Dorsal Stream Research Articles

Dorsal stream receptive field development entails growing visual field coverage

Dorsal stream receptive field development entails growing visual field coverage

Species and individual differences and connectional asymmetry of Broca's area in humans and macaques

To reveal the connectional specialization of the Broca's area (or its homologue), voxel-wise inter-species and individual differences, and inter-hemispheric asymmetry were respectively inspected in humans and macaques at both whole-brain connectivity and single tract levels. It was discovered that the developed connectivity blueprint approach is able to localize connectionally comparable voxels between the two species in Broca's area, whereas the quantitative differences between blueprints of locationally or connectionally corresponding voxels enable us to generate inter-hemispheric, inter-subject, and inter-species connectional variabilities, respectively. More importantly, the inter-species and inter-subject variabilities exhibited positive correlation in both two primates, and relatively higher variabilities were detected in the anatomically defined pars triangularis. By contrast, negative relationship was identified between the inter-species variability and hemispheric asymmetry in human brain. In particular, relatively higher asymmetry was revealed in the anatomically defined pars opercularis. Therefore, our novel findings demonstrated that pars triangularis, as compared to pars opercularis, might be a more active area during primate evolution, in which the brain connectivity and possible functions of pars triangularis show relatively higher degree in species specialization, yet lower in hemispheric specialization. Meanwhile, brain connectivity and possible functions of pars opercularis manifested an opposite pattern. At the tract level, functional roles related to the ventral stream in speech comprehension were relatively conservative and bilaterally organized, while those related to the dorsal stream in speech production show relatively higher species and hemispheric specializations.

Neural bases of elements of syntax during speech production in patients with aphasia

The ability to string together words into a structured arrangement capable of conveying nuanced information is key to speech production. The assessment of the neural bases for structuring sentences has been challenged by the need of experts to delineate the aberrant morphosyntactic structures in aphasic speech. Most studies have relied on focused tasks with limited ecological validity. We characterized syntactic complexity during connected speech produced by patients with chronic post-stroke aphasia. We automated this process by employing Natural Language Processing (NLP). We conducted voxel-based and connectome-based lesion-symptom mapping to identify brain regions crucially associated with sentence production and syntactic complexity. Posterior-inferior aspects of left frontal and parietal lobes, as well as white matter tracts connecting these areas, were essential for syntactic complexity, particularly the posterior inferior frontal gyrus. These findings suggest that sentence structuring during word production depends on the integrity of Broca’s area and the dorsal stream of language processing.

Isolating the white matter circuitry of the dorsal language stream: Connectome-Symptom Mapping in stroke induced aphasia.

The application of ℓ1‐regularized machine learning models to high‐dimensional connectomes offers a promising methodology to assess clinical‐anatomical correlations in humans. Here, we integrate the connectome‐based lesion‐symptom mapping framework with sparse partial least squares regression (sPLS‐R) to isolate elements of the connectome associated with speech repetition deficits. By mapping over 2,500 connections of the structural connectome in a cohort of 71 stroke‐induced cases of aphasia presenting with varying left‐hemisphere lesions and repetition impairment, sPLS‐R was trained on 50 subjects to algorithmically identify connectomic features on the basis of their predictive value. The highest ranking features were subsequently used to generate a parsimonious predictive model for speech repetition whose predictions were evaluated on a held‐out set of 21 subjects. A set of 10 short‐ and long‐range parieto‐temporal connections were identified, collectively delineating the broader circuitry of the dorsal white matter network of the language system. The strongest contributing feature was a short‐range connection in the supramarginal gyrus, approximating the cortical localization of area Spt, with parallel long‐range pathways interconnecting posterior nodes in supramarginal and superior temporal cortex with anterior nodes in both ventral and—notably—in dorsal premotor cortex, respectively. The collective disruption of these pathways indexed repetition performance in the held‐out set of participants, suggesting that these impairments might be characterized as a parietotemporal disconnection syndrome impacting cortical area Spt and its associated white matter circuits of the frontal lobe as opposed to being purely a disconnection of the arcuate fasciculus.

