Simultaneous Recording of Macaque Premotor and Primary Motor Cortex Neuronal Populations Reveals Different Functional Contributions to Visuomotor Grasp

2011

Despite recent advances in harnessing cortical motor-related activity to control computer cursors and robotic devices, the ability to decode and execute different grasping patterns remains a major obstacle. Here we demonstrate a simple Bayesian decoder for real-time classification of grip type and wrist orientation in macaque monkeys that uses higher-order planning signals from anterior intraparietal cortex (AIP) and ventral premotor cortex (area F5). Real-time decoding was based on multiunit signals, which had similar tuning properties to cells in previous single-unit recording studies. Maximum decoding accuracy for two grasp types (power and precision grip) and five wrist orientations was 63% (chance level, 10%). Analysis of decoder performance showed that grip type decoding was highly accurate (90.6%), with most errors occurring during orientation classification. In a subsequent off-line analysis, we found small but significant performance improvements (mean, 6.25 percentage points) when using an optimized spike-sorting method (superparamagnetic clustering). Furthermore, we observed significant differences in the contributions of F5 and AIP for grasp decoding, with F5 being better suited for classification of the grip type and AIP contributing more toward decoding of object orientation. However, optimum decoding performance was maximal when using neural activity simultaneously from both areas. Overall, these results highlight quantitative differences in the functional representation of grasp movements in AIP and F5 and represent a first step toward using these signals for developing functional neural interfaces for hand grasping.

Section: Multiunit Coding Propertiessupporting

confidence: 89%

“…However, modulation by orientation was absent. The observed strong modulation by grip type has been well characterized in previous single-unit studies of F5 Raos et al, 2006;Umilta et al, 2007;Fluet et al, 2010).…”

Section: Distribution Of Tuned Activitysupporting

confidence: 70%

Grasp Movement Decoding from Premotor and Parietal Cortex

Townsend¹,

Subasi²,

2011

“…9A), S cells were tuned for precision and power grips equally often, whereas SM and M cells showed a clear overrepresentation of precision grips. An overrepresentation of precision grips has been described in motor areas and could be due to the fact that complex grip types may need more neural resources for planning and execution than simpler grips (Muir and Lemon, 1983;Lemon et al, 2004;Umilta et al, 2007). In contrast, the balanced ratio of S cells suggests that these cells might employ a more abstract representation with equal resources for both grips.…”

Section: Specific Coding Of Cell Classesmentioning

confidence: 99%

“…It therefore requires the transformation of sensory information into appropriate hand motor commands. The ventral premotor cortex (PMv) in the frontal cortex, specifically area F5, participates in such visuomotor transformations for grasping (Gentilucci et al, 1983;Murata et al, 1997;Fogassi et al, 2001;Cerri et al, 2003;Umilta et al, 2007). Anatomically, area F5 is strongly and reciprocally connected to the parietal cortex, in particular to the anterior intraparietal area (AIP) (Matelli et al, 1986;Luppino et al, 1999;Tanné-Gariépy et al, 2002;Borra et al, 2008), which also contains hand grasping signals (Taira et al, 1990;Sakata et al, 1995;Murata et al, 2000;Baumann et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

Context-Specific Grasp Movement Representation in Macaque Ventral Premotor Cortex

Fluet¹,

Baumann²,

2010

110

109

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.

“…We consider late-onset neurons to be closely related to movement execution based on the following arguments: the overrepresentation of precision grips could be explained by the need of increased neural resources for controlling fine precision grips as opposed to power grips, as observed in other cortical areas (e.g., M1 and F5) (Muir and Lemon, 1983;Lemon et al, 2004;Umilta et al, 2007). Likewise, the overrepresentation of extreme object orientations could be explained by a motor-related encoding, namely a push-pull representation in pronation/supination coordinates.…”

Section: Possible Coding Schemesmentioning

confidence: 99%

Context-Specific Grasp Movement Representation in the Macaque Anterior Intraparietal Area

Baumann¹,

Fluet²,

2009

226

237

To perform grasping movements, the hand is shaped according to the form of the target object and the intended manipulation, which in turn depends on the context of the action. The anterior intraparietal cortex (AIP) is strongly involved in the sensorimotor transformation of grasping movements, but the extent to which it encodes context-specific information for hand grasping is unclear. To explore this issue, we recorded 571 single-units in AIP of two macaques during a delayed grasping task, in which animals were instructed by an external context cue (LED) to perform power or precision grips on a handle that was presented in various orientations. While 55% of the recorded neurons encoded the object orientation from the cue epoch on, the number of cells encoding the grip type increased from 25% during the cue epoch to 58% during movement execution. Furthermore, a classification of cells according to the time of their tuning onset revealed differences in the function and anatomical location of early-versus late-tuned cells. In a cue separation task, when the object was presented first, neurons representing power or precision grips were activated simultaneously until the actual grip type was instructed. In contrast, when the grasp type instruction was presented before the object, type information was only weakly represented in AIP, but was strongly encoded after the grasp target was revealed. We conclude that AIP encodes context specific hand grasping movements to perceived objects, but in the absence of a grasp target, the encoding of context information is weak.