Dorsal Visual Processing Stream Research Articles

Dorsal visual stream and LIMK1: hemideletion, haplotype, and enduring effects in children with Williams syndrome

BackgroundWilliams syndrome (WS), a rare neurodevelopmental disorder caused by hemizygous deletion of ~ 25 genes from chromosomal band 7q11.23, affords an exceptional opportunity to study associations between a well-delineated genetic abnormality and a well-characterized neurobehavioral profile. Clinically, WS is typified by increased social drive (often termed “hypersociability”) and severe visuospatial construction deficits. Previous studies have linked visuospatial problems in WS with alterations in the dorsal visual processing stream. We investigated the impacts of hemideletion and haplotype variation of LIMK1, a gene hemideleted in WS and linked to neuronal maturation and migration, on the structure and function of the dorsal stream, specifically the intraparietal sulcus (IPS), a region known to be altered in adults with WS.MethodsWe tested for IPS structural and functional changes using longitudinal MRI in a developing cohort of children with WS (76 visits from 33 participants, compared to 280 visits from 94 typically developing age- and sex-matched participants) over the age range of 5–22. We also performed MRI studies of 12 individuals with rare, shorter hemideletions at 7q11.23, all of which included LIMK1. Finally, we tested for effects of LIMK1 variation on IPS structure and imputed LIMK1 expression in two independent cohorts of healthy individuals from the general population.ResultsIPS structural (p < 10−4 FDR corrected) and functional (p < .05 FDR corrected) anomalies previously reported in adults were confirmed in children with WS, and, consistent with an enduring genetic mechanism, were stable from early childhood into adulthood. In the short hemideletion cohort, IPS deficits similar to those in WS were found, although effect sizes were smaller than those found in WS for both structural and functional findings. Finally, in each of the two general population cohorts stratified by LIMK1 haplotype, IPS gray matter volume (pdiscovery < 0.05 SVC, preplication = 0.0015) and imputed LIMK1 expression (pdiscovery = 10−15, preplication = 10−23) varied according to LIMK1 haplotype.ConclusionsThis work offers insight into neurobiological and genetic mechanisms responsible for the WS phenotype and also more generally provides a striking example of the mechanisms by which genetic variation, acting by means of molecular effects on a neural intermediary, can influence human cognition and, in some cases, lead to neurocognitive disorders.

The dorsal stream of visual processing and action-specific domains in parietal and frontal cortex in primates.

This review summarizes our findings obtained from over 15 years of research on parietal-frontal networks involved in the dorsal stream of cortical processing. We have presented considerable evidence for the existence of similar, partially independent, parietal-frontal networks involved in specific motor actions in a number of primates. These networks are formed by connections between action-specific domains representing the same complex movement evoked by electrical microstimulation. Functionally matched domains in the posterior parietal (PPC) and frontal (M1-PMC) motor regions are hierarchically related. M1 seems to be a critical link in these networks, since the outputs of M1 are essential to the evoked behavior, whereas PPC and PMC mediate complex movements mostly via their connections with M1. Thus, lesioning or deactivating M1 domains selectively blocks matching PMC and PPC domains, while having limited impact on other domains. When pairs of domains are stimulated together, domains within the same parietal-frontal network (matching domains) are cooperative in evoking movements, while they are mainly competitive with other domains (mismatched domains) within the same set of cortical areas. We propose that the interaction of different functional domains in each cortical region (as well as in striatum) occurs mainly via mutual suppression. Thus, the domains at each level are in competition with each other for mediating one of several possible behavioral outcomes.

Sequence learning recodes cortical representations instead of strengthening initial ones.

We contrast two computational models of sequence learning. The associative learner posits that learning proceeds by strengthening existing association weights. Alternatively, recoding posits that learning creates new and more efficient representations of the learned sequences. Importantly, both models propose that humans act as optimal learners but capture different statistics of the stimuli in their internal model. Furthermore, these models make dissociable predictions as to how learning changes the neural representation of sequences. We tested these predictions by using fMRI to extract neural activity patterns from the dorsal visual processing stream during a sequence recall task. We observed that only the recoding account can explain the similarity of neural activity patterns, suggesting that participants recode the learned sequences using chunks. We show that associative learning can theoretically store only very limited number of overlapping sequences, such as common in ecological working memory tasks, and hence an efficient learner should recode initial sequence representations.

