Decoding a Wide Range of Hand Configurations from Macaque Motor, Premotor, and Parietal Cortices

Abstract

Despite recent advances in decoding cortical activity for motor control, the development of hand prosthetics remains a major challenge. To reduce the complexity of such applications, higher cortical areas that also represent motor plans rather than just the individual movements might be advantageous. We investigated the decoding of many grip types using spiking activity from the anterior intraparietal (AIP), ventral premotor (F5), and primary motor (M1) cortices. Two rhesus monkeys were trained to grasp 50 objects in a delayed task while hand kinematics and spiking activity from six implanted electrode arrays (total of 192 electrodes) were recorded. Offline, we determined 20 grip types from the kinematic data and decoded these hand configurations and the grasped objects with a simple Bayesian classifier. When decoding from AIP, F5, and M1 combined, the mean accuracy was 50% (using planning activity) and 62% (during motor execution) for predicting the 50 objects (chance level, 2%) and substantially larger when predicting the 20 grip types (planning, 74%; execution, 86%; chance level, 5%). When decoding from individual arrays, objects and grip types could be predicted well during movement planning from AIP (medial array) and F5 (lateral array), whereas M1 predictions were poor. In contrast, predictions during movement execution were best from M1, whereas F5 performed only slightly worse. These results demonstrate for the first time that a large number of grip types can be decoded from higher cortical areas during movement preparation and execution, which could be relevant for future neuroprosthetic devices that decode motor plans.

Extending the Cortical Grasping Network: Pre-supplementary Motor Neuron Activity During Vision and Grasping of Objects

“…Although this percentage is clearly lower than that obtained for area F5 (41%), there are several additional similarities between object processing in the 2 areas, strengthening the idea of their functional interplay. First, we showed that neuronal discharge and object selectivity of F6 purely motor neurons were the same during grasping in both the light and the dark, indicating that their activity truly reflects a motor encoding of the hand grip, as previously shown for F5 (Raos et al 2006; Schaffelhofer et al 2015). Second, both the visual presentation response and object selectivity of F6 visuomotor neurons were stronger during go trials, which is consistent with previous findings in F5 (Raos et al 2006; Bonini et al 2014a), and suggests that visuomotor neurons of both areas encode visually presented objects in a motor format.…”

“…6 B ). In contrast, visuomotor neurons of area F5 display the typical visual-to-motor activation and selectivity pattern highlighted by several previous studies (Murata et al 1997; Raos et al 2006; Bonini et al 2014a; Schaffelhofer et al 2015), in which the motor-related discharge is even stronger than the visual one (Fig. 6 F ).…”

Organization and evolution of parieto-frontal processing streams in macaque monkeys and humans

“…AIP and F5 provides a good prediction of object and grip type during movement preparation, while motor cortex performs better during movement execution (Schaffelhofer et al, 2015), when F5 predictions deteriorate. The force input necessary for objects grasping, manipulation and tools use within this parietal network is first encoded in areas PFG/PG (Ferrari-Toniolo et al, 2015), where the population activity encodes dynamic force and its increments over time, and retains memory of unexpected changes in force conditions, thus providing a reservoir for future hand-object interactions.…”

“…The somato-motor stream (SS-MI clusters) encodes information related more directly to arm movement, such as limb position (Caminiti et al, 1990;Georgopoulos et al, 1984;Lacquaniti et al, 1995;Mountcastle and Powel, 1959;Prud'homme and Kalaska, 1994), movement direction (Caminiti et al, 1990;Georgopoulos et al, 1981;Lacquaniti et al, 1995), amplitude (Fu et al, 1993), velocity (Archambault et al, 2009(Archambault et al, , 2011Ashe and Georgopoulos, 1995;Averbeck et al, 2005;Moran and Schwartz, 1999), acceleration (Ashe and Georgopoulos, 1995), force (Cheney and Fetz, 1980;Georgopoulos et al, 1992;Hepp-Raymond et al, 1978;Kakei et al, 1999;Mayer et al, 1993;Sergio et al, 2005), hand grip type (Muir and Lemon, 1983;Schaffelhofer et al, 2015). The activity of individual cells is influenced by most movement parameters (Ashe and Georgopoulos, 1995), and their graded utilization is used for online control of hand trajectory by motor cortical cells (Archambault et al, 2011).…”

Wireless recording from unrestrained monkeys reveals motor goal encoding beyond immediate reach in frontoparietal cortex

“…Except for the steps related to our novel chamber system, the procedures for FMA implantation were equivalent to what was described in (Schaffelhofer, Agudelo-Toro, & Scherberger, 2015). The animal was placed in a stereotaxic instrument to stabilize the head and provide a Horsley-Clarke coordinate system.…”