Mixed selectivity in monkey anterior intraparietal area during visual and motor processes.

Classical studies suggest that the anterior intraparietal area (AIP) contributes to the encoding of specific information such as objects and actions of self and others, through a variety of neuronal classes, such as canonical, motor and mirror neurons. However, these studies typically focused on a single variable, leaving it unclear whether distinct sets of AIP neurons encode a single or multiple sources of information and how multimodal coding emerges. Here, we chronically recorded monkey AIP neurons in a variety of tasks and conditions classically employed in separate experiments. Most cells exhibited mixed selectivity for observed objects, executed actions, and observed actions, enhanced when this information came from the monkey's peripersonal working space. In contrast with the classical view, our findings indicate that multimodal coding emerges in AIP from partially-mixed selectivity of individual neurons for a variety of information relevant for planning actions directed to both physical objects and other subjects.

Largely shared neural codes for biological and nonbiological observed movements but not for executed actions in monkey premotor areas.

The neural processing of others' observed actions recruits a large network of brain regions (the action observation network; AON) in which frontal motor areas are thought to play a crucial role. As the discovery of mirror neurons (MNs) in the ventral premotor cortex, it has been assumed that their activation was conditional upon the presentation of biological rather than nonbiological motion stimuli, supporting a form of direct visuomotor matching. Nonetheless, nonbiological observed movements have rarely been used as control stimuli to evaluate visual specificity, thereby leaving the issue of similarity among neural codes for executed actions and biological or nonbiological observed movements unresolved. Here, we addressed this issue by recording from two nodes of the AON that are attracting increasing interest, namely, the ventrorostral part of the dorsal premotor area F2 and the mesial presupplementary motor area F6 of macaques while they 1) executed a reaching-grasping task, 2) observed an experimenter performing the task, and 3) observed a nonbiological effector moving in the same context. Our findings revealed stronger neuronal responses to the observation of biological than nonbiological movement, but biological and nonbiological visual stimuli produced highly similar neural dynamics and relied on largely shared neural codes, which in turn remarkably differed from those associated with executed actions. These results indicate that, in highly familiar contexts, visuomotor remapping processes in premotor areas hosting MNs are more complex and flexible than predicted by a direct visuomotor matching hypothesis.NEW & NOTEWORTHY Pioneering studies on mirror neurons (MNs) in premotor areas emphasized the absence of response to the sight of nonbiological moving objects, suggesting a match between execution and observation activities. This study shows that although premotor neurons can discriminate between biological and nonbiological observed movements, these visual stimuli rely on largely shared neural codes, which differ strongly from those associated with executed actions.

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.

Stable readout of observed actions from format-dependent activity of monkey's anterior intraparietal neurons.

Humans accurately identify observed actions despite large dynamic changes in their retinal images and a variety of visual presentation formats. A large network of brain regions in primates participates in the processing of others' actions, with the anterior intraparietal area (AIP) playing a major role in routing information about observed manipulative actions (OMAs) to the other nodes of the network. This study investigated whether the AIP also contributes to invariant coding of OMAs across different visual formats. We recorded AIP neuronal activity from two macaques while they observed videos portraying seven manipulative actions (drag, drop, grasp, push, roll, rotate, squeeze) in four visual formats. Each format resulted from the combination of two actor's body postures (standing, sitting) and two viewpoints (lateral, frontal). Out of 297 recorded units, 38% were OMA-selective in at least one format. Robust population code for viewpoint and actor's body posture emerged shortly after stimulus presentation, followed by OMA selectivity. Although we found no fully invariant OMA-selective neuron, we discovered a population code that allowed us to classify action exemplars irrespective of the visual format. This code depends on a multiplicative mixing of signals about OMA identity and visual format, particularly evidenced by a set of units maintaining a relatively stable OMA selectivity across formats despite considerable rescaling of their firing rate depending on the visual specificities of each format. These findings suggest that the AIP integrates format-dependent information and the visual features of others' actions, leading to a stable readout of observed manipulative action identity.

Connectional gradients underlie functional transitions in monkey pre-supplementary motor area.

