From motor to sensory processing in mirror neuron computational modelling

Mirror neurons within a monkey's premotor area F5 fire not only when the monkey performs a certain class of actions but also when the monkey observes another monkey (or the experimenter) perform a similar action. It has thus been argued that these neurons are crucial for understanding of actions by others. We offer the hand-state hypothesis as a new explanation of the evolution of this capability: the basic functionality of the F5 mirror system is to elaborate the appropriate feedback - what we call the hand state - for opposition-space based control of manual grasping of an object. Given this functionality, the social role of the F5 mirror system in understanding the actions of others may be seen as an exaptation gained by generalizing from one's own hand to an other's hand. In other words, mirror neurons first evolved to augment the "canonical" F5 neurons (active during self-movement based on observation of an object) by providing visual feedback on "hand state," relating the shape of the hand to the shape of the object. We then introduce the MNS1 (mirror neuron system 1) model of F5 and related brain regions. The existing Fagg-Arbib-Rizzolatti-Sakata model represents circuitry for visually guided grasping of objects, linking the anterior intraparietal area (AIP) with F5 canonical neurons. The MNS1 model extends the AIP visual pathway by also modeling pathways, directed toward F5 mirror neurons, which match arm-hand trajectories to the affordances and location of a potential target object. We present the basic schemas for the MNS1 model, then aggregate them into three "grand schemas" - visual analysis of hand state, reach and grasp, and the core mirror circuit - for each of which we present a useful implementation (a non-neural visual processing system, a multijoint 3-D kinematics simulator, and a learning neural network, respectively). With this implementation we show how the mirror system may learn to recognize actions already in the repertoire of the F5 canonical neurons. We show that the connectivity pattern of mirror neuron circuitry can be established through training, and that the resultant network can exhibit a range of novel, physiologically interesting behaviors during the process of action recognition. We train the system on the basis of final grasp but then observe the whole time course of mirror neuron activity, yielding predictions for neurophysiological experiments under conditions of spatial perturbation, altered kinematics, and ambiguous grasp execution which highlight the importance of the timing of mirror neuron activity.

A human-machine collaboration method based on real time action recognition is presented to achieve the collaboration between automated guided vehicles (AGVs) and human operators through the perception of tasks conducted by human operators. The process of action recognition is accomplished by a Kinect vision sensor and convolutional neural networks (CNN), and the methods of multiple features fusion and hierarchical cluster are applied in the process of action recognition. The utilization of action recognition technology can effectively shorten the expected waiting time, and can avoid the assembly line stagnation caused by human errors to a great extent. Finally, the experiment result indicates that the overall efficiency has been increased significantly after applying the method.

Traditionally the mirror neuron system (MNS) only includes premotor and posterior parietal cortices. However, somatosensory cortices, BA1/2 in particular, are also activated during action execution and observation. Here, we examine whether BA1/2 and the parietofrontal MNS integrate information by using functional magnetic resonance imaging (fMRI)-guided continuous theta-burst stimulation (cTBS) to perturb BA1/2. Measuring brain activity using fMRI while participants are under the influence of cTBS shows local cTBS effects in BA1/2 varied, with some participants showing decreases and others increases in the BOLD response to viewing actions vs control stimuli. We show how measuring cTBS effects using fMRI can harness this variance using a whole-brain regression. This analysis identifies brain regions exchanging action-specific information with BA1/2 by mapping voxels away from the coil with cTBS-induced, action-observation-specific BOLD contrast changes that mirror those under the coil. This reveals BA1/2 exchanges action-specific information with premotor, posterior parietal and temporal nodes of the MNS during action observation. Although anatomical connections between BA1/2 and these regions are well known, this is the first demonstration that these connections carry action-specific signals during observation and hence, that BA1/2 plays a causal role in the human MNS.

Movement observation (MO) modulates activity of brain regions involved in motor control. It is mentioned that this phenomenon is evoked by the mirror neurons system activity and reflects processes of action understanding, action recognition and covert imitation of observed movements. Desynchronization of sensorimotor EEG oscillations and increase in corticospinal excitability assessed by transcranial magnetic stimulation (TMS) are invasive markers of motor and somatosensory cortices activation. Despite the fact that numerous studies show sensitivity of these markers to movements observation, little is known about the dynamics of the EEG activity and corticospinal excitability during evaluating the anatomically correctness of observed actions. We designed a TMS-EEG experiment with passive observation of simple aimless movements, in which subjects observed natural and unnatural flexions of fingers. Spatially separated sensorimotor EEG oscillations and TMS evoked myographic potentials were studied. The results revealed sensitivity of mu/beta oscillations to the anatomical correctness of movement. No correlations between mu/beta desynchronization and motor evoked potentials (MEPs) were found, but a weak link between beta synchronization and MEPs was shown. It might be proposed that ERD reflects activity of rather somatosensory but not motor cortex. Our findings demonstrate that activity of the sensorimotor cortex is modulated by action observation and action recognition, whereas EEG activity from different frequency ranges is modulated in different ways. Importantly, no significant changes in MEPs amplitude during MO was found. This result is discussed with regard to the impact of experimental instructions and participant's mental state during the MO task.