Neural Activation in the Dorsal Visual Processing Stream is Context-Dependent in Williams Syndrome

Williams syndrome (WS), a rare neurodevelopmental disorder caused by a hemideletion of approximately 25 genes on chromosome 7q11.23, is behaviorally characterized by increased social drive and deficits in visuospatial construction. We previously reported that individuals with WS exhibit hypoactivation in the dorsal visual processing stream (DS) during visuospatial tasks; in contrast, we have also noted that these same DS areas are hyperactivated during processing of abstract social scenes. Here, we formally tested the hypothesis that DS activation is context-dependent by modeling a group-by-task interaction for children with WS and typically developing children (TDs) who completed both visuospatial and social tasks during fMRI.

Overt and Covert Object Features Mediate Timing of Patterned Brain Activity during Motor Planning.

Humans are seamless in their ability to efficiently and reliably generate fingertip forces to gracefully interact with objects. Such interactions rarely end in awkward outcomes like spilling, crushing, or tilting given advanced motor planning. Here we combine multiband imaging with deconvolution- and Bayesian pattern component modeling of functional magnetic resonance imaging data and in-scanner kinematics, revealing compelling evidence that the human brain differentially represents preparatory information for skillful object interactions depending on the saliency of visual cues. Earlier patterned activity was particularly evident in ventral visual processing stream-, but also selectively in dorsal visual processing stream and cerebellum in conditions of heightened uncertainty when an object’s superficial shape was incompatible rather than compatible with a key underlying object feature.

An fMRI study of age-associated changes in basic visual discrimination.

Clinical neuropsychology lacks tests of basic visuoperceptual and spatial skills that have well-controlled administration and sophisticated measurement methods. Items from the Visual Assessment Battery (VAB), a simultaneous match-to-sample task, assessed visual discrimination in 40 healthy adults aged 51-91 during fMRI. The tasks were designed to isolate discrimination of either location, shape, or velocity, and they each had three levels of difficulty. The Location task uniquely activated the dorsal visual processing stream, the Shape task the ventral stream, and the Velocity task an area encompassing V5. Greater age was associated with greater neural recruitment, particularly in frontal areas. Behaviorally, greater age was associated with prolonged response times, but not reduced accuracy. Increased difficulty was associated with slower responses and reduced accuracy, regardless of age. Results validated the specialization of brain regions for spatial, perceptual, and movement discriminations and the use of the VAB to assess functioning localized to these regions. Visual discrimination ability does not change dramatically with age, but like many cognitive processes, performance slows. Anterior neural recruitment during visual discrimination increases with age.

Williams syndrome hemideletion and LIMK1 variation both affect dorsal stream functional connectivity.

Williams syndrome is a rare genetic disorder caused by hemizygous deletion of ∼1.6 Mb affecting 26 genes on chromosome 7 (7q11.23) and is clinically typified by two cognitive/behavioural hallmarks: marked visuospatial deficits relative to verbal and non-verbal reasoning abilities and hypersocial personality. Clear knowledge of the circumscribed set of genes that are affected in Williams syndrome, along with the well-characterized neurobehavioural phenotype, offers the potential to elucidate neurogenetic principles that may apply in genetically and clinically more complex settings. The intraparietal sulcus, in the dorsal visual processing stream, has been shown to be structurally and functionally altered in Williams syndrome, providing a target for investigating resting-state functional connectivity and effects of specific genes hemideleted in Williams syndrome. Here, we tested for effects of the LIMK1 gene, deleted in Williams syndrome and important for neuronal maturation and migration, on intraparietal sulcus functional connectivity. We first defined a target brain phenotype by comparing intraparietal sulcus resting functional connectivity in individuals with Williams syndrome, in whom LIMK1 is hemideleted, with typically developing children. Then in two separate cohorts from the general population, we asked whether intraparietal sulcus functional connectivity patterns similar to those found in Williams syndrome were associated with sequence variation of the LIMK1 gene. Four independent between-group comparisons of resting-state functional MRI data (total n = 510) were performed: (i) 20 children with Williams syndrome compared to 20 age- and sex-matched typically developing children; (ii) a discovery cohort of 99 healthy adults stratified by LIMK1 haplotype; (iii) a replication cohort of 32 healthy adults also stratified by LIMK1 haplotype; and (iv) 339 healthy adolescent children stratified by LIMK1 haplotype. For between-group analyses, differences in intraparietal sulcus resting-state functional connectivity were calculated comparing children with Williams syndrome to matched typically developing children and comparing LIMK1 haplotype groups in each of the three general population cohorts separately. Consistent with the visuospatial construction impairment and hypersocial personality that typify Williams syndrome, the Williams syndrome cohort exhibited opposite patterns of intraparietal sulcus functional connectivity with visual processing regions and social processing regions: decreased circuit function in the former and increased circuit function in the latter. All three general population groups also showed LIMK1 haplotype-related differences in intraparietal sulcus functional connectivity localized to the fusiform gyrus, a visual processing region also identified in the Williams syndrome-typically developing comparison. These results suggest a neurogenetic mechanism, in part involving LIMK1, that may bias neural circuit function in both the general population and individuals with Williams syndrome.

