Two action systems in the human brain

In order to investigate the functional specificity of the dorsal and ventral visual processing steams we used transcranial magnetic stimulation (TMS) to briefly disrupt one or the other while subjects performed three tasks, involving discrimination of colour or shape or relative position. TMS was delivered over right posterior parietal cortex (PPC) or right lateral occipital (LO) cortex, regions known to have visuo-spatial and object processing properties respectively. LO but not PPC stimulation had a significant effect on reaction time when subjects were asked to make a discrimination of relative shape. PPC stimulation had a significant effect when subjects were asked to discriminate relative position of the same shapes. Stimulation of LO also lengthened reaction times on the position task. There were no effects of stimulation at either site on colour discrimination. Results are discussed within the framework of how the dorsal stream and ventral stream are dissociated following their damage in neurological patients and possible ways in which they may interact in the normal brain.

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.

The visual guidance of goal-directed movements requires transformations of incoming visual information that are different from those required for visual perception. For us to grasp an object successfully, our brain must use just-in-time computations of the object’s real-world size and shape, and its orientation and disposition with respect to our hand. These requirements have led to the emergence of dedicated visuomotor modules in the posterior parietal cortex of the human brain (the dorsal visual stream) that are functionally distinct from networks in the occipito-temporal cortex (the ventral visual stream) that mediate our conscious perception of the world. Although the identification and selection of goal objects and an appropriate course of action depends on the perceptual machinery of the ventral stream and associated cognitive modules, the execution of the subsequent goal-directed action is mediated by dedicated online control systems in the dorsal stream and associated motor areas. The dorsal stream allows an observer to reach out and grasp objects with exquisite ease, but by itself, deals only with objects that are visible at the moment the action is being programmed. The ventral stream, however, allows an observer to escape the present and bring to bear information from the past – including information about the function of objects, their intrinsic properties, and their location with reference to other objects in the world. Ultimately then, both streams contribute to the production of goal-directed actions. The principles underlying this division of labour between the dorsal and ventral streams are relevant to the design and implementation of autonomous robotic systems.

Action video games foster competitive environments that demand rapid spatial navigation and decision-making. Action video gamers often exhibit faster response times and slightly improved accuracy in vision-based sensorimotor tasks. Background/Objectives: However, the underlying functional and structural changes in the two visual streams of the brain that may be contributing to these cognitive improvements have been unclear. Methods: Using functional and diffusion MRI data, this study investigated the differences in connectivity between gamers who play action video games and nongamers in the dorsal and ventral visual streams. Results: We found that action video gamers have enhanced functional and structural connectivity, especially in the dorsal visual stream. Specifically, there is heightened functional connectivity—both undirected and directed—between the left superior occipital gyrus and the left superior parietal lobule during a moving-dot discrimination decision-making task. This increased connectivity correlates with response time in gamers. The structural connectivity in the dorsal stream, as quantified by diffusion fractional anisotropy and quantitative anisotropy measures of the axonal fiber pathways, was also enhanced for gamers compared to nongamers. Conclusions: These findings provide valuable insights into how action video gaming can induce targeted improvements in structural and functional connectivity between specific brain regions in the visual processing pathways. These connectivity changes in the dorsal visual stream underpin the superior performance of action video gamers compared to nongamers in tasks requiring rapid and accurate vision-based decision-making.

BackgroundThe brain network supporting visual-scene memory includes ventral (what) and dorsal (where, how) visual processing streams, and hubs within the medial temporal cortex, plus frontal, temporal, and parietal regions comprising the core-recollection memory system. However, the exact relationship between these regions and the capacity to memorize different types of visual-scene elements remains debated. Functional neuroimaging studies point to dissociable as well as common network components supporting perception and memory of different aspects of visual information. In the current neuropsychological study, we assess impact of stroke lesion topography on recall of identity, location, and action of event participants, as assessed by the WMS-III Family Pictures subtest.MethodsNinety-three first-event stroke patients (54 and 39 right- and left-hemisphere damaged, respectively; RHD, LHD) in the sub-acute phase performed the Family Pictures task. Voxel-based lesion-symptom mapping (VLSM) analysis identified brain lesions implicated in memory deficits for the composite score and separately for each scene element: characters' identity, the action they performed, and location of occurrence.ResultsBehavioral analysis revealed significant impairment in identity, location, and action memory among right hemisphere damage (RHD) patients compared to matched healthy controls. Performance was significantly lower in delayed compared to immediate testing condition, and memory domains showed a hierarchy of scores: highest for identity, intermediate for location, and lowest for action. VLSM revealed a markedly different pattern of lesion effects in the two hemispheres. In the RH, network was dominated by large voxel clusters in middle and superior temporal and inferior parietal regions. In contradistinction, the LH network was dominated by large voxel clusters in temporo-occipital and medial temporal lobe (MTL) regions. VLSM conjunction analysis disclosed further distinctions between anatomical regions subserving memory of character identity, action, and location.DiscussionVisual scene memory is supported by a bi-hemispheric network dominated in the LH by temporo-occipital/MTL structures and in the RH by temporo-parietal components of the core recollection network. The LH network regions were mostly implicated in a non-specific manner, whereas in the RH network more regions were implicated in memory for specific scene elements.

