Cross-talk connections underlying dorsal and ventral stream integration during hand actions

Abstract

According to the dual-stream theory, the processing of visual information is divided into a ventral pathway mediating object recognition, and a dorsal pathway supporting visuomotor control. Increasing evidence suggests that these streams are not independent, but where this dorsal-ventral stream integration occurs remains unknown. We explored the candidate white matter pathways linking dorsal and ventral visual streams in 30 right-handed participants performing object-oriented hand movements of varying complexity (reaching, grasping and lifting), using advanced diffusion imaging tractography based on the spherical deconvolution and kinematical analysis. We provided for the first time a direct evidence of cross-communication between dorsal and ventral visual streams in humans, through vertical occipital fasciculus and temporo-parietal fibers of the arcuate fasciculus during on-line control of grasping and lifting actions. We showed that individual differences in the microstructure of these cross-talk connections were associated with the variability of the arm deceleration, the grip opening and the grasp accuracy. This study suggests that hand kinematics, in skilled hand actions where high degree of online control is required, is related to the anatomy of the cross-talk networks between dorsal and ventral streams, bringing important insights to the dual-stream theory and the sensorimotor organization of hand actions.

Altered functional connectivity of cortical networks in semantic variant Primary Progressive Aphasia

“…This evidence of between-network functional connectivity between the dorsal attention and visual association networks is consistent with evidence for structural connectivity linking the two networks (tract tracing work in non-human primates: Felleman & Van Essen, 1991;Ungerleider, Galkin, Desimone, & Gattass, 2008; Wernicke, 1881; diffusion weighted imaging in humans: Takemura et al, 2016;Yeatman et al, 2014). Connectivity between the FFA and SPL may be mediated by the vertical occipital fasciculus (VOF), which has projections to the posterior intraparietal sulcus of the dorsal attention network and the fusiform gyrus of the visual association network (Budisavljevic et al, 2018;Takemura et al, 2016;Yeatman et al, 2014). Supporting the functional evidence of dorsal attention and visual association network communication, the VOF has been implicated in reading (Greenblatt, 1973(Greenblatt, , 1976), depth perception (Oishi et al, 2018), and object related motor actions (Budisavljevic et al, 2018).…”

“…Connectivity between the FFA and SPL may be mediated by the vertical occipital fasciculus (VOF), which has projections to the posterior intraparietal sulcus of the dorsal attention network and the fusiform gyrus of the visual association network (Budisavljevic et al, 2018;Takemura et al, 2016;Yeatman et al, 2014). Supporting the functional evidence of dorsal attention and visual association network communication, the VOF has been implicated in reading (Greenblatt, 1973(Greenblatt, , 1976), depth perception (Oishi et al, 2018), and object related motor actions (Budisavljevic et al, 2018). Although the VOF connects regions of the visual association and dorsal attention networks, the white matter architecture that would support direct connectivity between the nodes of interest in this study (the SPL and FFA) is not understood.…”

Gesturing tool use and tool transport actions modulates inferior parietal functional connectivity with the dorsal and ventral object processing pathways

“…A number of fMRI studies have demonstrated there is a high degree of cross-talk between the dorsal and ventral visual pathways as a function of grasping or generating tool-directed gestures (e.g., see Budisavljevic, Dell'Acqua, & Castiello, 2018;Garcea et al, 2018;Hutchison & Gallivan, 2018) or when viewing objects or making judgments about object manipulation (e.g., Chen, Snow, Culham, & Goodale, 2018;Chen et al, 2017;Freud, Rosenthal, Ganel, & Avidan, 2015;Kleineberg et al, 2018;Sim, Helbig, Graf, & Kiefer, 2015; for discussion, see Orban & Caruana, 2014;van Polanen & Davare, 2015). Our results offer a novel interpretation of the role that the left SMG plays in tool-directed actions: Tool manipulation knowledge is not "represented" in the left SMG; rather the left SMG sits at the nexus of the dorso-dorsal and ventro-dorsal visual pathways, and serves as an intermediary or "hub" region aggregating (a) representations of object properties and conceptual knowledge in the ventral stream with (b) online sensory-motor information processed in the dorsal stream, (c) which is informed by top-down biasing signals from prefrontal cortex to resolve competition between candidate tool use actions.…”

Spatiotemporal coding in the macaque supplementary eye fields: landmark influence in the target-to-gaze transformation

“…13), by combining our current results with FEF recordings obtained in the same recording sessions (Bharmauria et al, 2020). We begin with the conventional assumption that egocentric and allocentric information are coded separately in the dorsal and ventral streams, respectively, with considerable crosstalk between them (Milner, 2017;Budisavljevic et al, 2018). But regardless of the source, our data show that the FEF and SEF are initially driven by low latency (~80ms) egocentric visual inputs (target-in-eye coordinates), whereas the landmark influence has a higher latency (~200-300ms), consistent with more complex visual processing pathway.…”