Selectivity for Three-Dimensional Shape and Grasping-Related Activity in the Macaque Ventral Premotor Cortex

Abstract

Anatomical studies indicate that area F5 in the macaque ventral premotor cortex consists of three different sectors. One of these is F5a in the posterior bank of the inferior arcuate sulcus, but no functional characterization of F5a at the single-cell level exists. We investigated the neuronal selectivity for three-dimensional (3D) shape and grasping activity in F5a. In contrast to neighboring regions F5p and 45B, the great majority of F5a neurons showed selectivity for disparity-defined curved surfaces, and most neurons preserved this selectivity across positions in depth, indicating higher-order disparity selectivity. Thus, as predicted by monkey fMRI data, F5a neurons showed robust 3D-shape selectivity in the absence of a motor response. To investigate the relationship between disparity selectivity and grasping activity, we recorded from 3D-shape-selective F5a neurons during a visually guided grasping task and during grasping in the dark. F5a neurons encoding the depth profile of curved surfaces frequently responded during grasping of real-world objects in the light, but not in the dark, whereas nearby neurons were also active in the dark. The presence of 3D-shape-selective and "visual-dominant" neurons demonstrates that the F5a sector is distinct from neighboring regions of ventral premotor cortex, in line with recent anatomical connectivity studies.

Three-dimensional Shape Coding in Grasping Circuits: A Comparison between the Anterior Intraparietal Area and Ventral Premotor Area F5a

“…Consistent with the properties of individual ITC neurons (Janssen et al, 2000b), electrical microstimulation of ITC clusters during 3-D shape categorization exerts a profound and predictable influence on both perceptual choices and RTs (Verhoef, Vogels, & Janssen, 2012). In the F5a sector of ventral premotor cortex, in contrast, most 3-D shapeselective neurons were also active during visually guided grasping of real-world objects (Theys, Pani, et al, 2012), suggesting a close relationship between 3-D shape selectivity and visuomotor transformations for grasping. However, no data exist concerning the possible behavioral role of 3-D shape-selective sites in AIP.…”

“…We previously demonstrated that neurons in area AIP and area F5a, which is adjacent to F5p, provide a robust representation of 3-D shape (Theys, Pani, van Loon, Goffin, & Janssen, 2012;Srivastava, Orban, De Maziere, & Janssen, 2009). The presence of 3-D shape-selective neurons in F5a does not indicate how these neurons represent disparitydefined 3-D shapes, that is, which aspects of the stimuli are primarily encoded by the neurons.…”

Grasping Execution and Grasping Observation Activity of Single Neurons in the Macaque Anterior Intraparietal Area

“…AIP is connected with the F5a sector in PMv and to PFG (Gerbella, Belmalih, Borra, Rozzi, & Luppino, 2011;Belmalih et al, 2009;Borra et al, 2008), and these latter areas are both connected with the F5c sector in PMv. Furthermore TMS in humans has shown that AIP and PMv causally interact during object grasping (Davare, Rothwell, & Lemon, 2010), and it has been shown that AIP and F5a neurons share very similar visual selectivities for 3-D shape and grasping activity (Theys, Pani, van Loon, Goffin, & Janssen, 2013;Theys, Pani, et al, 2012;Theys, Srivastava, et al, 2012). Interestingly, videos of a grasping isolated hand activate the macaque AIP and F5a-even in the absence of an objectbut not F5c (Nelissen et al, 2011;Nelissen, Luppino, Vanduffel, Rizzolatti, & Orban, 2005).…”

“…monitor equipped with ultrafast P46 phosphor, frame rate 120 Hz, Vision Research Graphics, experimental setup as in Theys, Pani, van Loon, Goffin, & Janssen, 2012) on which videos of grasping actions were presented at a viewing distance of 40 cm (i.e., in extrapersonal space) during the passive fixation of a small spot located in the center of the display. Movie onset and end were registered by a photodiode attached to the lower right corner of the screen detecting the onset of a bright square (occluded and not visible to the monkey) appearing simultaneously with stimulus onset and endpoint.…”

Through the forest of motor representations

“…This visuomotor transformation relies on a well defined parietal-premotor network lying in between the posterior parietal cortex and the ventral premotor cortex, that is, a precise portion of the V-D, whose main components for these tasks are the anterior intraparietal (AIP) area (related to the anterior intraparietal sulcus) and area F5, in the most rostral part of the ventral premotor cortex (for a review of the leading role of AIP-F5 in the detection of action possibilities and the related visuomotor transformation of object properties into action properties and then of action properties into motor acts see Baumann, Fluet, & Scherberger, 2009;Borghi & Riggio, 2015;Castiello, 2005;Castiello & Begliomini, 2008;Chinellato & del Pobil, 2016;Ferretti, 2016;Fluet, Baumann, & Scherberger, 2010;Grafton, 2010;Janssen & Scherberger, 2015;Kandel, Schwartz, Jessell, Siegelbaum, & Hudspeth, 2013: chap. 19;Murata et al, 1997;Murata, Gallese, Luppino, Kaseda, & Sakata, 2000;Raos et al, 2006;Romero, Pani, & Janssen, 2014;Sakata, Taira, Murata, & Mine, 1995;Shikata et al, 2003;Srivastava, Orban, De Mazière, & Janssen, 2009;Theys, Pani, van Loon, Goffin, & Janssen, 2012Theys, Srivastava, van Loon, Goffin, & Janssen, 2012;Theys, Romero, van Loon, & Janssen, 2015 concerning lesion studies see Andersen, Andersen, Hwang, & Hauschild, 2014;Graziano, 2009;Turella & Lignau, 2014) -see footnote 19.…”