Visual Cortical Area MT Is Required for Development of the Dorsal Stream and Associated Visuomotor Behaviors.

The middle temporal (MT) area of the extrastriate visual cortex has long been studied in adulthood for its distinctive physiological properties and function as a part of the dorsal stream, yet interestingly it possesses a similar maturation profile as the primary visual cortex (V1). Here, we examined whether an early-life lesion in MT of marmoset monkeys (six female, two male) altered the dorsal stream development and the behavioral precision of reaching-to-grasp sequences. We observed permanent changes in the anatomy of cortices associated with both reaching (parietal and medial intraparietal areas) and grasping (anterior intraparietal area), as well as in reaching-and-grasping behaviors. In addition, we observed a significant impact on the anatomy of V1 and the direction sensitivity of V1 neurons in the lesion projection zone. These findings indicate that area MT is a crucial node in the development of primate vision, affecting both V1 and areas in the dorsal visual pathway known to mediate visually guided manual behaviors.SIGNIFICANCE STATEMENT Previous studies have identified a role for the MT area of the visual cortex in perceiving motion, yet none have examined its central role in the development of the visual cortex and in the establishment of visuomotor behaviors. To address this, we used a unilateral MT lesion model in neonatal marmosets before examining the anatomic, physiological, and behavioral consequences. In adulthood, we observed perturbations in goal-orientated reach-and-grasp behavior, altered direction selectivity of V1 neurons, and changes in the cytoarchitecture throughout dorsal stream areas. This study highlights the importance of MT as a central node in visual system development and consequential visuomotor activity.

Mapping Regional Homogeneity and Functional Connectivity of the Visual Cortex in Resting-State fMRI

A combined regional homogeneity (ReHo) and functional connectivity (FC) method, a type of noninvasive functional magnetic resonance imaging (fMRI) method, has been used to evaluate synchronous neuronal activity changes in retinitis pigmentosa (RP). The purpose of this study is to describe our method for analysis of intra- and interregional synchronizations of changes in neuronal activity in RP patients. The advantages of the combined ReHo and FC method are that it is both noninvasive and sufficiently sensitive to investigate changes in cerebral synchronous neuronal activity changes in vivo. Here, 16 RP patients and 14 healthy controls closely matched in age, sex, and education underwent resting-state fMRI scans. Two sample t-tests were conducted to compare ReHo and FC across groups. Our results showed that visual network disconnection and reorganization of the retino-thalamocortical pathway and dorsal visual stream occurred in the RP patients. Here, we describe the details of this method, its use, and the impact of its key parameters in a step-by-step manner.

Landmark cueing and exogenous (onset) cueing: How are they related?

Attentional consequences of (i) mere onset of a peripheral visual cue, and (ii)encoding spatially predictive, landmark features of that cue were studied in two experiments. Target location was associated with landmark features of peripheral cues. Cue onset elicited both attention capture (Experiment Two) and inhibition of return (Experiment One) effects. In both experiments, attentional effects of landmark features of the cues were observed early in practice, and diminished with time on task. Contrary to hypotheses based on models that liken attention to a moving spotlight or zoom lens, in both experiments attentional effects of landmark features were confined to the location where the cue was presented. To explain this, we enlist the concept of attentional priority maps, and propose that visual encoding causes attentional priorities to be updated via alternative input routes and mechanisms. We suggest that onset cueing effects are associated with retinotectal ‘spatial indexing’, which registers the location, but not the attributes of new stimuli, while landmark cueing effects are associated with interaction between spatial indexing and dorsal stream visual processing of attentionally relevant landmark features.

Unveiling functions of the visual cortex using task-specific deep neural networks.