Comparing population receptive fields in human and macaque visual cortex

The population receptive field (pRF) modelling approach has been applied widely in human fMRI to inform the organization of both early and late stages of the cortical visual hierarchy. Recently, a pRF implementation was developed that allows for oriented and elliptical pRFs and demonstrated that dorsal and ventral divisions of early visual cortex (EVC) differentially sample visual space. Thus, differences between the larger dorsal and ventral visual processing streams may be set early on in the visual hierarchy. However, despite its common use, we do not yet understand how pRFs relate to the receptive fields of single neurons. Therefore, cross-species validation by means of comparative fMRI would go a long way to bridging the gap between single-unit recordings in monkeys and fMRI in humans. Here, we compare pRFs from dorsal and ventral divisions of EVC in both humans (n=12) and macaques (Macaca mulatta; n=2). Participants (both humans and macaques) fixated centrally while a bar aperture traversed gradually across the visual field revealing brief scene fragments. Data from both study populations were analyzed in AFNI using both standard (circular) and elliptical pRF models. Cross-validation analyses revealed that, similar to the human, the elliptical pRF model captured more variance in the time-course of macaque data than a circular pRF implementation. Further, pRF eccentricity was positively correlated with both pRF aspect ratio and pRF area, with the strength of correlation increasing generally as a function of position in the visual hierarchy. Also consistent with our human data, the average pRF angles of dorsal and ventral divisions of EVC are oriented differentially. Finally, we found that on average pRF size estimates in macaques tended to be larger than in humans, despite the overall similarity. Overall, these results reveal a very similar pattern of pRF properties between macaque and human visual cortex

C-19 An fMRI Study of Age-Associated Changes in Basic Visual Discrimination

Abstract Objective The study was conducted to determine age-associated changes in functional brain response, measured with fMRI, during visual discrimination with regard to three elementary components of visual perception: shape, location, and velocity. A secondary aim was to validate the method used to isolate the hypothesized brain regions associated with these perceptual functions. Method Items from the Visual Assessment Battery (VAB), a simultaneous match-to-sample task, assessed visual discrimination in 40 healthy adults during fMRI. Participants were aged 51-91 and recruited from a larger community sample for a study on normal aging. The tasks were designed to isolate neural recruitment during discrimination of either location, shape, or velocity by using tasks that were identical aside from the perceptual skill required to complete them. Results The Location task uniquely activated the dorsal visual processing stream, the Shape task the ventral stream, and the Velocity task V5/MT. Greater age was associated with greater neural recruitment, particularly in frontal areas (uncorrected voxel-level p &lt; .001, family-wise error cluster-level p□.05). Conclusions Results validated the specialization of brain regions for spatial, perceptual, and movement discriminations and the use of the VAB to assess functioning localized to these regions. Anterior neural recruitment during visual discrimination increases with age.

