Rethinking category selectivity: insights from the macaque inferior temporal cortex

Integrative Benchmarking to Advance Neurally Mechanistic Models of Human Intelligence

Action-Related Properties Shape Object Representations in the Ventral Stream

FMRI of shared-stream priming of lexical identification by object semantics along the ventral visual processing stream

The primate visual system consists of a ventral stream, specialized for object recognition, and a dorsal visual stream, which is crucial for spatial vision and actions. However, little is known about the interactions and information flow between these two streams. We investigated these interactions within the network processing three-dimensional (3D) object information, comprising both the dorsal and ventral stream. Reversible inactivation of the macaque caudal intraparietal area (CIP) during functional magnetic resonance imaging (fMRI) reduced fMRI activations in posterior parietal cortex in the dorsal stream and, surprisingly, also in the inferotemporal cortex (ITC) in the ventral visual stream. Moreover, CIP inactivation caused a perceptual deficit in a depth-structure categorization task. CIP-microstimulation during fMRI further suggests that CIP projects via posterior parietal areas to the ITC in the ventral stream. To our knowledge, these results provide the first causal evidence for the flow of visual 3D information from the dorsal stream to the ventral stream, and identify CIP as a key area for depth-structure processing. Thus, combining reversible inactivation and electrical microstimulation during fMRI provides a detailed view of the functional interactions between the two visual processing streams.

A double dissociation between sensitivity to changes in object identity and object orientation in the ventral and dorsal visual streams: A human fMRI study

The co-involvement of the ventral and dorsal visual streams in spatial tasks investigated with dual-site TMS

Several studies have demonstrated that while perceptual judgements of object size can be biased by visual illusions, actions remain more closely scaled to true object properties. This dissociation is often cited in support of a two-stream model of visual processing, in which visual perception is thought to be mediated by a ventral stream, while goal-directed actions are controlled by a dorsal stream. Evidence suggests that pantomimed actions (i.e., actions directed toward remembered targets) are controlled differently to natural actions; indeed, it has been proposed that pantomimed actions are mediated by the ventral rather than the dorsal stream. To test this hypothesis, we examined the effect of a visual size illusion (a variation of the Müller-Lyer figure) on manual aperture formation during natural and pantomimed prehension (i.e., action) and aperture scaling (i.e., perception). As found in earlier studies, mean peak aperture (MPA) was significantly affected by the illusion in the perception task but not the natural action task. In the pantomime condition, action and perception were equally affected by the illusion as reflected by MPA. These results provide support for the hypothesis that pantomimed actions are mediated by the ventral visual processing stream, while natural actions depend on the dorsal stream.

Object and depth perception from motion cues involves the recruitment of visual dorsal stream brain areas. In 3-D structure-from-motion (SFM) perception, motion and depth information are first extracted in this visual stream to allow object categorization, which is in turn mediated by the ventral visual stream. Such interplay justifies the use of SFM paradigms to understand dorsal-ventral integration of visual information. The nature of such processing is particularly interesting to be investigated in a neurological model of cognitive dissociation between dorsal (impaired) and ventral stream (relatively preserved) processing, Williams syndrome (WS). In the current fMRI study, we assessed dorsal versus ventral stream processing by using a performance-matched 3-D SFM object categorization task. We found evidence for substantial reorganization of the dorsal stream in WS as assessed by whole-brain ANOVA random effects analysis, with subtle differences in ventral activation. Dorsal reorganization was expressed by larger medial recruitment in WS (cuneus, precuneus, and retrosplenial cortex) in contrast with controls, which showed the expected dorsolateral pattern (caudal intraparietal sulcus and lateral occipital cortex). In summary, we found a substantial reorganization of dorsal stream regions in WS in response to simple visual categories and 3-D SFM perception, with less affected ventral stream. Our results corroborate the existence of a medial dorsal pathway that provides the substrate for information rerouting and reorganization in the presence of lateral dorsal stream vulnerability. This interpretation is consistent with recent findings suggesting parallel routing of information in medial and lateral parts of dorsal stream.

