., Marchal, G., & Orban, G. A. (1999). Motion-responsive regions of the human brain. Experimental Brain Research, 127, 355–370. Regan, D., Giaschi, D., Sharpe, J. A., & Hong, X. H. (1992). Visual processing of motion-defined form: Selective failure in patients with parietotemporal lesions. The Journal of Neuroscience, 12(6), 2198–2210. Tootell, R. B. H., Reppas, J. B., Kwong, K. K., Malach, R., Born, R. T., Brady, T. J., et al. (1995). Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging. The Journal of Neuroscience, 15(4), 3215–3230. Vaina, L. M. (1989). Selective impairment of visual motion interpretation following lesions of the right occipito-parietal area in humans. Biological Cybernetics, 61, 347–359. Vaina, L. M. (1994). Functional segregation of colour and motion processing in the human visual cortex: Clinical evidence. Cerebral Cortex, 5, 555–572. Vaina, L. M., & Gross, C. G. (2004). Perceptual deficits in patients with impaired recognition of biological motion after temporal lobe lesions. Proceedings of the National Academy of Sciences, 101(48), 16947–16951. Vaina, L. M., Cowey, A., LeMay, M., Bienfang, D. C., & Kikinis, R. (2002). Visual deficits in a patient with ‘kaleidoscopic disintegration of the visual world’. European Journal of Neurology, 9, 463–477. Vaina, L. M., Lemay, M., Bienfang, D. C., Choi, A. Y., & Nakayama, K. (1990). Intact ‘biological motion’ and ‘structure from motion’ perception in a patient with impaired motion mechanisms: A case study. Visual Neuroscience, 5(4), 353– 369. Vanduffel, W., Fize, D., Peuskens, H., Denys, K., Sunaert, S., Todd, J. T., et al. (2002). Extracting 3D from motion: Differences in human and monkey intraparietal cortex. Science, 298(11), 413–415. Van Essen, D. C., Anderson, C. H., & Felleman, D. J. (1992). Information processing in the primate visual system: An integrated systems perspective. Science, 255(5043), 419–423. Wang, J., Zhou, T., Qiu, M., Du, A., Cai, K., Wang, Z., et al. (1999). Relationship between ventral stream for object vision and dorsal stream for spatial vision: An fMRI and ERP study. Human Brain Mapping, 8, 170–181. Zhuang, J., Peltier, S., He, S., LaConte, S., & Hu, X. (2008). Mapping the connectivity with structural equation modeling in an fMRI study of shape-from-motion task. NeuroImage, 42, 799–806. Zihl, J., Von Cramon, D., & Mai, N. (1983). Selective disturbance of movement vision after bilateral brain damage. Brain, 106, 313–340.