The human visual cortex enables visual perception through a cascade of hierarchical computations in cortical regions with distinct functionalities. Here, we introduce an AI-driven approach to discover the functional mapping of the visual cortex. We related human brain responses to scene images measured with functional MRI (fMRI) systematically to a diverse set of deep neural networks (DNNs) optimized to perform different scene perception tasks. We found a structured mapping between DNN tasks and brain regions along the ventral and dorsal visual streams. Low-level visual tasks mapped onto early brain regions, 3-dimensional scene perception tasks mapped onto the dorsal stream, and semantic tasks mapped onto the ventral stream. This mapping was of high fidelity, with more than 60% of the explainable variance in nine key regions being explained. Together, our results provide a novel functional mapping of the human visual cortex and demonstrate the power of the computational approach.

Engagement of Language and Domain General Networks during Word Monitoring in a Native and Unknown Language.

Functional neuroimaging studies have highlighted the roles of three networks in processing language, all of which are typically left-lateralized: a ventral stream involved in semantics, a dorsal stream involved in phonology and speech production, and a more dorsal “multiple demand” network involved in many effortful tasks. As lateralization in all networks may be affected by life factors such as age, literacy, education, and brain pathology, we sought to develop a task paradigm with which to investigate the engagement of these networks, including manipulations to selectively emphasize semantic and phonological processing within a single task performable by almost anyone regardless of literacy status. In young healthy participants, we administered an auditory word monitoring task, in which participants had to note the occurrence of a target word within a continuous story presented in either their native language, Portuguese, or the unknown language, Japanese. Native language task performance activated ventral stream language networks, left lateralized but bilateral in the anterior temporal lobe. Unfamiliar language performance, being more difficult, activated left hemisphere dorsal stream structures and the multiple demand network bilaterally, but predominantly in the right hemisphere. These findings suggest that increased demands on phonological processing to accomplish word monitoring in the absence of semantic support may result in the bilateral recruitment of networks involved in speech perception under more challenging conditions.

The neural basis of Tetris gameplay: implicating the role of visuospatial processing

Tetris is not only a widely used entertaining computer game, but has been used as a component in emerging psychological interventions targeting dysfunctional mental imagery, e.g., intrusive memories and imagery-based cravings. However, little is known about the neurobiological mechanisms underlying these interventions. Tetris gameplay has been hypothesized to disrupt dysfunctional mental imagery (e.g., imagery-based intrusive memories of adverse events) and cravings (e.g., substance use) by taxing visuospatial working memory. In line with this, the present study aimed to characterize brain areas involved in the visuospatial aspects of Tetris gameplay, by controlling for motor activity (button presses) and using gameplay instructions emphasizing mental rotation. Participants (N = 28) received mental rotation instructions and thereafter either played Tetris, or only pressed buttons as if playing Tetris (motor activity), while undergoing functional magnetic resonance imaging. Tetris gameplay (when using mental rotation instructions and controlling for motor activity) robustly activated brain areas located in the ventral and dorsal stream, with maximum peak activation in the inferior and mid temporal gyrus. To the best of our knowledge, this is the first study to characterize brain areas specifically associated with the visuospatial aspects of Tetris gameplay, by controlling for motor activity and when using mental rotation instructions. Results demonstrate that engaging in Tetris gameplay recruits an extensive brain circuitry previously tied to visuospatial processing. Thus, findings are consistent with the use of Tetris as an imagery-competing task as one of several components of emerging interventions targeting dysfunctional mental imagery.

Dedifferentiation of Functional Brain Activation Associated With Greater Visual Discrimination Accuracy in Middle-Aged and Older Adults.