Since their discovery, mirror neurons--units in the macaque brain that discharge both during action observation and execution--have attracted considerable interest. Whether mirror neurons are an innate endowment or acquire their sensorimotor matching properties ontogenetically has been the subject of intense debate. It is widely believed that these units are an innate trait; that we are born with a set of mature mirror neurons because their matching properties conveyed upon our ancestors an evolutionary advantage. However, an alternative view is that mirror neurons acquire their matching properties during ontogeny, through correlated experience of observing and performing actions. The present article re-examines frequently overlooked neurophysiological reports of 'tool-use' and 'audiovisual' mirror neurons within the context of this debate. It is argued that these findings represent compelling evidence that mirror neurons are a product of sensorimotor experience, and not an innate endowment.

The observation of actions performed by another person activates parts of the brain as if the observer were performing that action, referred to as the ‘mirror system’. Very little is currently known about the developmental trajectory of the mirror system and related social cognitive processes. This experimental study sought to explore the modulation of the sensorimotor mu rhythm during action observation using EEG measures, and how these may relate to social cognitive abilities across the lifespan, from late childhood through to old age. Three-hundred and one participants aged 10- to 86-years-old completed an action observation EEG task and three additional explicit measures of social cognition. As predicted, findings show enhanced sensorimotor alpha and beta desynchronization during hand action observation as compared to static hand observation. Overall, our findings indicate that the reactivity of the sensorimotor mu rhythm to the observation of others’ actions increases throughout the lifespan, independently from social cognitive processes.

Mirror neurons and imitation: A computationally guided review

Background: Parkinson's disease (PD) is a neurodegenerative disorder characterized by motor symptoms such as tremors, rigidity, and bradykinesia. Rehabilitation utilizing mirror neurons leverages the brain's capacity for action observation (AO) and motor imagery (MI) to enhance motor function. This approach involves patients imitating movements observed in therapists or videos, aiming to improve gait, coordination, and overall quality of life. Mirror neuron activation facilitates motor learning and may decelerate disease progression, thus enhancing patient mobility and independence. Methods: This scoping review aimed to map current evidence on PD therapies employing mirror neuron-based rehabilitation. Databases searched included PubMed, PEDro, and Cochrane. The review included randomized controlled trials (RCTs) and systematic reviews that examined the effects of AO and MI in PD rehabilitation. Results: Five studies met the inclusion criteria, encompassing various rehabilitation techniques focusing on AO and MI. These studies consistently demonstrated positive outcomes, such as reduced disease severity and improved quality of life, gait, and balance in PD patients. The activation of mirror neurons through AO and MI was shown to facilitate motor learning and contribute to improved functional mobility. Conclusions: Although the included studies support the beneficial impact of AO and MI techniques in PD rehabilitation, numerous questions remain unresolved. Further research is necessary to evaluate the potential integration of these techniques into standard physiotherapy routines for PD patients. This review highlights the promise of AO and MI in enhancing motor rehabilitation for PD, suggesting the need for more comprehensive studies to validate and refine these therapeutic approaches.

BackgroundExisting rehabilitation techniques are not satisfactory in improving motor function after stroke, resulting in heavy social burdens. With discovery of mirror neuron system (MNS), action observation (AO) has become a promising strategy to promote motor learning in rehabilitation. Based on MNS theory and virtual reality (VR) technology, we designed an innovative rehabilitative approach: synchronous 360° VR video AO (VRAO) and neuromuscular electrical stimulation (NMES). We hypothesized that VRAO+NMES could enhance MNS activation, thus to improve upper limb motor function and activities of daily living in stroke survivors.MethodsTo explore the efficacy and mechanism of VRAO+NMES, we designed this single center, evaluator blinded, prospective, two arm parallel group randomized controlled trial with 1:1 allocation ratio. The experiment group will receive VRAO+NMES, while the control group will receive VR landscape observation combined with NMES. The Fugl-Meyer Assessment for Upper Extremity is the primary outcome of this study, Brunstrom Recovery Stages for Upper Extremity, Manual Muscle Test, Range of Motion, Modified Barthel Index, and Functional Independence Measure are the secondary outcomes. In addition, functional near-infrared spectroscopy (fNIRS) and surface electromyography (sEMG) will be used to evaluate the activation of MNS brain regions and related muscles, respectively.DiscussionApplying VR in AO therapy (AOT) has become popular, another study direction to improve AOT is to combine it with peripheral stimulations simultaneously. Due to its full immersive characteristic and multi-sensory input, 360° videos based VRAO+NMES could improve the motivation and engagement level of participants. In addition, fNIRS and sEMG test results may act as good biomarkers to predict rehabilitation outcomes, helping select suitable candidates for this new intervention.ConclusionThe results of this study will provide evidence for the feasibility and potential clinical efficacy of VRAO+NMES in stroke rehabilitation, thus to promote the clinical applicability and generalize its use in hospital, community, and home rehabilitation settings.Clinical trial registrationhttps://www.chictr.org.cn/showproj.html?proj=178276, Identifier [ChiCTR2200063552].

