We have discovered mirror neurons in the frontal and premotor cortex of macaques that fire both when a monkey performs an action and when it observes the same action performed by another monkey or a human. This feature of monkey neuron activation has been shown to provide a key to the neural basis of imitation learning and empathy in humans.
Observation of others’ actions
The observation of others’ actions is one of the most fundamental aspects of social behavior. This is because it allows us to understand the internal states that drive others’ behaviors and therefore to gain a better understanding of ourselves. It is also possible to use this information for predicting the actions of other people in future situations.
To examine the neural mechanisms of action observation, we conducted a series of experiments using fMRI. In the first experiment, we tested monkeys while they observed an experimenter perform (Action condition) or withhold a grasping action.
We recorded from mirror neurons in the ventral premotor area F5 that encoded grasping actions. When monkeys saw an action, these neurons responded in a similar manner to when they performed the same action themselves (Figure 1A).
In the second experiment, we tested the hypothesis that this activation could be due to simulation of the processes that would occur in another person. Observing another person successfully inhibit an action or make an error evokes a number of inhibitory processes in the observer’s brain that would not occur when this act is produced by the observer.
When the monkey observed an action being performed in the extrapersonal space, MN population activity was activated, on average, 340 ms before the go signal. This activation occurred earlier than when the monkey observed an action being performed in the peripersonal space (Figure 2A).
The predictive activity of these neurons is in accordance with their discharge pattern, which can be classified into either reactive or predictive forms. The predictive type is the most common form, and accounts for 70% of the total number of activated MNs.
However, the reactive type is a more rare type of activation and is found only in about 30% of the activated MNs. These cells are called “strictly congruent” neurons, because they exhibit a matching discharge pattern between visual and motor representations of the same action.
Moreover, in addition to predictive and reactive coding of others’ actions, MNs can also be activated when an action is withheld by the experimenter. This activation is in contrast to the activation of other neural circuits involved in visuomotor processing, which can only be activated when an action is performed.
Grasping is an important part of human interaction. It allows us to grasp objects and move them in a variety of ways. It is also a key skill in social communication. For example, when someone hands you a cup of coffee, it is important for you to have it in your hand before you let go of it. Similarly, when someone gives you a piece of fruit, it is important for you to have the fruit in your mouth before you bite it.
Several studies have reported the involvement of neurons in the motor cortex during observation of goal-directed hand actions, such as grasping, manipulating, and breaking. However, very few studies investigated the activation of these neurons during observation of different body parts such as mouth or foot movements.
In monkeys, the main areas activated during the observation of reaching and grasping activities are located in dorsal premotor cortical areas (SPL, PMd, and IPS). The classic distinction between reaching and grasping is evident, as reaching movements are typically processed within a dorso-dorsal circuit, while grasping activities mainly activate a ventral-most circuit (anterior IPS and PMv).
While the majority of studies on the MNS during reaching observed activations of the lateral limb area (PMv), few studies have also focused on the parietal and premotor MNS during reaching. In these studies, activations of the parietal areas BA45 and IPS were more symmetrically distributed than those of the premotor areas (PMv, PMd).
These findings support the hypothesis that mirror neurons play a role in the understanding of other people’s actions by discharging when subjects perform a similar motor act. In humans, mirror neurons are found in a number of brain regions, including the premotor and parietal cortical areas.
They code the motor action performed and its context, as well as predicting how the motor act will end. These predictions are reflected in the motor-evoked potentials (MEPs) of the muscle fibers.
The most common type of video stimulus that produced the strongest response was a first person or third person view of a monkey grasping an object. More rarely, responses to objects that were moving during the grasping act were recorded.
During food consumption, the sight and taste of food activate noradrenergic neurons in the lateral hypothalamus and substantia innominata. They are robustly stimulated during food consumption, but they are attenuated by satiety (4-6).
The role of these brain-stimulation reward neurons in feeding is unclear, but their activation during food consumption has been reported to be correlated with food intake (7-9), suggesting that they can play a direct role in feeding behavior. Moreover, AgRP neurons are also involved in appetitive behaviors that lead to food obtainment, such as lever pressing (Atasoy et al., 2012; Krashes et al., 2011).
However, it is unknown whether these appetitive behaviors are a driving force behind the motivation to consume food or if they are simply part of the animal’s natural feeding dynamics. We examined this question by using optogenetic stimulation of LC-NE neurons to suppress feeding in hungry mice (LCChrimsonR).
Brief photostimulation of LC-NE neurons triggered a reduction in food intake in hungry LCChrimsonR mice, which was statistically significant and not observed in control mice. Stimulating LC-NE neurons for short periods also reduces feeding in aversive conditions. This effect likely is mediated by reduced attention and distraction that redirects the focus of the monkey’s behavior away from food.
In contrast, chemogenetic activation of AgRP neurons induced voracious eating, but it required prolonged prestimulation in order to maintain this response. The duration of prestimation was a strong predictor of subsequent food intake, with first order association kinetics (Figure 1E; R2 = 0.96).
We found that the number of neurons responding during a video depicting a hand grasping action in a human agent masked by black shading differed across different video epochs. In the basic condition, most HS neurons discharged during both epochs, but when they were obscured, their responses diminished. This suggests that they code either specific aspects of the observed action, such as the hand-object interaction, or the context (e.g., the target/context and beginning of forelimb movement) that give enough information to predict the outcome of the action (see Figs. 2 and 3).
The researchers found that when marmosets observed social interactions, they activated a network of areas in the brain known to be involved in processing social information. These areas include the dorsomedial prefrontal cortex (dmPFC; Brodmann’s area 24), visual, temporal, and parietal cortex.
To test this hypothesis, they scanned the monkeys’ brains as they ate and then recorded their brain activity while the animals performed a task. This task required the monkeys to offer an apple slice to another monkey.
They used fMRI to track the activity of individual neurons as they were scanned. Activation of these neurons was significantly higher when the monkeys were offering an apple slice to one of their group members than when they were offering an apple slice to a stranger.
This study is the first to show that a brain network activates when marmosets observe other people’s actions. This network is similar to the regions previously shown to be involved in processing social information in humans and macaques.
These regions are important for social interaction because they enable people to track the actions of others and predict what those other people will do in the future. They also allow people to see how others are feeling and understand what they want from those other people.
Moreover, these brain regions encode other people’s peripersonal space. This is because the mirror neurons can match the peripersonal space of a person to their own peripersonal space.
It is thought that the mirror neuron system allows the monkey to process others’ actions by integrating different contextual aspects. These include spatial cues, gaze direction and kinematic parameters.
In addition, the mirror neurons may help the monkeys understand their own peripersonal space by providing other brain regions with a metric representation of it. In this way, the peripersonal space becomes a part of the extrapersonal space and is able to be accessed by the monkey. This might make it easier for the monkeys to cooperate with other people in a joint action.