Neural dedifferentiation refers to an age-related phenomenon whereby brain functions that are localized to specific, distinct, and differentiated brain areas in young adults become less so as people reach more advanced age. Older adults tend to exhibit greater spread of cortical activation on fMRI during cognitive processing compared to younger adults, with evidence that this occurs during visuoperceptual processing. Some age-related functional changes are considered compensatory, but whether dedifferentiation is compensatory is not clearly understood. The current study assessed dedifferentiation and visual discrimination performance during simultaneous match-to-sample tasks from the Visual Assessment Battery (VAB) among 40 healthy middle-aged and older adults using fMRI. Task-relevant regions of interest (ROIs) were created in the dorsal stream for discrimination of spatial location, the ventral stream for shape, and an area encompassing V5 for velocity. Dedifferentiation, or less specificity in functional activation, was associated with greater discrimination accuracy and more years of education. Secondary analyses showed that reduced functional activation in task-relevant ROIs was associated with faster discrimination speed. Age was unassociated with functional activation. Results suggest that dedifferentiation is compensatory. Lack of age effects suggest that other factors beyond age, such as cognitive or brain reserve, may better predict performance when considering cognitive skills that are relatively stable as adults age, such as visual discrimination.

Neural encoding and functional interactions underlying pantomimed movements

Pantomimes are a unique movement category which can convey complex information about our intentions in the absence of any interaction with real objects. Indeed, we can pretend to use the same tool to perform different actions or to achieve the same goal adopting different tools. Nevertheless, how our brain implements pantomimed movements is still poorly understood. In our study, we explored the neural encoding and functional interactions underlying pantomimes adopting multivariate pattern analysis (MVPA) and connectivity analysis of fMRI data. Participants performed pantomimed movements, either grasp-to-move or grasp-to-use, as if they were interacting with two different tools (scissors or axe). These tools share the possibility to achieve the same goal. We adopted MVPA to investigate two levels of representation during the planning and execution of pantomimes: (1) distinguishing different actions performed with the same tool, (2) representing the same final goal irrespective of the adopted tool. We described widespread encoding of action information within regions of the so-called “tool” network. Several nodes of the network—comprising regions within the ventral and the dorsal stream—also represented goal information. The spatial distribution of goal information changed from planning—comprising posterior regions (i.e. parietal and temporal)—to execution—including also anterior regions (i.e. premotor cortex). Moreover, connectivity analysis provided evidence for task-specific bidirectional coupling between the ventral stream and parieto-frontal motor networks. Overall, we showed that pantomimes were characterized by specific patterns of action and goal encoding and by task-dependent cortical interactions.

Resting-state functional brain connectivity is related to subsequent procedural learning skills in school-aged children

This magnetoencephalography (MEG) study investigates how procedural sequence learning performance is related to prior brain resting-state functional connectivity (rsFC), and to what extent sequence learning induces rapid changes in brain rsFC in school-aged children.Procedural learning was assessed in 30 typically developing children (mean age ± SD: 9.99 years ± 1.35) using a serial reaction time task (SRTT). During SRTT, participants touched as quickly and accurately as possible a stimulus sequentially or randomly appearing in one of the quadrants of a touchscreen. Band-limited power envelope correlation (brain rsFC) was applied to MEG data acquired at rest pre- and post-learning. Correlation analyses were performed between brain rsFC and sequence-specific learning or response time indices.Stronger pre-learning interhemispheric rsFC between inferior parietal and primary somatosensory/motor areas correlated with better subsequent sequence learning performance and faster visuomotor response time. Faster response time was associated with post-learning decreased rsFC within the dorsal extra-striate visual stream and increased rsFC between temporo-cerebellar regions.In school-aged children, variations in functional brain architecture at rest within the sensorimotor network account for interindividual differences in sequence learning and visuomotor performance. After learning, rapid adjustments in functional brain architecture are associated with visuomotor performance but not sequence learning skills.

Impaired Set-Shifting from Dorsal Stream Disconnection: Insights from a European Series of Right Parietal Lower-Grade Glioma Resection.

