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.

Figure 1.

Task paradigm and recording sites. A, Picture of the handle. Two sensors in grooves (red circle, only one sensor visible) detected the execution of the precision grip, and a light barrier (red line) detected the insertion of the monkey hand into the handle during power grip execution. B, Representation of the time course of the delayed grasping task. The task is divided into four epochs: fixation, cue, planning, and movement. The entire task is performed in the dark except for the cue period in which the handle is visible and a colored LED indicates the grip type (power or precision). The lights are projected onto the middle of the handle through a half mirror. C, MRI section showing a coronal view of monkey J. Red line indicates the orientation of the recording chamber, white crosses indicate image artifacts from two titanium bone screws located within (not below) the skull. D, MRI section of the right hemisphere of monkey L in the plane of the recording chamber. Superimposed on the image are the recording sites in area F5 (yellow dots). E, Same as D for monkey J.

Figure 2.

Firing rate histograms and raster plots of four example neurons. A–D, Left, Precision grip trials. Right, Power grip trials. The five orientations are represented by different colors. Graphs are doubly aligned to the end of the cue and the release of the handrest button (black arrowheads). Realignment occurs at 0.6 s and is marked by a gap in the curves and the spike rasters. Black vertical lines mark cue onset, cue offset, and the go-signal. The dotted line within the movement epoch indicates the handrest release and the gray line the (mean) time of handle contact. A, Neuron modulated by grip type and orientation from the cue until completion of the task. B, Neuron modulated by grip type only, starting from the cue until task completion. C, Neuron showing no task modulation during cue and planning, but clear grip-type tuning during movement execution. D, Neuron modulated by grip type and orientation exclusively in the cue period.

Figure 3.

Population firing rate of the 420 cells during the preferred and nonpreferred conditions (grip type and orientation). Alignment and definition of time epochs as in Figure 2.

Figure 4.

Grip type and orientation tuning in the population (n = 420). A, Percentage of cells that are tuned for grip type (black) and object orientation (gray) during each task epoch (fixation, cue, planning, and movement) (ANOVA, p < 0.01). B, Percentage of tuned cells for grip type (black) and object orientation (gray) in 200 ms time windows (ANOVA, p < 0.01; curves report data at the center of each window). Alignment and definition of time epochs as in Figure 2.

Figure 5.

Preferred grip type and orientation of significantly tuned cells in each task epoch. A, Number of grip type-specific cells preferring precision (white) and power grip (black) during the cue, planning, and movement epoch. B, Number of orientation-specific cells preferring individual object orientations (−50°, −25°, 0°, 25°, 50°) during cue, planning, and movement.

Figure 6.

Tuning consistency between different task epochs. A, Grip type tuning consistency. Number of cells that kept (black), altered (gray), or lost (white) their tuning from cue to planning and from the planning to the movement epoch. B, Orientation tuning consistency. Fraction of cells as a function of shift from their preferred orientation (in degrees) from cue to planning and from planning to movement. n.t., No longer tuned.

Figure 7.

Time of significant tuning of grip type and orientation. A, Sliding window analysis indicating the times with significant grip-type tuning (black lines) for each cell (ANOVA, p < 0.01; window size, 200 ms; step, 50 ms; centered in the middle of the window). Cells are ordered by tuning onset; red dots indicate tuning offset. B, Same as A, for orientation tuning. C–D, Histograms of tuning onset of grip type and orientation. E–F, Histograms of tuning offset for grip type and orientation.

Figure 8.

Scatter plots of tuning onset and offset. A, B, Cell classification based on the tuning onset and tuning offset for grip type (A) and orientation (B). The separation between the S, SM, and M classes is set at 0.7 s (gray lines).

Figure 9.

Specific tuning for grip type and orientation (orient) in cell classes. A, Percentage of grip type-specific cells preferring precision (white) versus power grip (black) for sensory, sensorimotor, and motor cells. B, Histogram, Number of cells preferring individual object orientations (−50°, −25°, 0°, 25°, 50°) for sensory, sensorimotor, and motor cells. Pie chart, Percentage of orientation-specific cells preferring extreme orientations (black) or middle orientations (gray).

Figure 10.

Anatomical distribution of cell classes. Percentage of sensory (white bars), sensorimotor (gray bars), and motor cells (black bars) for grip type (left) and object orientation (right) as a function of their position along the inferior arcuate sulcus.