Space-dependent representation of objects and other's action in monkey ventral premotor grasping neurons

Abstract

The macaque ventral premotor area F5 hosts two types of visuomotor grasping neurons: "canonical" neurons, which respond to visually presented objects and underlie visuomotor transformation for grasping, and "mirror" neurons, which respond during the observation of others' action, likely playing a role in action understanding. Some previous evidence suggested that canonical and mirror neurons could be anatomically segregated in different sectors of area F5. Here we investigated the functional properties of single neurons in the hand field of area F5 using various tasks similar to those originally designed to investigate visual responses to objects and actions. By using linear multielectrode probes, we were able to simultaneously record different types of neurons and to precisely localize their cortical depth. We recorded 464 neurons, of which 243 showed visuomotor properties. Canonical and mirror neurons were often present in the same cortical sites; and, most interestingly, a set of neurons showed both canonical and mirror properties, discharging to object presentation as well as during the observation of experimenter's goal-directed acts (canonical-mirror neurons). Typically, visual responses to objects were constrained to the monkey peripersonal space, whereas action observation responses were less space-selective. Control experiments showed that space-constrained coding of objects mostly relies on an operational (action possibility) rather than metric (absolute distance) reference frame. Interestingly, canonical-mirror neurons appear to code object as target for both one's own and other's action, suggesting that they could play a role in predictive representation of others' impending actions.

Keywords: area F5; canonical neurons; macaque; mirror neurons; visuomotor neurons.

Figure 1.

Apparatus, tasks phases, and conditions of the VMT and OT. A, Box and apparatus settled for performing the VMT. B, C, Box and apparatus settled for performing the OT in the monkey's extrapersonal (OTe) and peripersonal (OTp) space. Dashed circles represent the physical extension of the 5° tolerance window for monkey's eye position during each task. D, Task phases of object fixation, grasping in the light, and grasping in the dark conditions of the VMT. The temporal structure and task phases of the observation tasks are identical to those of the corresponding conditions of the VMT.

Figure 2.

Functional map of body parts movement derived from preliminary recordings in each monkey. The light blue shaded area identifies, in each monkey, the hand sector of area F5 where the penetrations included in the present study (data not shown) have been performed. Penetrations were performed at an approximate angle of 40° relative to the sagittal plane. Each penetration in the recording region was located within a maximum of 3 mm from penetrations performed in FEF. The asterisk in the map of M1 identifies the location of the exemplary penetration shown in Figure 3. As, Arcuate sulcus; FEF, frontal eye fields; R, rostral; C, caudal; M, medial; L, lateral. The junction of the spur with the arcuate sulcus is located (in anteroposterior and mediolateral stereotaxic coordinates) at 21.5–20 in M1 and 22–18 in M2.

Figure 3.

A, Schematic drawing of a linear multielectrode probe and example of the multiunit activity simultaneously recorded during a typical penetration. The multiunit activity, which is the aggregate spiking activity of a number of neurons in the vicinity of an electrode (Supèr and Roelfsema, 2005), is plotted in spikes based on color code and aligned (white line) on the moment when the monkey started pulling the target object (45 trials for each panel, with the three objects pooled together). The location of this penetration, performed in M1, is shown by the asterisk in the functional map of Figure 2. B, Example of a purely motor neuron (Unit A), a canonical neuron (Unit B), and a mirror neuron (Unit C), simultaneously recorded and off-line sorted from the multiunit activity of channel 13 of the penetration shown in A. For each neuron, the gap in the histogram and rastergram is used to indicate that the activity on its left side has been aligned on object presentation (first vertical dashed line in the left panel), whereas that on its right side is aligned on the pulling onset (second vertical dashed line in the right panel) of the same trial. The gray shaded areas represent the time windows used for statistical analysis of neuronal response. Markers: dark green, cue sound onset; light green, cue sound offset (go signal); orange, detachment of the hand from the starting position (reaching onset); red, reward delivery at the end of the trial. The same markers have been used to identify the behavioral event of interest of both the visuomotor and observation tasks.

Figure 4.

Examples of canonical-mirror neurons. Differences in the baseline firing rates shown by some of the neurons between VMT and OT depend on the different behavioral setting that characterizes the two task contexts because, in the period used as baseline, the monkey was already fixating and was instructed on the ongoing task context and experimental condition. However, these differences do not affect the results of data analyses (see Materials and Methods) and their interpretation. Conventions as in Figure 3B.

Figure 5.

Depth distribution of all the recorded neurons. A similar profile of property distribution characterized the recordings performed at different rostrocaudal levels.

Figure 6.

Histograms showing the relative proportion of mirror, canonical-mirror, and canonical neurons selectively responding to visual stimuli presented either in the peripersonal (black) or extrapersonal (white) space, or activated for stimuli presented in both space sectors (gray). Histograms for canonical-mirror neurons have been represented twice to show the space selectivity of both their response to mirror (on the left) and canonical (on the right).

Figure 7.

A, Distribution of object-action contrast indexes computed for all canonical-mirror neurons in the peripersonal and extrapersonal space. There is a relative advantage for action (light gray bars represent negative values) compared with object (dark gray bars represent positive values) coding in the extrapersonal, but not in the peripersonal, space. B, Time course and intensity of the net normalized response of canonical-mirror neuronal population relative to the preferred (red) and not preferred (blue) target object. The activity is aligned on the light onset during fixation (left) and grasping (center) condition, as well as on the object pulling onset (right). Gray shaded regions identify the time windows used for statistical analysis of neural activity: Pulling onset divides the grasping period into two epochs: an “early grasping” (gray shading on the left of the alignment point) and “pulling” (gray shading on the right of the alignment point). Obj pres, object presentation epoch.

Figure 8.

A, Pie-chart showing the proportion of canonical-mirror (left) and canonical (right) neurons with visual presentation responses selective or unselective for a specific orientation of the presented object. B, Correlation between the visual responses triggered by object presented with 0° and 90° orientation in canonical-mirror and canonical neurons. C, Comparison among object presentation responses during the fixation (OTe-fix) and grasping (OTe-grasp) conditions of the OTe, the OTp, and the fixation (VMT-fix) and grasping (VMT-grasp) conditions of the VMT. *p < 0.001. ns, not significant.

Figure 9.

A, Example of a canonical neuron recorded during a control experiment with the object presented behind a transparent plastic barrier. Object presentation responses are shown for the different objects in the different tasks and conditions. The green markers indicate the onset of the cue sound at the beginning of each trial. Other conventions as in Figure 3B. B, Time course and intensity of the net normalized response of canonical-mirror and canonical neuronal populations relative to the preferred (red) and not preferred (blue) target object. The activity is aligned on the light onset during different tasks and conditions. Other conventions as in Figure 7B.