Global motion perception is associated with motor function in 2-year-old children

The dorsal visual processing stream that includes V1, motion sensitive area V5 and the posterior parietal lobe, supports visually guided motor function. Two recent studies have reported associations between global motion perception, a behavioural measure of processing in V5, and motor function in pre-school and school aged children. This indicates a relationship between visual and motor development and also supports the use of global motion perception to assess overall dorsal stream function in studies of human neurodevelopment. We investigated whether associations between vision and motor function were present at 2 years of age, a substantially earlier stage of development. The Bayley III test of Infant and Toddler Development and measures of vision including visual acuity (Cardiff Acuity Cards), stereopsis (Lang stereotest) and global motion perception were attempted in 404 2-year-old children (±4 weeks). Global motion perception (quantified as a motion coherence threshold) was assessed by observing optokinetic nystagmus in response to random dot kinematograms of varying coherence. Linear regression revealed that global motion perception was modestly, but statistically significantly associated with Bayley III composite motor (r2=0.06, P<0.001, n=375) and gross motor scores (r2=0.06, p<0.001, n=375). The associations remained significant when language score was included in the regression model. In addition, when language score was included in the model, stereopsis was significantly associated with composite motor and fine motor scores, but unaided visual acuity was not statistically significantly associated with any of the motor scores. These results demonstrate that global motion perception and binocular vision are associated with motor function at an early stage of development. Global motion perception can be used as a partial measure of dorsal stream function from early childhood.

Optic ataxia and the dorsal visual steam re-visited: Impairment in bimanual haptic matching performed without vision

The ‘two visual systems’ account proposed by Milner and Goodale (1992) argued that visual perception and the visual control of action depend upon functionally distinct and anatomically separable brain systems: a ventral stream of visual processing that mediates visual perception (object identification and recognition) and a dorsal stream of visual processing mediating visually guided action. Compelling evidence for this proposal was provided by the neuropsychological studies of brain injured patients, in particular the contrasting pattern of impaired and preserved visual processing abilities of the visual object agnostic patient [DF] and optic ataxic patients who it was argued presented with impaired dorsal stream function. Optic ataxia [OA] has thus become a cornerstone of this ‘two visual system’ account (Pisella et al., 2009). In the current study we re-examine this assumption by investigating how several individuals presenting with OA performed on a bimanual haptic matching task performed without vision, when the bar to be matched was presented haptically or visually. We demonstrate that, unlike neurologically healthy controls who perform the task with high levels of accuracy, all of the optic ataxic patients were unable to perform the task. We interpret this finding as further evidence that the key difficulty experienced by optic ataxic patients across a range of behavioural tasks may be an inability to simultaneously and directly compare two spatial representations so as to compute the difference between them.

An effect of multisensory training on visual processing (Commentary on Grasso etal. (2016)).

An effect of multisensory training on visual processing (Commentary on Grasso etal. (2016)).

Signal Propagation in the Human Visual Pathways: An Effective Connectivity Analysis.

Although the visual system has been extensively investigated, an integrated account of the spatiotemporal dynamics of long-range signal propagation along the human visual pathways is not completely known or validated. In this work, we used dynamic causal modeling approach to provide insights into the underlying neural circuit dynamics of pattern reversal visual-evoked potentials extracted from concurrent EEG-fMRI data. A recurrent forward-backward connectivity model, consisting of multiple interacting brain regions identified by EEG source localization aided by fMRI spatial priors, best accounted for the data dynamics. Sources were first identified in the thalamic area, primary visual cortex, as well as higher cortical areas along the ventral and dorsal visual processing streams. Consistent with hierarchical early visual processing, the model disclosed and quantified the neural temporal dynamics across the identified activity sources. This signal propagation is dominated by a feedforward process, but we also found weaker effective feedback connectivity. Using effective connectivity analysis, the optimal dynamic causal modeling revealed enhanced connectivity along the dorsal pathway but slightly suppressed connectivity along the ventral pathway. A bias was also found in favor of the right hemisphere consistent with functional attentional asymmetry. This study validates, for the first time, the long-range signal propagation timing in the human visual pathways. A similar modeling approach can potentially be used to understand other cognitive processes and dysfunctions in signal propagation in neurological and neuropsychiatric disorders. Significance statement: An integrated account of long-range visual signal propagation in the human brain is currently incomplete. Using computational neural modeling on our acquired concurrent EEG-fMRI data under a visual evoked task, we found not only a substantial forward propagation toward "higher-order" brain regions but also a weaker backward propagation. Asymmetry in our model's long-range connectivity accounted for the various observed activity biases. Importantly, the model disclosed the timing of signal propagation across these connectivity pathways and validates, for the first time, long-range signal propagation in the human visual system. A similar modeling approach could be used to identify neural pathways for other cognitive processes and their dysfunctions in brain disorders.

Saccade planning evokes topographically specific activity in the dorsal and ventral streams.