Event Abstract Back to Event Dissociating the role of dorsal and ventral visual streams in object lifting and weight perception Vonne Van Polanen1*, Guy Rens1 and Marco Davare1 1 KU Leuven, Belgium When sequentially lifting a series of differently weighted objects, our fingertip forces are typically scaled according to the weight of the previously lifted object, an effect often referred to as sensorimotor memory [2]. For instance, force rates are higher after the lift of a heavy compared to a light object. Recently, we showed that this effect on force parameters also changes perceptual estimates, where objects are judged lighter after the lift of a heavy compared to a light weight [3]. Here, we aimed to investigate the causal role of the dorsal vs. ventral visual streams in these processes, given they are classically involved in computing motor vs. perceptual parameters, respectively. We used transcranial magnetic stimulation (TMS) to investigate the contribution of the left anterior intraparietal sulcus (aIPS) and lateral occipital (LO) areas, which are important nodes for processing hand-object interactions in the dorsal and ventral streams. Subjects received TMS to either aIPS or LO. Neuronavigation (Brainsight) was used to localize our TMS targets on individual structural brain imaging scans. The left aIPS was defined anatomically as the intersection between the intraparietal and postcentral sulci and LO was located using previously published functional coordinates [1]. Subjects were asked to grip and lift equally sized but differently weighted (light, 2N, or heavy, 6N) objects in a pseudo-randomized order and provide a weight estimate on a self-chosen scale. During object lifting, TMS was applied in a burst of 3 pulses (10Hz) at 120% of the active motor threshold. Three stimulation conditions were compared for each brain area, with stimulation at object contact (dynamic phase), 500 ms after object lift-off (static phase) or no stimulation. We quantified the effect of TMS on perceptual weight estimates, peak grip and load force rates, loading phase duration and mean grip force during stable hold. For each parameter, a mixed ANOVA was performed with TMS target (aIPS or LO) as between-subject factor and TMS condition (dynamic, static, or no stimulation) and object order (light-light, heavy-light, light-heavy, or heavy-heavy) as within-subject factors. When previously lifting a heavy object, peak grip and load force rates were higher and loading phase durations were shorter compared to previously lifting a light object, in line with classical sensorimotor memory effects. It is noteworthy that TMS did not alter this order effect. We only found a general effect of TMS when applied during the dynamic phase, with increased force rate peaks compared to the other TMS conditions. Furthermore, stable grip forces were higher after lifting a heavy object compared to a light one. Interestingly, this effect was cancelled in the aIPS group. No general effect of TMS condition on stable grip force was found. Finally, weight estimations were lower when a light object was preceded by a heavy object compared to a light one, replicating our earlier findings [3]. TMS led to overall lighter weight ratings, independently of the targeted area or timing. Remarkably, the order effect on weight estimations was cancelled when TMS was applied during the static phase over either aIPS or LO. These findings suggest that both aIPS and LO are involved in late phases of object weight perception. Moreover, the role of dorsal and ventral stream areas in mediating sensorimotor memory effects seems limited to aIPS for controlling grip forces in later phases of lifting. Overall, this sheds new light on the interactions between brain networks mediating action and perception during object manipulation.

Ventral and dorsal stream contributions to the online control of immediate and delayed grasping: A TMS approach

Adaptive behavior relies on the integration of perceptual and motor processes. In this study, we aimed at characterizing the cerebral processes underlying perceptuo-motor interactions evoked during prehension movements in healthy humans, as measured by means of functional magnetic resonance imaging. We manipulated the viewing conditions (binocular or monocular) during planning of a prehension movement, while parametrically varying the slant of the grasped object. This design manipulates the relative relevance and availability of different depth cues necessary for accurate planning of the prehension movement, biasing visual information processing toward either the dorsal visual stream (binocular vision) or the ventral visual stream (monocular vision). Two critical nodes of the dorsomedial visuomotor stream [V6A (anterior visual area 6) and PMd (dorsal premotor cortex)] increased their activity with increasing object slant, regardless of viewing conditions. In contrast, areas in both the dorsolateral visuomotor stream [anterior intraparietal area (AIP) and ventral premotor cortex (PMv)] and in the ventral visual stream [lateral-occipital tactile-visual area (LOtv)] showed differential slant-related responses, with activity increasing when monocular viewing conditions and increasing slant required the processing of pictorial depth cues. These conditions also increased the functional coupling of AIP with both LOtv and PMv. These findings support the view that the dorsomedial stream is automatically involved in processing visuospatial parameters for grasping, regardless of viewing conditions or object characteristics. In contrast, the dorsolateral stream appears to adapt motor behavior to the current conditions by integrating perceptual information processed in the ventral stream into the prehension plan.

