Processing of own hand visual feedback during object grasping in ventral premotor mirror neurons

Mirror neurons (MNs) discharge during action execution as well as during observation of others’ actions. Our own actions are those that we have the opportunity to observe more frequently, but no study thus far to our knowledge has addressed the issue of whether, and to what extent, MNs can code own hand visual feedback (HVF) during object grasping. Here, we show that MNs of the ventral premotor area F5 of macaque monkeys are particularly sensitive to HVF relative to non-MNs simultaneously recorded in the same penetrations. Importantly, the HVF effect is more evident on MN activity during hand-object interaction than during the hand-shaping phase. Furthermore, the increase of MN activity induced by HVF and others’ actions observed from a subjective perspective were positively correlated. These findings indicate that at least part of ventral premotor MNs can process the visual information coming from own hand interacting with objects, likely playing a role in self-action monitoring

Differential neural dynamics underling pragmatic and semantic affordance processing in macaque ventral premotor cortex

Premotor neurons play a fundamental role in transforming physical properties of observed objects, such as size and shape, into motor plans for grasping them, hence contributing to "pragmatic" affordance processing. Premotor neurons can also contribute to "semantic" affordance processing, as they can discharge differently even to pragmatically identical objects depending on their behavioural relevance for the observer (i.e. edible or inedible objects). Here, we compared the response of monkey ventral premotor area F5 neurons tested during pragmatic (PT) or semantic (ST) visuomotor tasks. Object presentation responses in ST showed shorter latency and lower object selectivity than in PT. Furthermore, we found a difference between a transient representation of semantic affordances and a sustained representation of pragmatic affordances at both the single neuron and population level. Indeed, responses in ST returned to baseline within 0.5 s whereas in PT they showed the typical sustained visual-to-motor activity during Go trials. In contrast, during No-go trials, the time course of pragmatic and semantic information processing was similar. These findings suggest that premotor cortex generates different dynamics depending on pragmatic and semantic information provided by the context in which the to-be-grasped object is presented

Local and system mechanisms for action execution and observation in parietal and premotor cortices

The action observation network (AON) includes a system of brain areas largely shared with action execution in both human and nonhuman primates. Yet temporal and tuning specificities of distinct areas and of physiologically identified neuronal classes in the encoding of self and others’ action remain unknown. We recorded the activity of 355 single units from three crucial nodes of the AON, the anterior intraparietal area (AIP), and premotor areas F5 and F6, while monkeys performed a Go/No-Go grasping task and observed an experimenter performing it. At the system level, during task execution, F6 displays a prevalence of suppressed neurons and signals whether an action has to be performed, whereas AIP and F5 share a prevalence of facilitated neurons and remarkable target selectivity; during task observation, F5 stands out for its unique prevalence of facilitated neurons and its stronger and earlier modulation than AIP and F6. By applying unsupervised clustering of spike waveforms, we found distinct cell classes unevenly distributed across areas, with different firing properties and carrying specific visuomotor signals. Broadly spiking neurons exhibited a balanced amount of facilitated and suppressed activity during action execution and observation, whereas narrower spiking neurons showed more mutually facilitated responses during the execution of one’s own and others’ action, particularly in areas AIP and F5. Our findings elucidate the time course of activity and firing properties of neurons in the AON during one’s own and others’ action, from the system level of anatomically distinct areas to the local level of physiologically distinct cell classes

Selectivity for grip type and action goal in macaque inferior parietal and ventral premotor grasping neurons.

Grasping objects requires the selection of specific grip postures in relation to objects' physical properties. Furthermore, grasping acts can be embedded into actions aimed at different goals, depending on the context in which the action is performed. Here we assessed whether information on grip and action type integrate at the single neuron level within the parieto-frontal motor system. For this purpose, we trained three monkeys to perform simple grasp-to-eat and grasp-to-place actions, depending on contextual cues, in which different grip types were required, in relation to target features. We recorded 173 grasping neurons: 86 from the inferior parietal area PFG and 87 from the ventral premotor area F5. Results showed that most neurons in both areas are selective for the grip type, but the discharge of many of them, particularly in PFG, appears to differ in relation to action context. Kinematics data and control experiments indicated that neuronal selectivity appears to more likely depend on the action goal triggered by the context rather than on specific contextual elements. The temporal dynamics of grip and goal selectivity showed that grasping neurons reflect first "how" the object has to be grasped (grip), to guide and monitor the hand shaping phase, then "why" the action is performed (goal), very likely to facilitate subsequent motor acts following grasping. These findings suggest that, in the parieto-frontal system, grip types and action goals are processed by both parallel and converging pathways, and area PFG appears to be particularly relevant for integrating this information for action organization

Anterior Intraparietal Area: a Hub in the Observed Manipulative Action Network.