Dissociation and convergence of the dorsal and ventral visual working memory streams in the human prefrontal cortex

The distinction between know how and knowledge that is one that has failed to draw much attention in philosophy, despite its importance in other fields. This distinction is explored and neuropsychological studies are presented that support this distinction. In particular, the dorsal and ventral visual processing streams are examined and shown to process information individually despite lesions to the other processing stream. Studies are also presented that further highlight the idea that the distinction between know how and knowledge that take place in decision-making and in judgements of how to act. These studies also contradict Carr's assessment that a necessary aspect of connecting know how with ability is conscious intent. The idea of a more general functional connection between know how and ability is explored and it is emphasized that this functional connection should include very basic neurobiological functions.

Sensory cortical areas send long-range projections to cortical areas from other sensory modalities, supporting multisensory integration to generate a unified representation of the external world. However, the organizational principles underlying these extensive cross-modal connections remain poorly understood. In this study, we investigated the anatomical and functional organisation of auditory cortex inputs in the visual cortex. We found that populations of anatomically segregated auditory cortex neurons project to different visual cortical areas, broadcasting distinct auditory information to the dorsal and ventral visual processing streams. While sound frequency information was homogenously distributed across visual cortical areas, sound location information was differentially broadcast across the visual cortex. Specifically, sound azimuth and elevation were differentially encoded across visual cortical areas and streams matching the retinotopic bias of the target area. These findings suggest that cross-modal cortico-cortical connections follow a simple rule whereby specialised projection pathways are topographically aligned with the organisational principles of the target sensory area, ensuring spatially coherent integration of multisensory signals.

Reading the prevailing emotion of groups of people ("crowd emotion") is critical to understanding their overall intention and disposition. It alerts us to potential dangers, such as angry mobs or panicked crowds, giving us time to escape. A critical aspect of processing crowd emotion is that it must occur rapidly, because delays often are costly. Although knowing the timing of neural events is crucial for understanding how the brain guides behaviors using coherent signals from a glimpse of multiple faces, this information is currently lacking in the literature on face ensemble coding. Therefore, we used magnetoencephalography to examine the neurodynamics in the dorsal and ventral visual streams and the periamygdaloid cortex to compare perception of groups of faces versus individual faces. Forty-six participants compared two groups of four faces or two individual faces with varying emotional expressions and chose which group or individual they would avoid. We found that the dorsal stream was activated as early as 68 msec after the onset of stimuli containing groups of faces. In contrast, the ventral stream was activated later and predominantly for individual face stimuli. The latencies of the dorsal stream activation peaks correlated with participants' response times for facial crowds. We also found enhanced connectivity earlier between the periamygdaloid cortex and the dorsal stream regions for crowd emotion perception. Our findings suggest that ensemble coding of facial crowds proceeds rapidly and in parallel by engaging the dorsal stream to mediate adaptive social behaviors, via a distinct route from single face perception.

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.

To what extent are shifts of attention driven by encoding of visual-spatial landmarks, associated with useful locations, or by encoding of environmental cues that act as symbolic representations, providing information about where to look next? In Experiment 1 we found that when cues were presented with a long exposure time (300 ms) attention shifts were driven by the symbolic identity of cue stimuli, independently of their visual-spatial (landmark) features; but when cues were exposed very briefly, (66 ms), attention shifts were independent of symbolic information, and were driven instead by visual landmark features. This unexpected finding was interpreted in terms of the transient and sustained response characteristics of the M-cell and P-cell inputs to the dorsal and ventral visual streams, respectively, and informed our theoretical proposal that attentional effects elicited by visual-spatial landmarks may be driven by dorsal stream ("where pathway") encoding; while attentional effects driven by the symbolic identity of cues may be driven by ventral stream ("what pathway") encoding. Detailed predictions derived from this proposal, and based on distinct physiological properties of the 2 visual streams were tested and confirmed in Experiments 2-6. Our results suggest that a 2-process view of attention shifting can be integrated with dual-stream models of vision. According to this unified theory: (a) Landmarks associated with visually useful locations elicit rapid, nonconscious shifts of attention, via nonsemantic, dorsal visual stream encoding of their features and spatial relationships; (b) Slower, endogenous shifts of attention are elicited by ventral visual stream encoding of symbolic-semantic information. (PsycINFO Database Record

Our understanding of the neural underpinnings of perception is largely built upon studies employing 2-dimensional (2D) planar images. Here we used slow event-related functional imaging in humans to examine whether neural populations show a characteristic repetition-related change in haemodynamic response for real-world 3-dimensional (3D) objects, an effect commonly observed using 2D images. As expected, trials involving 2D pictures of objects produced robust repetition effects within classic object-selective cortical regions along the ventral and dorsal visual processing streams. Surprisingly, however, repetition effects were weak, if not absent on trials involving the 3D objects. These results suggest that the neural mechanisms involved in processing real objects may therefore be distinct from those that arise when we encounter a 2D representation of the same items. These preliminary results suggest the need for further research with ecologically valid stimuli in other imaging designs to broaden our understanding of the neural mechanisms underlying human vision.

