Context-Specific Grasp Movement Representation in Macaque Ventral Premotor Cortex

Abstract

Hand grasping requires the transformation of sensory signals to hand movements. Neurons in area F5 (ventral premotor cortex) represent specific grasp movements (e.g., precision grip) as well as object features like orientation, and are involved in movement preparation and execution. Here, we examined how F5 neurons represent context-dependent grasping actions in macaques. We used a delayed grasping task in which animals grasped a handle either with a power or a precision grip depending on context information. Additionally, object orientation was varied to investigate how visual object features are integrated with context information. In 420 neurons from two animals, object orientation and grip type were equally encoded during the instruction epoch (27% and 26% of all cells, respectively). While orientation representation dropped during movement execution, grip type representation increased (20% vs 43%). According to tuning onset and offset, we classified neurons as sensory, sensorimotor, or motor. Grip type tuning was predominantly sensorimotor (28%) or motor (25%), whereas orientation-tuned cells were mainly sensory (11%) or sensorimotor (15%) and often also represented grip type (86%). Conversely, only 44% of grip-type tuned cells were also orientation-tuned. Furthermore, we found marked differences in the incidence of preferred conditions (power vs precision grips and middle vs extreme orientations) and in the anatomical distribution of the various cell classes. These results reveal important differences in how grip type and object orientation is processed in F5 and suggest that anatomically and functionally separable cell classes collaborate to generate hand grasping commands.

Grasp Movement Decoding from Premotor and Parietal Cortex

“…Using predominantly multiunit activity recorded simultaneously from AIP and F5, we demonstrated real-time decoding by maximum likelihood estimation. The tuning properties of these multiunit data were largely similar to single-unit studies (Baumann et al, 2009;Fluet et al, 2010), with neural activity in F5 being better suited for the decoding of grip type and that in AIP being more accurate for predicting object orientation.…”

“…For grasping, key areas for such high-level control are ventral premotor cortex (area F5) and anterior intraparietal cortex (AIP), which are strongly interconnected (Luppino et al, 1999) and form a frontoparietal network for transforming visual signals into hand grasping instructions (Jeannerod et al, 1984;Kakei et al, 1999;Brochier and Umilta, 2007). Unlike M1, these areas represent upcoming hand movements at a conceptual or categorical level well before their execution (Musallam et al, 2004;Baumann et al, 2009;Fluet et al, 2010). Targeting these areas could therefore considerably simplify the decoding of complex movements.…”

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

“…Moreover the presence of visualdominant neurons encoding 3D object information in F5a also provides a functional interpretation of the concept of pre-premotor cortex, as suggested by Gerbella et al (2010): the pre-premotor F5a sector is clearly much more visual than the other F5 sectors, where previous studies have observed no visual-dominant neurons (Raos et al, 2006). Fluet et al (2010), however, also described the presence of "sensory" (visual-dominant) neurons in F5. These authors reported a higher concentration of sensory orientation-tuned neurons in a dorsal and a ventral F5 region, which they related to the sites in F5 with strong AIP inputs described by Borra et al (2008).…”

“…These authors reported a higher concentration of sensory orientation-tuned neurons in a dorsal and a ventral F5 region, which they related to the sites in F5 with strong AIP inputs described by Borra et al (2008). It is conceivable that one of these F5 regions with sensory neurons described by Fluet et al (2010) may have at least partially corresponded to F5a. Note that the so-called "canonical" neurons, which respond during object fixation and during object grasping, were recorded in F5p (Rizzolatti et al, 2002).…”

Spatiotemporal distribution of location and object effects in the electromyographic activity of upper extremity muscles during reach-to-grasp

“…The dorsal premotor cortex (PMd) has been studied most frequently during reaching (Cisek and Kalaska 2005;Hatsopoulos et al 2004;Weinrich et al 1984) and the ventral premotor cortex (PMv), most frequently during grasping (Carpaneto et al 2011;Fluet et al 2010;Raos et al 2006;Rizzolatti et al 1988;Spinks et al 2008). A number of studies have shown, however, that many neurons in PMd and PMv vary their discharge in relation to both the location of reaching and the object grasped (Bansal et al 2012;Raos et al 2004;Stark et al 2007;Wu and Hatsopoulos 2007), calling into question the notion that PMd controls reaching, whereas PMv controls grasping.…”