Recent reports have documented greater plasticity in the dorsal visual stream as compared with the ventral visual stream. This study sought to test the hypothesis that this greater plasticity may be related to a more protracted period of development in the dorsal as compared with the ventral stream. Age-related effects on event-related potentials (ERPs) elicited by motion and color stimuli, designed to activate the two visual streams, were assessed in healthy individuals aged 6 years through adulthood. Although significant developmental effects were observed in amplitudes of ERPs to both color and motion stimuli, marked latency effects were observed only in response to motion. These results provide support for the hypothesis that the dorsal stream displays a longer developmental time course across the early school years than the ventral stream. Implications for neural and behavioral plasticity are discussed.

The Ebbinghaus illusion, in which a central circle surrounded by large circles appears to be smaller than a central circle surrounded by small circles, affects the speed of pointing movements. When the central circle appears to be big, pointing movements directed towards it are faster than when the central circle appears to be small. This effect could be due to an interaction between ventral stream processing associated with determining relative object size and dorsal stream processing associated with sensorimotor output. Alternatively, the dorsal stream alone could mediate the effect via the transformation of object shape representations into motor output within the parietal lobe. Finally, ventral stream processing could be integrated into motor output through projections to the prefrontal cortex and subsequently to the motor areas of the cortex, thus bypassing the dorsal stream. These three alternatives were tested by disrupting either the ventral or dorsal stream processing using transcranial magnetic stimulation (TMS) while subjects made pointing movements as quickly and accurately as possible to the central target circles within the Ebbinghaus illusion display. The relative changes in reaction time, movement speed, and movement accuracy for small versus large appearing target circles were compared when TMS was delivered over each site as well as at a control site (SMA). The results showed that TMS over either the dorsal or ventral stream but not the SMA reduced the influence of the illusion on the pointing movement speed but did not affect reaction time or movement accuracy. A second control experiment was completed in which TMS was delivered during pointing movements to target circles of physically different sizes that were not surrounded by either large or small circles. This allowed us to determined whether the effect we observed in the main experiment was due specifically to the relative size information contained within the illusory display and the effect this has on the preparation of pointing responses or to an influence on basic perceptual and sensorimotor processes occurring within the ventral and dorsal streams, respectively. The results showed that the affect on pointing movement speed was still present with dorsal but not ventral stream stimulation. Taken together, this evidence suggests that the ventral stream contributes to pointing movements based on relative object size information via its projections to the prefrontal areas and not necessarily through interactions with the dorsal stream.

We used positron emission tomography (PET) and functional magnetic resonance imaging (fMRI) in human subjects to investigate whether the ventral and dorsal visual stream cooperate when active judgements about color have to be made. Color was used as the attribute, because it is processed primarily in the ventral stream. The centrally positioned stimuli were equiluminant shades of brown. The successive color discrimination task was contrasted to a dimming detection task, in which retinal input was identical but with double the number of motor responses. The stimulus presentation rate was parametrically varied and a constant performance level was obtained for all conditions. The visual activation sites were identified by retinotopic mapping and cortical flattening. In addition, one psychophysical and two fMRI experiments were performed to control for differences in visuospatial attention and motor output. Successive color discrimination involved early visual areas, including V1 and VP and the ventral color-responsive region, as well as anterior and middle dorsal intraparietal sulcus, dorsal premotor cortex and pre-SMA. Cortical regions involved in dimming detection and motor output included area V3A, hMT/V5+, lateral occipital sulcus, posterior dorsal intraparietal sulcus, primary motor cortex and SMA. These experiments demonstrated that even with color as the attribute, successive discrimination, in which a decision process has to link visual signals to motor responses, involves both ventral and dorsal visual stream areas.

The degree of interaction between the ventral and dorsal visual streams has been discussed in multiple scientific domains for decades. Recently, several white matter tracts that directly connect cortical regions associated with the dorsal and ventral streams have become possible to study due to advancements in automated and reproducible methods. The developmental trajectory of this set of tracts, here referred to as the posterior vertical pathway (PVP), has yet to be described. We propose an input-driven model of white matter development and provide evidence for the model by focusing on the development of the PVP. We used reproducible, cloud-computing methods and diffusion imaging from adults and children (ages 5-8years) to compare PVP development to that of tracts within the ventral and dorsal pathways. PVP microstructure was more adult-like than dorsal stream microstructure, but less adult-like than ventral stream microstructure. Additionally, PVP microstructure was more similar to the microstructure of the ventral than the dorsal stream and was predicted by performance on a perceptual task in children. Overall, results suggest a potential role for the PVP in the development of the dorsal visual stream that may be related to its ability to facilitate interactions between ventral and dorsal streams during learning. Our results are consistent with the proposed model, suggesting that the microstructural development of major white matter pathways is related, at least in part, to the propagation of sensory information within the visual system.