Simple SummaryAwake surgery with cognitive monitoring has increasingly been implemented to preserve brain networks and functionality. More recently, not only surgery in the left but also in the right hemisphere, i.c., the parietal lobe, was associated with potential risk for deficits in cognitive functions, such as cognitive flexibility. We describe an explorative pilot study in an international consortium within clinical care as usual. Careful interpretation of our findings indicates that disconnection of the lateral part of the dorsal stream correlated with impaired set-shifting. More importantly, it illustrates the need for international collaboration on neuropsychological tests and methodologies to improve our understanding of white matter networks at risk during awake surgery.Awake surgery with cognitive monitoring has increasingly been implemented to preserve brain networks and functionality. More recently, not only surgery in the left but also in the right hemisphere, i.c., the parietal lobe, was associated with potential risk for deficits in cognitive functions, such as cognitive flexibility. In this explorative pilot study, we compare cognitive performance more than three months after surgery with baseline measurements and explore the association between cognitive decline and subcortical tracts that may have been severed during surgery in the right hemisphere. Twenty-two patients who underwent surgery for a right parietal low-grade glioma were assessed pre- and postoperatively using the Trail Making Test and the Stroop task to administer set-shifting abilities and inhibition. Volume measurements and lesion–symptom mapping analyses were performed on postoperative MRI scans. Careful interpretation of the results shows a change in TMT performance and not on the Stroop Task when the lateral part of the arcuate fasciculus is damaged, indicating that disconnection of the lateral part of the dorsal stream might be correlated specifically with impaired set-shifting and not with inhibition. More importantly, this study underlines the need for international concertation to allow larger studies to increase power and perform more detailed analyses.

Virtually spatialized sounds enhance auditory processing in healthy participants and patients with a disorder of consciousness

Neuroscientific and clinical studies on auditory perception often use headphones to limit sound interference. In these conditions, sounds are perceived as internalized because they lack the sound-attributes that normally occur with a sound produced from a point in space around the listener. Without the spatial attention mechanisms that occur with localized sounds, auditory functional assessments could thus be underestimated. We hypothesize that adding virtually externalization and localization cues to sounds through headphones enhance sound discrimination in both healthy participants and patients with a disorder of consciousness (DOC). Hd-EEG was analyzed in 14 healthy participants and 18 patients while they listened to self-relevant and irrelevant stimuli in two forms: diotic (classic sound presentation with an “internalized” feeling) and convolved with a binaural room impulse response (to create an “externalized” feeling). Convolution enhanced the brains’ discriminative response as well as the processing of irrelevant sounds itself, in both healthy participants and DOC patients. For the healthy participants, these effects could be associated with enhanced activation of both the dorsal (where/how) and ventral (what) auditory streams, suggesting that spatial attributes support speech discrimination. Thus, virtually spatialized sounds might “call attention to the outside world” and improve the sensitivity of assessment of brain function in DOC patients.

Card posting does not rely on visual orientation: A challenge to past neuropsychological dissociations

A common set of tasks frequently employed in the neuropsychological assessment of patients with visuomotor or perceptual deficits are the card-posting and the perceptual orientation matching tasks. In the posting task, patients have to post a card (or their hand) through a slot of varying orientations while the matching task requires them to indicate the slot's orientation as accurately as possible. Observations that damage to different areas of the brain (dorsal vs. ventral stream) is associated with selective impairment in one of the tasks - but not the other - has led to the suggestion that different cortical pathways process visual orientation information for perception versus action. In three experiments, we show that this conclusion may be premature as posting does not seem to rely on the processing of visual orientation information but is instead performed using obstacle avoidance strategies that require an accurate judgement of egocentric distances between the card's and the slot's edges. Specifically, we found that while matching is susceptible to the oblique effect (i.e., common perceptual orientation bias with higher accuracy for cardinal than oblique orientations), this was not the case for posting, neither in immediate nor in memory-guided conditions. In contrast to matching, posting errors primarily depended on biomechanical demands and reflected a preference for performing efficient and comfortable movements. Thus, we suggest that previous dissociations between perceptual and visuomotor performance in letter posting tasks are better explained by impairments in egocentric and allocentric spatial processing than by independent visual processing systems.