Current knowledge regarding the processing of observed manipulative actions (OMAs) (e.g., grasping, dragging, or dropping) is limited to grasping and underlying neural circuitry remains controversial. Here, we addressed these issues by combining chronic neuronal recordings along the anteroposterior extent of monkeys\u2019 anterior intraparietal (AIP) area with tracer injections into the recorded sites. We found robust neural selectivity for 7 distinct OMAs, particularly in the posterior part of AIP (pAIP), where it was associated with motor coding of grip type and own-hand visual feedback. This cluster of functional properties appears to be specifically grounded in stronger direct connections of pAIP with the temporal regions of the ventral visual stream and the prefrontal cortex, as connections with skeletomotor related areas and regions of the dorsal visual stream exhibited opposite or no rostrocaudal gradients. Temporal and prefrontal areas may provide visual and contextual information relevant for manipulative action processing. These results revise existing models of the action observation network, suggesting that pAIP constitutes a parietal hub for routing information about OMA identity to the other nodes of the network

Organizzazione anatomo-funzionale della porzione laterale della corteccia motoria primaria e premotoria di scimmia

Le attuali conoscenze sulle diverse funzioni assolte dalle aree localizatte tra il solco arcuato inferiore e il solco centrale della scimmia sono prevalentemente basate su studi sperimentali focalizzati su ristretti settori corticali. Manca una visione generale sulla distribuzione delle proprietà funzionali di questa ampia regione e, soprattutto, abbiamo scarse informazioni sulla sua convessità laterale. In questo studio sono state utilizzate la microstimolazione intracorticale e la registrazione extracellulare dell’attività neuronale su due scimmie allo scopo di descrivere le proprietà funzionali generali dell’intera regione e la loro relazione con le diverse suddivisioni citoarchitettoniche di cui si compone, ovvero, le aree F1, F4 ed F5. I risultati mostrano che nella porzione caudale della regione registrata esiste un settore ventrale che attraversa i bordi anatomici tra F4 ed F1, caratterizzato da elevata eccitabilità elettrica, movimenti semplici di bocca, frequenti risposte somatosensoriali ma assenza di risposte visive, mentre la controparte dorsale delle stesse aree presenta soglie di stimolazione più alte, atti motori di braccio-mano e bocca e diversi tipi di risposte visive. Nella porzione rostrale della regione registrata, l’area F5c sembra ben caratterizzata sia dal punto di vista anatomico che funzionale, mostrando un drastico crollo dell’eccitabilità elettrica, spiccata specificità motoria per il tipo di prensione utilizzato per afferrare oggetti, e proprietà visive più complesse, come per esempio risposte di tipo “mirror”. Nel complesso, questi dati consentono di delineare alcune similarità funzionali tra la corteccia motoria frontale dell’uomo e della scimmia, suggerendo che i settori posteriori siano maggiormente coinvolti nell’organizzazione e controllo fine di atti motori diretti ad uno scopo e movimenti della bocca entro parti diverse dello spazio personale e peri-personale, mentre la corteccia premotoria ventrale rostrale possiede la capacità di sfruttare la conoscenza motoria dell’individuo ad un livello più astratto, consentendo l’emergere di funzioni socio-cognitive che potrebbero essere state importanti precursori per l’evoluzione del linguaggio umano.The current knowledge on the different functions played by the areas comprised between the inferior arcuate and the central sulcus of the monkey is mainly based on experimental studies focused on restricted cortical sectors, and only few information is available about its lateral convexity. Here we carried out intracortical microstimulations (ICMS) and extracellular recordings of neuronal activity in the most lateral portion of the frontal motor and premotor cortex of two macaque monkeys, to the purpose of describing the functional properties of these regions and their relationship with the different cytoarchitectonic subdivisions, namely, area F1, F4 and F5. Results showed that in the caudal part of the recorded region there is a ventral sector encompassing the anatomic border between F4 and F1, which appears characterized by high electrical excitability, mouth simple movements, and absence of visual properties, while the dorsal counterpart of the same areas show higher stimulation thresholds, forelimb and mouth motor acts, and different types of visual properties. In the rostral part of the recorded region, area F5c appears to be well characterized from both the anatomical and functional point of view, showing a dramatic drop of cortical excitability, higher motor specificity for the type of grip, and more complex visual properties, such as mirror responses. Taken together, these data allow to trace some functional similarities between the monkey and the human frontal motor cortex, suggesting that the posterior sectors are more involved in the organization and fine control of goal directed motor acts and mouth movement within different part of the personal and peripersonal space, while the rostral ventral premotor cortex possesses the capacity to exploit the individual’s motor knowledge at a more abstract level, enabling the emergence of socio-cognitive functions which could have been important precursors for the evolution of human language

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

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