Saccade planning may invoke spatially-specific feedback signals that bias early visual activity in favor of top-down goals. We tested this hypothesis by measuring cortical activity at the early stages of the dorsal and ventral visual processing streams. Human subjects maintained saccade plans to (prosaccade) or away (antisaccade) from a spatial location over long memory-delays. Results show that cortical activity persists in early visual cortex at the retinotopic location of upcoming saccade goals. Topographically specific activity persists as early as V1, and activity increases along both dorsal (V3A/B, IPS0) and ventral (hV4, VO1) visual areas. Importantly, activity persists when saccade goals are available only via working memory and when visual targets and saccade goals are spatially disassociated. We conclude that top-down signals elicit retinotopically specific activity in visual cortex both in the dorsal and ventral streams. Such activity may underlie mechanisms that prioritize locations of task-relevant objects.

Resolving the organization of the third tier visual cortex in primates: a hypothesis-based approach.

As highlighted by several contributions to this special issue, there is still ongoing debate about the number, exact location, and boundaries of the visual areas located in cortex immediately rostral to the second visual area (V2), i.e., the "third tier" visual cortex, in primates. In this review, we provide a historical overview of the main ideas that have led to four models of third tier cortex organization, which are at the center of today's debate. We formulate specific predictions of these models, and compare these predictions with experimental evidence obtained primarily in New World primates. From this analysis, we conclude that only one of these models (the "multiple-areas" model) can accommodate the breadth of available experimental evidence. According to this model, most of the third tier cortex in New World primates is occupied by two distinct areas, both representing the full contralateral visual quadrant: the dorsomedial area (DM), restricted to the dorsal half of the third visual complex, and the ventrolateral posterior area (VLP), occupying its ventral half and a substantial fraction of its dorsal half. DM belongs to the dorsal stream of visual processing, and overlaps with macaque parietooccipital (PO) area (or V6), whereas VLP belongs to the ventral stream and overlaps considerably with area V3 proposed by others. In contrast, there is substantial evidence that is inconsistent with the concept of a single elongated area V3 lining much of V2. We also review the experimental evidence from macaque monkey and humans, and propose that, once the data are interpreted within an evolutionary-developmental context, these species share a homologous (but not necessarily identical) organization of the third tier cortex as that observed in New World monkeys. Finally, we identify outstanding issues, and propose experiments to resolve them, highlighting in particular the need for more extensive, hypothesis-driven investigations in macaque and humans.

Controversies about the visual areas located at the anterior border of area V2 in primates.

Anatomical and electrophysiological studies have provided us with detailed information regarding the extent and topography of the primary (V1) and secondary (V2) visual areas in primates. The consensus about the V1 and V2 maps, however, is in sharp contrast with controversies regarding the organization of the cortical areas lying immediately rostral to V2. In this review, we address the contentious issue of the extent of the third visual area (V3). Specifically, we will argue for the existence of both ventral (V3v) and dorsal (V3d) segments of V3, which are located, respectively, adjacent to the anterior border of ventral and dorsal V2. V3v and V3d would together constitute a single functional area with a complete representation of both upper and lower visual hemifields. Another contentious issue is the organization of the parietal-occipital (PO) area, which also borders the rostral edge of the medial portion of dorsal V2. Different from V1, V2, and V3, which exhibit a topography based on the defined lines of isoeccentricity and isopolar representation, area PO only has a systematic representation of polar angles, with an emphasis on the peripheral visual field (isoeccentricity lines are not well defined). Based on the connectivity patterns of area PO with distinct cytochrome oxidase modules in V2, we propose a subdivision of the dorsal stream of visual information processing into lateral and medial domains. In this model, area PO constitutes the first processing instance of the dorsal-medial stream, coding for the full-field flow of visual cues during navigation. Finally, we compare our findings with those in other species of Old and New World monkeys and argue that larger animals, such as macaque and capuchin monkeys, have similar organizations of the areas rostral to V2, which is different from that in smaller New World monkeys.

