Luciano Simone

The Representation of Tool Use in Humans and Monkeys: Common and Uniquely Human Features

Though other species of primates also use tools, humans appear unique in their capacity to understand the causal relationship between tools and the result of their use. In a comparative fMRI study, we scanned a large cohort of human volunteers and untrained monkeys, as well as two monkeys trained to use tools, while they observed hand actions and actions performed using simple tools. In both species, the observation of an action, regardless of how performed, activated occipitotemporal, intraparietal, and ventral premotor cortex, bilaterally. In humans, the observation of actions done with simple tools yielded an additional, specific activation of a rostral sector of the left inferior parietal lobule (IPL). This latter site was considered human-specific, as it was not observed in monkey IPL for any of the tool videos presented, even after monkeys had become proficient in using a rake or pliers through extensive training. In conclusion, while the observation of a grasping hand activated similar regions in humans and monkeys, an additional specific sector of IPL devoted to tool use has evolved in Homo sapiens, although tool-specific neurons might reside in the monkey grasping regions. These results shed new light on the changes of the hominid brain during evolution.

Default Mode of Brain Function in Monkeys

Human neuroimaging has revealed a specific network of brain regions—the default-mode network (DMN)—that reduces its activity during goal-directed behavior. So far, evidence for a similar network in monkeys is mainly indirect, since, except for one positron emission tomography study, it is all based on functional connectivity analysis rather than activity increases during passive task states. Here, we tested whether a consistent DMN exists in monkeys using its defining property. We performed a meta-analysis of functional magnetic resonance imaging data collected in 10 awake monkeys to reveal areas in which activity consistently decreases when task demands shift from passive tasks to externally oriented processing. We observed task-related spatially specific deactivations across 15 experiments, implying in the monkey a functional equivalent of the human DMN. We revealed by resting-state connectivity that prefrontal and medial parietal regions, including areas 9/46d and 31, respectively, constitute the DMN core, being functionally connected to all other DMN areas. We also detected two distinct subsystems composed of DMN areas with stronger functional connections between each other. These clusters included areas 24/32, 8b, and TPOC and areas 23, v23, and PGm, respectively. Such a pattern of functional connectivity largely fits, but is not completely consistent with anatomical tract tracing data in monkeys. Also, analysis of afferent and efferent connections between DMN areas suggests a multisynaptic network structure. Like humans, monkeys increase activity during passive epochs in heteromodal and limbic association regions, suggesting that they also default to internal modes of processing when not actively interacting with the environment.

Grasping Neurons of Monkey Parietal and Premotor Cortices Encode Action Goals at Distinct Levels of Abstraction during Complex Action Sequences

Natural actions are formed by distinct motor acts, each of which is endowed with its own motor purpose (i.e., grasping), chained together to attain the final action goal. Previous studies have shown that grasping neurons of parietal area PFG and premotor area F5 can code the goal of simple actions in which grasping is embedded. While during simple actions the target is usually visible, directly cueing the final goal, during complex action sequences is often concealed and has to be kept in mind to shape action unfolding. The aim of this study was to assess the relative contribution of sensory-cued or memory-driven information about the final goal to PFG and F5 grasping neurons activity. To this purpose, we trained two monkeys to perform complex action sequences, each including two successive grasping acts, aimed at specific final goals (eating or placing). We recorded 122 PFG and 89 F5 neurons. Forty-seven PFG and 26 F5 neurons displayed action goal selectivity only during the late phase of the action, when sensory information cueing the action goal became available. Reward contingency did not affect neuronal selectivity. Notably, 17 PFG neurons reflected the final goal from the early phase of action unfolding, when only memory-driven information was available. Crucially, when monkeys were prevented from obtaining such information before action onset, neurons lost their early selectivity. Our findings suggest that external sensory cues and individuals motor intention integrate at different level of abstraction within a large anatomo-functional network, encompassing parietal and premotor cortices.