The pre-supplementary motor area F6 is involved in a variety of functions in multiple domains, from planning/withholding goal-directed actions in space to rule-based cognitive processes and social interactions. Yet, the neural machinery underlying this functional heterogeneity remains unclear. Here, we measured local population dynamics in different rostro-caudal sites of cytoarchitectonically verified area F6 in two monkeys during spatial, contextual and motor processes, both in individual and social conditions. Then, we correlated multimodal population tuning with local anatomical connectivity revealed by neural tracer injections into the functionally characterized sites. We found stronger tuning for object position relative to the monkey in the rostral portion of area F6 than in its caudal part, which in turn exhibits stronger tuning to self and other's (observed) action. Functional specificities were associated with a rostro-caudal transition in connectivity strength from lateral prefrontal cortex, pregenual anterior cingulate cortex and associative striatum (rostrally), to dorso-ventral premotor areas and the motor putamen (caudally). These findings suggest that the functional heterogeneity of the pre-supplementary area F6 is accounted for by gradual transitions in functional properties grounded on local cortico-cortical and cortico-striatal connectional specificities.

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' 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.

Agent-based representations of objects and actions in the monkey pre-supplementary motor area.

Information about objects around us is essential for planning actions and for predicting those of others. Here, we studied pre-supplementary motor area F6 neurons with a task in which monkeys viewed and grasped (or refrained from grasping) objects, and then observed a human doing the same task. We found "action-related neurons" encoding selectively monkey's own action [self-type (ST)], another agent's action [other-type (OT)], or both [self- and other-type (SOT)]. Interestingly, we found "object-related neurons" exhibiting the same type of selectivity before action onset: Indeed, distinct sets of neurons discharged when visually presented objects were targeted by the monkey's own action (ST), another agent's action (OT), or both (SOT). Notably, object-related neurons appear to signal self and other's intention to grasp and the most likely grip type that will be performed, whereas action-related neurons encode a general goal attainment signal devoid of any specificity for the observed grip type. Time-resolved cross-modal population decoding revealed that F6 neurons first integrate information about object and context to generate an agent-shared signal specifying whether and how the object will be grasped, which progressively turns into a broader agent-based goal attainment signal during action unfolding. Importantly, shared representation of objects critically depends upon their location in the observer's peripersonal space, suggesting an "object-mirroring" mechanism through which observers could accurately predict others' impending action by recruiting the same motor representation they would activate if they were to act upon the same object in the same context.

Comparative Performance of Linear Multielectrode Probes and Single-Tip Electrodes for Intracortical Microstimulation and Single-Neuron Recording in Macaque Monkey.

Intracortical microstimulation (ICMS) is one of the most widely employed techniques for providing causal evidence of the relationship between neuronal activity and specific motor, perceptual, or even cognitive functions. In recent years, several new types of linear multielectrode silicon probes have been developed, allowing researchers to sample neuronal activity at different depths along the same cortical site simultaneously and with high spatial precision. Nevertheless, silicon multielectrode probes have been rarely employed for ICMS studies and, more importantly, it is unknown whether and to what extent they can be used for combined recording and stimulation experiments. Here, we addressed these issues during both acute and chronic conditions. First, we compared the behavioral outcomes of ICMS delivered to the hand region of a monkey's motor cortex with multielectrode silicon probes, commercially available multisite stainless-steel probes and single-tip glass-coated tungsten microelectrodes. The results for all three of the probes were reliable and similar. Furthermore, we tested the impact of long-train ICMS delivered through chronically implanted silicon probes at different time intervals, from 1 to 198 days after ICMS sessions, showing that although the number of recorded neurons decreased over time, in line with previous studies, ICMS did not alter silicon probes' recording capabilities. These findings indicate that in ICMS experiments, the performance of linear multielectrode silicon probes is comparable to that of both single-tip and multielectrode stainless-steel probes, suggesting that the silicon probes can be successfully used for combined recording and stimulation studies in chronic conditions.

Extending the Cortical Grasping Network: Pre-supplementary Motor Neuron Activity During Vision and Grasping of Objects.