The neural representation of faces and bodies in motion and at rest

The neural organization of person processing relies on brain regions functionally selective for faces or bodies, with a subset of these regions preferring moving stimuli. Although the response properties of the individual areas are well established, less is known about the neural response to a whole person in a natural environment. Targeting an area of cortex that spans multiple functionally-selective face and body regions, we examined the relationship among neural activity patterns elicited in response to faces, bodies, and people in static and moving displays. When both stimuli were static or moving, pattern classification analyses indicated highly discriminable responses to faces, bodies, and whole people. Neural discrimination transferred in both directions between representations created from moving or static stimuli. It transferred also to stimuli experienced across static and dynamic presentations (one static and the other dynamic). In both transfer cases, however, discrimination accuracy decreased relative to the case where the representations were both created and tested with static or moving forms. Next, we examined the relative contribution of activity pattern and response magnitude to discrimination by comparing classifiers that operated with magnitude-normalized scans with classifiers that retained pattern and magnitude information. When both stimuli were moving or static, response magnitude contributed to classification, but the spatially distributed activity pattern accounted for most of the discrimination. Across static and moving presentations, activity pattern accounted completely for the discriminability of neural responses to faces, bodies, and people, with no contribution from response magnitude. Combined, the results indicate redundant and flexible access to person-based shape codes from moving and static presentations. The transfer of shape information across presentation types that preferentially access dorsal and ventral visual processing streams indicates that a common shape code may ground functional divisions in the processing of face and body information.

Grasping with the eyes: The role of elongation in visual recognition of manipulable objects

Processing within the dorsal visual stream subserves object-directed action, whereas visual object recognition is mediated by the ventral visual stream. Recent findings suggest that the computations performed by the dorsal stream can nevertheless influence object recognition. Little is known, however, about the type of dorsal stream information that is available to assist in object recognition. Here, we present a series of experiments that explored different psychophysical manipulations known to bias the processing of a stimulus toward the dorsal visual stream in order to isolate its contribution to object recognition. We show that elongated-shaped stimuli, regardless of their semantic category and familiarity, when processed by the dorsal stream, elicit visuomotor grasp-related information that affects how we categorize manipulable objects. Elongated stimuli may reduce ambiguity during grasp preparation by providing a coarse cue to hand shaping and orientation that is sufficient to support action planning. We propose that this dorsal-stream-based analysis of elongation along a principal axis is the basis for how the dorsal visual object processing stream can affect categorization of manipulable objects.

Neural correlates of the impact of control on decision making in pathological gambling

Perceived control over a gambling outcome leads individuals to accept more and larger bets, increased risk-taking. Pathological gamblers, however, do not diminish risk-taking when control is absent, suggesting an illusion of control. To evaluate neural correlates of perceived control in gamblers, this study compared magnetoencephalography responses of 36 pathological (PG) and 36 non-pathological gamblers (NPG) during the Georgia Gambling Task.PGs exhibited greater activity in bilateral primary sensory regions. An interaction between pathology and control over the gambling task was observed bilaterally throughout dorsal and ventral visual processing streams, and lateral PFC. NPGs showed decreased activity when control was absent. Groups did not differ in response to potential bet cost. These findings provide neurophysiological evidence that PGs suffer from the pattern of risk-taking associated with perceived control, even when no control exists. They suggest that gambling pathology contributes to differential processing of gambling stimuli other than potential costs or rewards.

FMRI evidence for dorsal stream processing abnormality in adults born preterm

We investigated the consequences of premature birth on the functional neuroanatomy of the dorsal stream of visual processing. fMRI was recorded while sixteen healthy participants, 8 (two men) adults (19years 6months old, SD 10months) born premature (mean gestational age 30weeks), referred to as Premas, and 8 (two men) matched controls (20years 1month old, SD13months), performed a 1-back memory task of Object or Grip information using a hand grasping a drinking vessel as stimulus. While history of prematurity did not significantly affect task performance, Group by Task analysis of variance in regions of interest spanning the occipital, temporal and parietal lobes revealed main effects of Task and interactions between the two factors. Object processing activated the left inferior occipital cortex and bilateral ventral temporal regions, belonging to the ventral stream, with no effect of Group. Grip processing across groups activated the early visual cortex and the left supramarginal gyrus belonging to the dorsal stream. Group effect on the brain activity during Grip suggested that Controls represented the actions’ goal while Premas relied more on low-level visual information. This shift from higher- to lower-order visual processing between Controls and Premas may reflect a more general trend, in which Premas inadequately recruit higher-order visual functions for dorsal stream task performance, and rely more on lower-level functions.