Ventral Stream Damage Research Articles

Dysfunctional tissue correlates of unrelated naming errors in acute left hemisphere stroke

ABSTRACT Most naming error lesion-symptom mapping (LSM) studies have focused on semantic and/or phonological errors. Anomic individuals also produce unrelated word errors, which may be linked to semantic or modality-independent lexical deficits. To investigate the neural underpinnings of rarely-studied unrelated errors, we conducted LSM analyses in 100 individuals hospitalised with a left hemisphere stroke who completed imaging protocols and language assessments. We used least absolute shrinkage and selection operator regression to capture relationships between naming errors and dysfunctional brain tissue metrics (regional damage or hypoperfusion in vascular territories) in two groups: participants with and without impaired single-word auditory comprehension. Hypoperfusion—particularly within the parietal lobe—was an important error predictor, especially for the unimpaired group. In both groups, higher unrelated error proportions were associated with primarily ventral stream damage, the language route critical for processing meaning. Nonetheless, brain metrics implicated in unrelated errors were distinct from semantic error correlates.

The ability to recall scenes is a stable individual difference: Evidence from autobiographical remembering

Four behavioral studies (ns ~ 200 to 400) extended neural studies of ventral stream damage and fMRI activation and behavioral studies of scene recall conducted on individual memories to individual differences in normal populations. Ratings of scene and contents were made on one set of autobiographical memories. Ratings of reliving, vividness, belief, emotional intensity, and temporal specificity were made on different memories. Thus, correlations between these ratings were due to variability in the participants, not the events remembered. Scene correlated more highly than contents with reliving, vividness, belief, and emotional intensity but not temporal specificity. Scene correlated more highly than other visual imagery tests with reliving, vividness, and belief. Scene correlated with individual differences tests of episodic memories and future events more highly than it did with tests of semantic memory and spatial navigation abilities. Moreover, scene had high test-retest correlations measured at periods of up to one month. The ability to recall scenes is a stable disposition, with both convergent and divergent validity, which predicts basic qualities of autobiographical memories. A Scene Recall Imagery Test is introduced.

Types of naming errors in chronic post-stroke aphasia are dissociated by dual stream axonal loss

The types of errors during speech production can vary across individuals with chronic post-stroke aphasia, possibly due to the location and extent of brain damage. In this study, we evaluated the relationship between semantic vs. phonemic errors during confrontational naming, and their relationship with the degree of damage to ventral and dorsal white matter pathways extending beyond the necrotic stroke lesion. Based on the dual stream model of language processing, we tested the hypothesis that semantic errors would be associated with ventral stream damage, whereas phonemic errors would be associated with dorsal stream damage, but not vice-versa. Multi-shell diffusion MRI was used to obtain kurtosis-based white matter tractography from 32 chronic stroke survivors. Using diffusion microstructural tissue modeling, we estimated axonal loss along the length of the inferior and superior longitudinal fasciculi (ILF and SLF), representing the main pathways in the ventral and dorsal streams, respectively. The frequency of semantic paraphasias was strongly associated with ILF axonal loss, whereas phonemic paraphasias were strongly associated with SLF axonal loss, but not vice versa. This dissociation between semantic and phonological processing is in agreement with the dual stream model of language processing and corroborates the concept that, during speech production, knowledge association (semantics) depends on the integrity of ventral, whereas form encoding (phonological encoding) is more localized to dorsal pathways. These findings also demonstrate the importance of the residual integrity of specific white matter pathways beyond regional gray matter damage for speech production.

Memory-guided reaching in a patient with visual hemiagnosia

The two-visual-systems hypothesis (TVSH) postulates that memory-guided movements rely on intact functions of the ventral stream. Its particular importance for memory-guided actions was initially inferred from behavioral dissociations in the well-known patient DF. Despite of rather accurate reaching and grasping movements to visible targets, she demonstrated grossly impaired memory-guided grasping as much as impaired memory-guided reaching. These dissociations were later complemented by apparently reversed dissociations in patients with dorsal damage and optic ataxia. However, grasping studies in DF and optic ataxia patients differed with respect to the retinotopic position of target objects, questioning the interpretation of the respective findings as a double dissociation. In contrast, the findings for reaching errors in both types of patients came from similar peripheral target presentations. However, new data on brain structural changes and visuomotor deficits in DF also questioned the validity of a double dissociation in reaching. A severe visuospatial short-term memory deficit in DF further questioned the specificity of her memory-guided reaching deficit. Therefore, we compared movement accuracy in visually-guided and memory-guided reaching in a new patient who suffered a confined unilateral damage to the ventral visual system due to stroke. Our results indeed support previous descriptions of memory-guided movements' inaccuracies in DF. Furthermore, our data suggest that recently discovered optic-ataxia like misreaching in DF is most likely caused by her parieto-occipital and not by her ventral stream damage. Finally, multiple visuospatial memory measurements in HWS suggest that inaccuracies in memory-guided reaching tasks in patients with ventral damage cannot be explained by visuospatial short-term memory or perceptual deficits, but by a specific deficit in visuomotor processing.