Grasping relies on a network of parieto-frontal areas lying on the dorsolateral and dorsomedial parts of the hemispheres. However, the initiation and sequencing of voluntary actions also requires the contribution of mesial premotor regions, particularly the pre-supplementary motor area F6. We recorded 233 F6 neurons from 2 monkeys with chronic linear multishank neural probes during reaching-grasping visuomotor tasks. We showed that F6 neurons play a role in the control of forelimb movements and some of them (26%) exhibit visual and/or motor specificity for the target object. Interestingly, area F6 neurons form 2 functionally distinct populations, showing either visually-triggered or movement-related bursts of activity, in contrast to the sustained visual-to-motor activity displayed by ventral premotor area F5 neurons recorded in the same animals and with the same task during previous studies. These findings suggest that F6 plays a role in object grasping and extend existing models of the cortical grasping network.

Evidence for a functional subdivision of Premotor Ear-Eye Field (Area 8B).

The Supplementary Eye Field (SEF) and the Frontal Eye Field (FEF) have been described as participating in gaze shift control. Recent evidence suggests, however, that other areas of the dorsomedial prefrontal cortex also influence gaze shift. Herein, we have investigated electrically evoked ear- and eye movements from the Premotor Ear-Eye Field, or PEEF (area 8B) of macaque monkeys. We stimulated PEEF during spontaneous condition (outside the task performance) and during the execution of a visual fixation task (VFT). In the first case, we functionally identified two regions within the PEEF: a core and a belt. In the core region, stimulation elicited forward ear movements; regarding the evoked eye movements, in some penetrations, stimulation elicited contraversive fixed-vectors with a mean amplitude of 5.14°; while in other penetrations, we observed prevalently contralateral goal-directed eye movements having end-points that fell within 15° in respect to the primary eye position. On the contrary, in the belt region, stimulation elicited backward ear movements; regarding the eye movements, in some penetrations stimulation elicited prevalently contralateral goal-directed eye movements having end-points that fell within 15° in respect to the primary eye position, while in the lateral edge of the investigated region, stimulation elicited contralateral goal-directed eye movements having end-points that fell beyond 15° in respect to the primary eye position. Stimulation during VFT either did not elicit eye movements or evoked saccades of only a few degrees. Finally, even though no head rotation movements were observed during the stimulation period, we viewed a relationship between the duration of stimulation and the neck forces exerted by the monkey's head. We propose an updated vision of the PEEF composed of two functional regions, core and belt, which may be involved in integrating auditory and visual information important to the programming of gaze orienting movements.

Facial muscle coordination in monkeys during rhythmic facial expressions and ingestive movements.

Evolutionary hypotheses regarding the origins of communication signals generally suggest, particularly for the case of primate orofacial signals, that they derive by ritualization of noncommunicative behaviors, notably including ingestive behaviors such as chewing and nursing. These theories are appealing in part because of the prominent periodicities in both types of behavior. Despite their intuitive appeal, however, there are little or no data with which to evaluate these theories because the coordination of muscles innervated by the facial nucleus has not been carefully compared between communicative and ingestive movements. Such data are especially crucial for reconciling neurophysiological assumptions regarding facial motor control in communication and ingestion. We here address this gap by contrasting the coordination of facial muscles during different types of rhythmic orofacial behavior in macaque monkeys, finding that the perioral muscles innervated by the facial nucleus are rhythmically coordinated during lipsmacks and that this coordination appears distinct from that observed during ingestion.

Neuronal activity reflecting progression of trials in the pre-supplementary motor area of macaque monkey: an expression of neuronal flexibility.

We studied the activity of single neurons in the pre-supplementary motor area (pre-SMA) of macaque monkeys as they performed two visuomotor tasks, called the visual fixation task and the visual fixation-blink task. Both tasks involved a sequence of three visual stimuli, red followed by yellow and green. The tasks differed in that the latter one had a gap within the period of the red stimulus, called a "blink". The tasks were performed in two modes, one of which included movements of both the arm and eye and the other of which involved only eye movements. In the arm-eye mode, the monkeys had to press a bar and fixate the red stimulus that appeared after bar press. To receive a reward, both the bar press and visual fixation had to be maintained until the green stimulus triggered bar release. In the eye mode, bar press and bar release were eliminated from the task. Of the 42 neurons active during the visual fixation task, 15 showed task-related activity in both arm-eye and eye modes, and our analysis focused on these cells. We found that the introduction of the blink in visual fixation-blink task abolished the task-related activity of these cells over the course of 2-4 trials. This finding suggests a role for the pre-SMA in reflecting progression of trials as an updating of motor instruction.