Spatial and viewpoint selectivity for others’ observed actions in monkey ventral premotor mirror neurons

Abstract

The spatial location and viewpoint of observed actions are closely linked in natural social settings. For example, actions observed from a subjective viewpoint necessarily occur within the observer’s peripersonal space. Neurophysiological studies have shown that mirror neurons (MNs) of the monkey ventral premotor area F5 can code the spatial location of live observed actions. Furthermore, F5 MN discharge can also be modulated by the viewpoint from which filmed actions are seen. Nonetheless, whether and to what extent MNs can integrate viewpoint and spatial location of live observed actions remains unknown. We addressed this issue by comparing the activity of 148 F5 MNs while macaque monkeys observed an experimenter grasping in three different combinations of viewpoint and spatial location, namely, lateral view in the (1) extrapersonal and (2) peripersonal space and (3) subjective view in the peripersonal space. We found that the majority of MNs were space-selective (60.8%): those selective for the peripersonal space exhibited a preference for the subjective viewpoint both at the single-neuron and population level, whereas space-unselective neurons were view invariant. These findings reveal the existence of a previously neglected link between spatial and viewpoint selectivity in MN activity during live-action observation.

Perspective-dependent reactivity of sensorimotor mu rhythm in alpha and beta ranges during action observation: an EEG study

“…According to this latter hypothesis, on the one hand, both FP and LE, considered “egocentric” since anatomical details of displayed actions are congruent with those of observed self-movements and body parts, should induce the strongest levels of mu suppression. On the contrary, LE evoked significantly lower suppression than FP in both frequency ranges, matching recent single-neuron recording evidence in monkeys of a preferential tuning of F5 MNs to actions seen from FP relative to LE 6 . On the other hand, LE should induce stronger mu suppression than LA, while no significant differences emerged in our study either in alpha or in beta ranges.…”

“…Theoretically, others’ actions perceived from egocentric perspectives, being more visually similar to self-actions, should induce a stronger activation in the motor system of the observer with respect to actions perceived from allocentric viewpoints. Nevertheless, experimental data so far available in monkeys 4 – 6 and humans 7 – 15 are inconsistent and definite evidence is still lacking. Indeed, a single-cell recording study in macaques revealed view-dependent responses in most of F5 mirror neurons (MNs), which were tuned to one or, more frequently, two viewpoints among three tested perspectives (FP, lateral and TP).…”

“…Nonetheless, a further study on local field potentials (LFPs) of F5 MNs confirmed the preference for FP relative to TP 5 . More recently, single-cell recordings demonstrated a prevalent tuning of F5 MNs to FP than to LE during observation of actions carried out in monkey’s peripersonal space 6 . While AO experiments in monkeys included both longitudinal and lateral perspectives, human studies compared only cerebral responses evoked by FP vs TP, with inconsistent results.…”

Idiosyncratic representation of peripersonal space depends on the success of one's own motor actions, but also the successful actions of others!

“…We may thus assume that the observed manual reaching actions were processed by participants from a first-person perspective [ 67 , 73 ], integrating the outcomes of the observed actions, as if they were performed by the observer in agreement with the mirror system hypothesis [ 74 – 75 ]. In support of this view, mirror neurons in monkey studies were found to be space-selective and also sensitive to the viewpoint during live-action observation [ 76 ]. We may thus speculate that, in a social context, participants’ representation of peripersonal space extended so as to overlap or merge with the peripersonal space of the (successful) facing conspecific.…”

Movement initiation and grasp representation in premotor and primary motor cortex mirror neurons

“…The task design itself, with observed actions taking place within the monkey’s reach, may introduce some similarity between observation and NoGo, such that the strategy adopted by the monkeys is to treat the observation Go cue and NoGo cue similarly. Observed actions occurring in peri-personal space often modulate MirN responses differently to when the action is beyond the monkey’s reach (Caggiano et al, 2009; Bonini et al, 2014a; Maranesi et al, 2017), suggesting the capability to interact with observed actions is an important aspect of mirror activity. A further important point is the difference between F5 and M1, which indicate that while M1’s priority is to distinguish movement from non-movement from an egocentric perspective, F5 maintains a more similar representation across executed and observed actions, independent of the acting agent’s identity.…”