Patient DF’s visual brain in action: Visual feedforward control in visual form agnosia

Patient DF, who developed visual form agnosia following ventral-stream damage, is unable to discriminate the width of objects, performing at chance, for example, when asked to open her thumb and forefinger a matching amount. Remarkably, however, DF adjusts her hand aperture to accommodate the width of objects when reaching out to pick them up (grip scaling). While this spared ability to grasp objects is presumed to be mediated by visuomotor modules in her relatively intact dorsal stream, it is possible that it may rely abnormally on online visual or haptic feedback. We report here that DF’s grip scaling remained intact when her vision was completely suppressed during grasp movements, and it still dissociated sharply from her poor perceptual estimates of target size. We then tested whether providing trial-by-trial haptic feedback after making such perceptual estimates might improve DF’s performance, but found that they remained significantly impaired. In a final experiment, we re-examined whether DF’s grip scaling depends on receiving veridical haptic feedback during grasping. In one condition, the haptic feedback was identical to the visual targets. In a second condition, the haptic feedback was of a constant intermediate width while the visual target varied trial by trial. Despite this incongruent feedback, DF still scaled her grip aperture to the visual widths of the target blocks, showing only normal adaptation to the false haptically-experienced width. Taken together, these results strengthen the view that DF’s spared grasping relies on a normal mode of dorsal-stream functioning, based chiefly on visual feedforward processing.

Delayed action does not always require the ventral stream: A study on a patient with visual form agnosia

It has been suggested that while movements directed at visible targets are processed within the dorsal stream, movements executed after delay rely on the visual representations of the ventral stream (Milner & Goodale, 2006). This interpretation is supported by the observation that a patient with ventral stream damage (D.F.) has trouble performing accurate movements after a delay, but performs normally when the target is visible during movement programming. We tested D.F.'s visuomotor performance in a letter-posting task whilst varying the amount of visual feedback available. Additionally, we also varied whether D.F. received tactile feedback at the end of each trial (posting through a letter box vs posting on a screen) and whether environmental cues were available during the delay period (removing the target only vs suppressing vision completely with shutter glasses). We found that in the absence of environmental cues patient D.F. was unaffected by the introduction of delay and performed as accurately as healthy controls. However, when environmental cues and vision of the moving hand were available during and after the delay period, D.F.'s visuomotor performance was impaired. Thus, while healthy controls benefit from the availability of environmental landmarks and/or visual feedback of the moving hand, such cues seem less beneficial to D.F. Taken together our findings suggest that ventral stream damage does not always impact the ability to make delayed movements but compromises the ability to use environmental landmarks and visual feedback efficiently.

DF's visual brain in action: The role of tactile cues

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

Task- and response related dissociations between neglect in near and far space: a morphometric case study.

Introduction: Patients with unilateral neglect may show line bisection errors selectively in either near (within hand reaching) or far (beyond hand reaching) space which suggests that these two spatial areas are coded differently by the brain. This exploratory study investigated, whether any difference in performance between these spatial domains might be task-independent or modulated by the requirement for a motor response.Methods: A 31-year-old right brain damaged patient (MF) and a group of age matched healthy controls were assessed with two serial visual search tasks and a Landmark paradigm. Both types of task required either a directional (pointing) or non-directional (button press) motor response. Participants were assessed with both task types and response modes in near (57 cm) and far space (114 cm).Results: MF showed left neglect during visual search only in far space for the perceptual condition and in near space for the motor condition. MF showed no neglect in both versions of the Landmark task irrespective of spatial distance. A voxel-based morphometric assessment of MF's brain lesion showed marked damage in the right ventro-temporal cortex, superior temporal gyrus, insula, inferior frontal gyrus, angular gyrus and bilaterally in the posterior cingulate cortex.Conclusions: Our preliminary findings suggest that processing of far space during visual search is associated with ventral stream damage but only when space is coded through visual information. Neglect involving directional motor activity in near space seems to be associated with damage of structures sharing close connections with the dorsal stream.