Recent behavioral and neuroimaging studies using continuous flash suppression (CFS) have suggested that action-related processing in the dorsal visual stream might be independent of perceptual awareness, in line with the "vision-for-perception" versus "vision-for-action" distinction of the influential dual-stream theory. It remains controversial if evidence suggesting exclusive dorsal stream processing of tool stimuli under CFS can be explained by their elongated shape alone or by action-relevant category representations in dorsal visual cortex. To approach this question, we investigated category- and shape-selective functional magnetic resonance imaging-blood-oxygen level-dependent responses in both visual streams using images of faces and tools. Multivariate pattern analysis showed enhanced decoding of elongated relative to non-elongated tools, both in the ventral and dorsal visual stream. The second aim of our study was to investigate whether the depth of interocular suppression might differentially affect processing in dorsal and ventral areas. However, parametric modulation of suppression depth by varying the CFS mask contrast did not yield any evidence for differential modulation of category-selective activity. Together, our data provide evidence for shape-selective processing under CFS in both dorsal and ventral stream areas and, therefore, do not support the notion that dorsal "vision-for-action" processing is exclusively preserved under interocular suppression.

Visuospatial processing impairments are prevalent in individuals with cerebral visual impairment (CVI) and are typically ascribed to "dorsal stream dysfunction" (DSD). However, the contribution of other cortical regions, including early visual cortex (EVC), frontal cortex, or the ventral visual stream, to such impairments remains unknown. Thus, here, we examined fMRI activity in these regions, while individuals with CVI (and neurotypicals) performed a visual search task within a dynamic naturalistic scene. First, behavioral performance was measured with eye tracking. Participants were instructed to search and follow a walking human target. CVI participants took significantly longer to find the target, and their eye gaze patterns were less accurate and less precise. Second, we used the same task in the MRI scanner. Along the dorsal stream, activation was reduced in CVI participants, consistent with the proposed DSD in CVI. Intriguingly, however, visual areas along the ventral stream showed the complete opposite pattern, with greater activation in CVI participants. In contrast, we found no differences in either EVC or frontal cortex between groups. These results suggest that the impaired visuospatial processing abilities in CVI are associated with differential recruitment of the dorsal and ventral visual streams, likely resulting from impaired selective attention.

Assessment of brain-damaged subjects presenting with dissociated repetition deficits after selective injury to either the left dorsal or ventral auditory pathways can provide further insight on their respective roles in verbal repetition. We evaluated repetition performance and its neural correlates using multimodal imaging (anatomical MRI, DTI, fMRI, and18FDG-PET) in a female patient with transcortical motor aphasia (TCMA) and in a male patient with conduction aphasia (CA) who had small contiguous but non-overlapping left perisylvian infarctions. Repetition in the TCMA patient was fully preserved except for a mild impairment in nonwords and digits, whereas the CA patient had impaired repetition of nonwords, digits and word triplet lists. Sentence repetition was impaired, but he repeated novel sentences significantly better than clichés. The TCMA patient had tissue damage and reduced metabolism in the left sensorimotor cortex and insula. DTI showed damage to the left temporo-frontal and parieto-frontal segments of the arcuate fasciculus (AF) and part of the left ventral stream together with well-developed right dorsal and ventral streams, as has been reported in more than one-third of females. The CA patient had tissue damage and reduced metabolic activity in the left temporoparietal cortex with additional metabolic decrements in the left frontal lobe. DTI showed damage to the left temporo-parietal and temporo-frontal segments of the AF, but the ventral stream was spared. The direct segment of the AF in the right hemisphere was also absent with only vestigial remains of the other dorsal subcomponents present, as is often found in males. fMRI during word and nonword repetition revealed bilateral perisylvian activation in the TCMA patient suggesting recruitment of spared segments of the left dorsal stream and right dorsal stream with propagation of signals to temporal lobe structures suggesting a compensatory reallocation of resources via the ventral streams. The CA patient showed a greater activation of these cortical areas than the TCMA patient, but these changes did not result in normal performance. Repetition of word triplet lists activated bilateral perisylvian cortices in both patients, but activation in the CA patient with very poor performance was restricted to small frontal and posterior temporal foci bilaterally. These findings suggest that dissociated repetition deficits in our cases are probably reliant on flexible interactions between left dorsal stream (spared segments, short tracts remains) and left ventral stream and on gender-dimorphic architecture of the right dorsal stream.