Action-specific feature processing in the human visual cortex

Abstract

Sensorimotor integration involves feedforward and reentrant processing of sensory input. Grasp-related motor activity precedes and is thought to influence visual object processing. Yet, while the importance of reentrant feedback is well established in perception, the top-down modulations for action and the neural circuits involved in this process have received less attention. Do action-specific intentions influence the processing of visual information in the human cortex? Using a cue-separation fMRI paradigm, we found that action-specific instruction (manual alignment vs. grasp) influences the cortical processing of object orientation several seconds after the object had been viewed. This influence occurred as early as in the primary visual cortex and extended to ventral and dorsal visual stream areas.Importantly, this modulation was unrelated to non-specific action planning. Further, the primary visual cortex showed stronger functional connectivity with frontal-parietal areas and the inferior temporal cortex during the delay following orientation processing for align than grasping movements, strengthening the idea of reentrant feedback from dorsal visual stream areas involved in action. To our knowledge, this is the first demonstration that intended manual actions have such an early, pervasive, and differential influence on the cortical processing of vision.

Visual working memory and action: Functional links and bi-directional influences

“…This work has also made clear that memory retention may often not be restricted to visual representations or motor intentions alone (Colby & Goldberg, 1999 ; Gilad et al, 2018 ; Snyder et al, 1997 ), but instead involve joint visual and motor retention (with the possibility for mutual interaction). This is reinforced by recent studies that have revealed recruitment of visual brain areas for guiding precise manual action, even in the absence of visual input (Fiehler et al, 2011 ; Monaco et al, 2018 ; Singhal et al, 2013 ).…”

“…Recent fMRI studies have begun to link working memory of visual-shape information to memory-guided manual actions after multi-second delays. Through this work, it has become clear that planning and executing precise manual actions recruit early visual brain areas (Gallivan et al, 2019 ; Gutteling et al, 2015 ), even in the absence of current visual stimulation (Fiehler et al, 2011 ; Monaco et al, 2018 ; Singhal et al, 2013 ). This is in line with a call to detailed visual representations from working memory, in which these “sensory” brain areas have been argued to participate (Harrison & Tong, 2009 ; Pasternak & Greenlee, 2005 ; Sreenivasan et al, 2014 ; van Ede, 2018 ).…”

Output planning at the input stage in visual working memory

“…One fundamental purpose for holding detailed sensory information in working memory is to guide action (15,(19)(20)(21)(22)(23)(24)(25). In accordance, recent work has shown that when memorized visual information is probed for guiding behavior, action plans can be selected from memory concurrently with probed visual representations (26).…”

Sense of external agency is sustained by multisensory functional integration in the somatosensory cortex

“…whereas action-specific plans influence visual feature processing F I G U R E 2 Nodes of cortical regions related to the curve pick values of subjects' performance in the Agency Attribution Task. 3D dorsal (left panel) and ventral (right panel) views of nodes resulted as significantly related to consistency in self-agency attribution for: (a) Degree Centrality, (Gutteling, Park, Kenemans, & Neggers, 2013;Monaco, Chen, Menghi, & Douglas Crawford, 2018). The fact that this area showed the highest number of connections with other cortical nodes when measures of consistency in the action-effect integration are considered, indicates that the state of preparedness and functional connectivity of this sensory region is crucial when competing internal and external cues have to be integrated as to derive a sense of control over external events.…”

“…Moreover, the secondary visual cortex, parallelly processing motion, objects location and shape, is in the mainstream of the visual information flow related to visual‐motor integration. Indeed, the latter implies an intensive cross‐talk between cortical areas, since vision is used to plan movements in a feed‐forward fashion (Gallivan & Culham, 2015), whereas action‐specific plans influence visual feature processing (Gutteling, Park, Kenemans, & Neggers, 2013; Monaco, Chen, Menghi, & Douglas Crawford, 2018). The fact that this area showed the highest number of connections with other cortical nodes when measures of consistency in the action‐effect integration are considered, indicates that the state of preparedness and functional connectivity of this sensory region is crucial when competing internal and external cues have to be integrated as to derive a sense of control over external events.…”