Task- and Response Related Dissociations between Neglect in Near and Far Space: A Morphometric Case Study

Introduction: Patients with unilateral neglect may show line bisection errors selectively in either near (within hand reaching) or far (beyond hand reaching) space which suggests that these two spatial areas are coded differently by the brain. This exploratory study investigated, whether any difference in performance between these spatial domains might be task-independent or modulated by the requirement for a motor response.Methods: A 31-year-old right brain damaged patient (MF) and a group of age matched healthy controls were assessed with two serial visual search tasks and a Landmark paradigm. Both types of task required either a directional (pointing) or non-directional (button press) motor response. Participants were assessed with both task types and response modes in near (57 cm) and far space (114 cm).Results: MF showed left neglect during visual search only in far space for the perceptual condition and in near space for the motor condition. MF showed no neglect in both versions of the Landmark task irrespective of spatial distance. A voxel-based morphometric assessment of MF's brain lesion showed marked damage in the right ventro-temporal cortex, superior temporal gyrus, insula, inferior frontal gyrus, angular gyrus and bilaterally in the posterior cingulate cortex.Conclusions: Our preliminary findings suggest that processing of far space during visual search is associated with ventral stream damage but only when space is coded through visual information. Neglect involving directional motor activity in near space seems to be associated with damage of structures sharing close connections with the dorsal stream.

Visuomotor performance based on peripheral vision is impaired in the visual form agnostic patient DF

The perception–action model states that visual information is processed in different cortical areas depending on the purpose for which the information is acquired. Specifically, it was suggested that the ventral stream mediates visual perception, whereas the dorsal stream primarily processes visual information for the guidance of actions ( Goodale & Milner, 1992). Evidence for the model comes from patient studies showing that patients with ventral stream damage (visual form agnosia) and patients with dorsal stream damage (optic ataxia) show divergent performance in action and perception tasks. Whereas DF, a patient suffering from visual form agnosia, was found to perform well in visuomotor tasks despite her inability to use vision for perceptual tasks, patients with optic ataxia show usually the opposite pattern, i.e. good perception but impaired visuomotor control. The finding that both disorders seem to provoke a mirror-reversed pattern of spared and impaired visual functions, led to the belief that optic ataxia and visual form agnosia can be considered as complementary disorders. However, the visuomotor performance of patients with optic ataxia is typically only impaired when they are tested in visual periphery while being often preserved when tested in central vision. Here, we show that DF's visuomotor performance is also only preserved when the target is presented centrally. Her reaching and grasping movements to targets in peripheral vision are abnormal. Our findings indicate that DF's visuomotor performance is quite similar to the visuomotor performance of patients with optic ataxia which undermines previous suggestions that the two disorders form a double-dissociation.

Testing the dorsal stream attention hypothesis: Electrophysiological correlates and the effects of ventral stream damage

The roles of dorsal and ventral processing streams in visual orienting and conscious perception were examined in two experiments. The first employed high density EEG with source localization. The second comprised a neuropsychological case study. Visual orienting was assessed with an attention procedure, where peripheral letters cued participants towards a target location. In the perception procedure participants responded to the same letters by performing an explicit conscious discrimination. In Experiment 1, the peripheral letters elicited rapid dorsal stream activation in the attention procedure, and this activation preceded top-down enhancement of target processing in occipital cortex. In the perception procedure early ventral stream activation was seen. In addition, peripheral letters elicited an “early directing attention negativity” (EDAN) over parietal recording sites in the attention procedure, but not in the perception procedure. In Experiment 2, a patient with a bilateral ventral stream lesion but preserved dorsal stream function showed clear disruption to performance in the perception procedure, whilst exhibiting a normal visual orienting effect in the attention procedure. Taken together these findings (1) highlight the distinct roles of the dorsal and ventral streams in attention and perception, and (2) suggest how these streams might interact, via reentrant effects of attention on perceptual processing.

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

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

Intact automatic avoidance of obstacles in patients with visual form agnosia

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

Gradients of detection in neglect: comparison of peripersonal and extrapersonal space

Previous studies of target-cancellation performance in visuospatial neglect patients have reported lateral (left–right) and radial (near–far) gradients of attentional ability. The purpose of the present study was to replicate the reported attentional gradients in peripersonal space (within arms reach) and to examine whether lateral gradients of detection also appear in extrapersonal space (beyond arms reach), using equivalent tasks with no manual requirement. The relationship between radial gradients in peripersonal space and neglect severity (degree of lateral gradient) in extrapersonal space was also of interest. Right-hemisphere stroke subjects, with and without neglect, and healthy control subjects named visual targets on scanning sheets placed in peripersonal and extrapersonal space. The neglect group showed lateral gradients of increasing target detection from left to right in both peripersonal and extrapersonal space, which were not evident in the performance of either of the control groups. Double dissociations of neglect severity in peripersonal and extrapersonal space were also found in analyses of individual performance. Lesion analyses showed that peripersonal neglect was related to dorsal stream damage and extrapersonal neglect was related to ventral stream damage. Group analyses showed no significant radial gradients in peripersonal space in the three groups. In addition, while analyses of some individuals found significant near–far and far-near radial gradients, there was no correlation between radial gradients in peripersonal space and neglect severity in extrapersonal space. These results are discussed in terms of theorised hemispheric mechanisms of spatial attention and the relationship of neglect in the two co-ordinate spaces to the extent and location of damaged neurons in the right hemisphere.