Movement‐related activity during goal‐directed hand actions in the monkey ventrolateral prefrontal cortex

Grasping actions require the integration of two neural processes, one enabling the transformation of object properties into corresponding motor acts, and the other involved in planning and controlling action execution on the basis of contextual information. The first process relies on parieto‐premotor circuits, whereas the second is considered to be a prefrontal function. Up to now, the prefrontal cortex has been mainly investigated with conditional visuomotor tasks requiring a learned association between cues and behavioural output. To clarify the functional role of the prefrontal cortex in grasping actions, we recorded the activity of ventrolateral prefrontal (VLPF) neurons while monkeys (Macaca mulatta) performed tasks requiring reaching–grasping actions in different contextual conditions (in light and darkness, memory‐guided, and in the absence of abstract learned rules). The results showed that the VLPF cortex contains neurons that are active during action execution (movement‐related neurons). Some of them showed grip selectivity, and some also responded to object presentation. Most movement‐related neurons discharged during action execution both with and without visual feedback, and this discharge typically did not change when the action was performed with object mnemonic information and in the absence of abstract rules. The findings of this study indicate that a population of VLPF neurons play a role in controlling goal‐directed grasping actions in several contexts. This control is probably exerted within a wider network, involving parietal and premotor regions, where the role of VLPF movement‐related neurons would be that of activating, on the basis of contextual information, the representation of the motor goal of the intended action (taking possession of an object) during action planning and execution.

Action observation activates neurons of the monkey ventrolateral prefrontal cortex

Prefrontal cortex is crucial for exploiting contextual information for the planning and guidance of behavioral responses. Among contextual cues, those provided by others’ behavior are particularly important, in primates, for selecting appropriate reactions and suppressing the inappropriate ones. These latter functions deeply rely on the ability to understand others’ actions. However, it is largely unknown whether prefrontal neurons are activated by action observation. To address this issue, we recorded the activity of ventrolateral prefrontal (VLPF) neurons of macaque monkeys during the observation of videos depicting biological movements performed by a monkey or a human agent, and object motion. Our results show that a population of VLPF neurons respond to the observation of biological movements, in particular those representing goal directed actions. Many of these neurons also show a preference for the agent performing the action. The neural response is present also when part of the observed movement is obscured, suggesting that these VLPF neurons code a high order representation of the observed action rather than a simple visual description of it.

The Mirror System in Monkeys and Humans and its Possible Motor-Based Functions

Mirror neurons are neurons, found in both ventral premotor and inferior parietal cortex of the monkey, that respond during both observation and execution of motor acts. This property suggested that the mirror neuron system underpins the understanding of goal-related motor acts. The existence of a mirror system has also been demonstrated in humans. The research of the last 10 years has been crucial for specifying in more details the properties of mirror neurons in monkeys. For instance, it has been recently shown that the response to an observed motor act can be modulated by the space sector in which the act is performed, and that part of mirror neurons can be modulated by the perspective from which the motor act is observed. In humans, evidence accumulated in favor of an involvement of the mirror matching mechanism in several types of social functions, such as imitation, intention and emotion understanding and speech comprehension. In this article we will first describe the main properties of mirror neurons in monkeys and some of the studies demonstrating the presence of an action observation or execution matching system in humans and also discuss possible criticisms to the presence of mirror neurons in our species. Then we will be present the evidence on the role of the mirror system in intention understanding and imitation. Finally, we discuss the role of the mirror system in language evolution and, starting from the recent evidence of the presence of mirror neurons in songbirds, we suggest that the mirror matching system of primates could derive from an ancestor common to primates and birds.

Cortical and subcortical connections of parietal and premotor nodes of the monkey hand mirror neuron network

Mirror neurons (MNs) are a class of cells originally discovered in the monkey ventral premotor cortex (PMv) and inferior parietal lobule (IPL). They discharge during both action execution and action observation and appear to play a crucial role in understanding others’ actions. It has been proposed that the mirror mechanism is based on a match between the visual description of actions, encoded in temporal cortical regions, and their motor representation, provided by PMv and IPL. However, neurons responding to action observation have been recently found in other cortical regions, suggesting that the mirror mechanism relies on a wider network. Here we provide the first description of this network by injecting neural tracers into physiologically identified IPL and PMv sectors containing hand MNs. Our results show that these sectors are reciprocally connected, in line with the current view, but IPL MN sectors showed virtually no direct connection with temporal visual areas. In addition, we found that PMv and IPL MN sectors share connections with several cortical regions, including the dorsal and mesial premotor cortex, the primary motor cortex, the secondary somatosensory cortex, the mid-dorsal insula and the ventrolateral prefrontal cortex, as well as subcortical structures, such as motor and polysensory thalamic nuclei and the mid-dorsal claustrum. We propose that each of these regions constitutes a node of an “extended network”, through which information relative to ongoing movements, social context, environmental contingencies, abstract rules, and internal states can influence MN activity and contribute to several socio-cognitive functions.