To probe the presence of mirror neurons in the human brain, cross-modal fMRI adaptation has been suggested as a suitable technique. The rationale behind this suggestion is that this technique allows making more accurate inferences about neural response properties underlying fMRI voxel activations, beyond merely showing shared voxels that are active during both action observation and execution. However, the validity of using cross-modal fMRI adaptation to demonstrate the presence of mirror neurons in parietal and premotor brain regions has been questioned given the inconsistent and weak results obtained in human studies. A better understanding of cross-modal fMRI adaptation effects in the macaque brain is required as the rationale for using this approach is based on several assumptions related to macaque mirror neuron response properties that still need validation. Here, we conducted a cross-modal fMRI adaptation study in macaque monkeys, using the same action execution and action observation tasks that successfully yielded mirror neuron region cross-modal action decoding in a previous monkey MVPA study. We scanned two male rhesus monkeys while they first executed a sequence of either reach-and-grasp or reach-and-touch hand actions and then observed a video of a human actor performing these motor acts. Both whole-brain and region-of-interest analyses failed to demonstrate cross-modal fMRI adaptation effects in parietal and premotor mirror neuron regions. Our results, in line with previous findings in non-human primates, show that cross-modal motor-to-visual fMRI adaptation is not easily detected in monkey brain regions known to house mirror neurons. Thus, our results advocate caution in using cross-modal fMRI adaptation as a method to infer whether mirror neurons can be found in the primate brain.

In robotics, objects and body parts can be represented in various coordinate frames to ease computation. In biological systems, body or body part centered coordinate frames have been proposed as possible reference frames that the brain uses for interacting with the environment. Coordinate transformations are standard tools in robotics and can facilitate perspective invariant action recognition and action prediction based on observed actions of other agents. Although it is known that human adults can do explicit coordinate transformations, it is not clear whether this capability is used for recognizing and understanding the actions of others. Mirror neurons, found in the ventral premotor cortex of macaque monkeys, seem to undertake action understanding in a perspective invariant way, which may rely on lower level perceptual mechanisms. To this end, in this paper we propose a novel reference frame that is ecologically plausible and can sustain basic action understanding and mirror function. We demonstrate the potential of this representation by simulation of an upper body humanoid robot with an action repertoire consisting of push, poke, move-away and bring-to-mouth actions. The simulation experiments indicate that the representation is suitable for action recognition and effect prediction in a perspective invariant way, and thus can be deployed as an artificial mirror system for robotic applications.

Neural circuits involved in imitation and perspective-taking

Neurons in macaque ventral premotor cortex and inferior parietal lobe discharge during both the observation and the execution of motor acts. It has been claimed that these so-called mirror neurons form the basis of action understanding by matching the visual input with the corresponding motor program (direct matching). Functional magnetic resonance imaging (fMRI) adaptation can be used to test the direct matching account of action recognition by determining whether putative mirror neurons show adaptation for repeated motor acts independently of whether they are observed or executed. An unambiguous test of the hypothesis requires that the motor acts be meaningless to ensure that any adaptation effect is directly because of movement recognition/motor execution and not contextually determined inferences. We found adaptation for motor acts that were repeatedly observed or repeatedly executed. We also found adaptation for motor acts that were first observed and then executed, as would be expected if a previously seen act primed the subsequent execution of that act. Crucially, we found no signs of adaptation for motor acts that were first executed and then observed. Failure to find cross-modal adaptation for executed and observed motor acts is not compatible with the core assumption of mirror neuron theory, which holds that action recognition and understanding are based on motor simulation.

The inferior frontal gyrus (IFG) is active during both goal-directed action and while observing the same motor act, leading to the idea that also the meaning of a motor act (action understanding) is represented in this "mirror neuron system" (MNS). However, in the dual-loop model, based on dorsal and ventral visual streams, the MNS is thought to be a function of the dorsal steam, projecting to pars opercularis (BA44) of IFG, while recent studies suggest that conceptual meaning and semantic analysis are a function of ventral connections, projecting mainly to pars triangularis (BA45) of IFG. To resolve this discrepancy, we investigated action observation (AO) and imitation (IMI) using fMRI in a large group of subjects. A grasping task (GR) assessed the contribution from movement without AO. We analyzed connections of the MNS-related areas within IFG with postrolandic areas with the use of activation-based DTI. We found that action observation with imitation are mainly a function of the dorsal stream centered on dorsal part of BA44, but also involve BA45, which is dorsally and ventrally connected to the same postrolandic regions. The current finding suggests that BA45 is the crucial part where the MNS and the dual-loop system interact.

Autism Spectrum Disorder: Seeing Is Not Understanding