Structural connectivity differs between males and females in the brain object manipulation network.

Object control skills are one of the most important abilities in daily life. Knowledge of object manipulation is an essential factor in improving object control skills. Although males and females equally try to use object manipulation knowledge, their object control abilities often differ. To explain this difference, we investigated how structural brain networks in males and females are differentially organized in the tool-preferring areas of the object manipulation network. The structural connectivity between the primary motor and premotor regions and between the inferior parietal regions in males was significantly higher than that in females. However, females showed greater structural connectivity in various regions of the object manipulation network, including the paracentral lobule, inferior parietal regions, superior parietal cortices, MT+ complex and neighboring visual areas, and dorsal stream visual cortex. The global node strength found in the female parietal network was significantly higher than that in males but not for the entire object manipulation, ventral temporal, and motor networks. These findings indicated that the parietal network in females has greater inter-regional structural connectivity to retrieve manipulation knowledge than that in males. This study suggests that differential structural networks in males and females might influence object manipulation knowledge retrieval.

Presence of the Endocannabinoid System in the Inferior Pulvinar of the Vervet Monkey.

The expression of the endocannabinoid (eCB) system, including cannabinoid receptor type 1 (CB1R) and the cannabinoid synthesizing (NAPE-PLD) and degrading (FAAH) enzymes, has been well-characterized in the retina of rodents and monkeys. More recently, the presence of CB1R was localized throughout the dorsal lateral geniculate nucleus of the thalamus of vervet monkeys. Given that the retina projects also to the pulvinar either via a direct projection or via the superior colliculus, it was reasonable to assume that this system would be present therein. The visual pulvinar, namely the inferior pulvinar (PI) region, was delineated with calbindin immunohistochemical staining. Using Western blots and immunofluorescence, we demonstrated that CB1R, NAPE-PLD and FAAH are expressed in the PI of the vervet monkey. Throughout the PI, CB1R was mainly colocalized with VGLUT2-positive axon terminals in the vicinity of calbindin and parvalbumin-positive neurons. NAPE-PLD and FAAH rather colocalized with calbindin over the somatodendritic compartment of PI neurons. Our results suggest that visual information coming from the retina and entering the PI is modulated by the eCB system on its way to the dorsal visual stream. These results provide insights for understanding the role of eCBs in the modulation of visual thalamic inputs and, hence, visual perception.

Lesion loci of impaired affective prosody: A systematic review of evidence from stroke

Affective prosody, or the changes in rate, rhythm, pitch, and loudness that convey emotion, has long been implicated as a function of the right hemisphere (RH), yet there is a dearth of literature identifying the specific neural regions associated with its processing. The current systematic review aimed to evaluate the evidence on affective prosody localization in the RH. One hundred and ninety articles from 1970 to February 2020 investigating affective prosody comprehension and production in patients with focal brain damage were identified via database searches. Eleven articles met inclusion criteria, passed quality reviews, and were analyzed for affective prosody localization. Acute, subacute, and chronic lesions demonstrated similar profile characteristics. Localized right antero-superior (i.e., dorsal stream) regions contributed to affective prosody production impairments, whereas damage to more postero-lateral (i.e., ventral stream) regions resulted in affective prosody comprehension deficits. This review provides support that distinct RH regions are vital for affective prosody comprehension and production, aligning with literature reporting RH activation for affective prosody processing in healthy adults as well. The impact of study design on resulting interpretations is discussed.

Aligning one’s sights: The pulvinar provides context for visual information processing

The pulvinar (lateral posterior [LP]), like other higher-order thalamic nuclei, receives input from-and sends output to-multiple neocortical structures. In this issue of Neuron, Blot etal. (2021) demonstrate that LP integrates multimodal inputs to put visual information in context.