Attention and cognitive load modulate motor resonance during action observation.

Observation of others' actions evokes a motor resonant (MR) response, in the parieto-frontal Action Observation Network (AON, comprising BA40, BA6, BA4). In order to investigate the effect of cognitive processes on the AON we manipulated attention and cognitive load during central and peripheral observation of hand grasping actions with three experiments. Motor Evoked Potentials (MEPs) were elicited in the opponent of the thumb (OP) and abductor of the little finger (ADM) by Transcranial Magnetic Stimulation (TMS) of the primary motor cortex. First, we investigated the role of selective attention by asking subjects to focus their attention on the thumb of the moving hand in central vision. A selective facilitation of OP MEPs was recorded, without the expected ADM MEPs modulation. Second, a "covert attention" paradigm was used to investigate the role of attention in peripheral vision. Surprisingly, MEP modulation was virtually abolished. In the third experiment we tested the hypothesis that the higher cognitive load introduced by the covert attention instruction had interfered with MR. We allowed subjects to view the action before its peripheral presentation with covert attention, thereby decreasing the cognitive effort necessary to decode the grasping action. The accuracy of motor resonant response was restored.

Broca's Area as a Pre-articulatory Phonetic Encoder: Gating the Motor Program.

The exact nature of the role of Broca's area in control of speech and whether it is exerted at the cognitive or at the motor level is still debated. Intraoperative evidence of a lack of motor responses to direct electrical stimulation (DES) of Broca's area and the observation that its stimulation induces a "speech arrest" without an apparent effect on the ongoing activity of phono-articulatory muscles, raises the argument. Essentially, attribution of direct involvement of Broca's area in motor control of speech, requires evidence of a functional connection of this area with the phono-articulatory muscles' motoneurons. With a quantitative approach we investigated, in 20 patients undergoing surgery for brain tumors, whether DES delivered on Broca's area affects the recruitment of the phono-articulatory muscles' motor units. The electromyography (EMG) of the muscles active during two speech tasks (object picture naming and counting) was recorded during and in absence of DES on Broca's area. Offline, the EMG of each muscle was analyzed in frequency (power spectrum, PS) and time domain (root mean square, RMS) and the two conditions compared. Results show that DES on Broca's area induces an intensity-dependent "speech arrest." The intensity of DES needed to induce "speech arrest" when applied on Broca's area was higher when compared to the intensity effective on the neighboring pre-motor/motor cortices. Notably, PS and RMS measured on the EMG recorded during "speech arrest" were superimposable to those recorded at baseline. Partial interruptions of speech were not observed. Speech arrest was an "all-or-none" effect: muscle activation started only by removing DES, as if DES prevented speech onset. The same effect was observed when stimulating directly the subcortical fibers running below Broca's area. Intraoperative data point to Broca's area as a functional gate authorizing the phonetic translation to be executed by the motor areas. Given the absence of a direct effect on motor units recruitment, a direct control of Broca's area on the phono-articulatory apparatus seems unlikely. Moreover, the strict correlation between DES-intensity and speech prevention, might attribute this effect to the inactivation of the subcortical fibers rather than to Broca's cortical neurons.

The role of attention in human motor resonance.

Observation of others' actions evokes in primary motor cortex and spinal circuits of observers a subliminal motor resonance response, which reflects the motor program encoding observed actions. We investigated the role of attention in human motor resonance with four experimental conditions, explored in different subject groups: in the first explicit condition, subjects were asked to observe a rhythmic hand flexion-extension movement performed live in front of them. In two other conditions subjects had to monitor the activity of a LED light mounted on the oscillating hand. The hand was clearly visible but it was not the focus of subjects' attention: in the semi-implicit condition hand movement was relevant to task completion, while in the implicit condition it was irrelevant. In a fourth, baseline, condition subjects observed the rhythmic oscillation of a metal platform. Motor resonance was measured with the H-reflex technique as the excitability modulation of cortico-spinal motorneurons driving a hand flexor muscle. As expected, a normal resonant response developed in the explicit condition, and no resonant response in the baseline condition. Resonant responses also developed in both semi-implicit and implicit conditions and, surprisingly, were not different from each other, indicating that viewing an action is, per se, a powerful stimulus for the action observation network, even when it is not the primary focus of subjects' attention and even when irrelevant to the task. However, the amplitude of these responses was much reduced compared to the explicit condition, and the phase-lock between the time courses of observed movement and resonant motor program was lost. In conclusion, different parameters of the response were differently affected by subtraction of attentional resources with respect to the explicit condition: time course and muscle selection were preserved while the activation of motor circuits resulted in much reduced amplitude and lost its kinematic specificity.

Decreased motor cortex excitability mirrors own hand disembodiment during the rubber hand illusion.

During the rubber hand illusion (RHI), subjects experience an artificial hand as part of their own body, while the real hand is subject to a sort of 'disembodiment'. Can this altered belief about the body also affect physiological mechanisms involved in body-ownership, such as motor control? Here we ask whether the excitability of the motor pathways to the real (disembodied) hand are affected by the illusion. Our results show that the amplitude of the motor-evoked potentials recorded from the real hand is significantly reduced, with respect to baseline, when subjects in the synchronous (but not in the asynchronous) condition experience the fake hand as their own. This finding contributes to the theoretical understanding of the relationship between body-ownership and motor system, and provides the first physiological evidence that a significant drop in motor excitability in M1 hand circuits accompanies the disembodiment of the real hand during the RHI experience.

What you see is what you get: motor resonance in peripheral vision.

Observation of others' actions evokes a subliminal motor resonant response, which reflects the motor program encoding observed actions. The possibility that actions located in the peripheral field of vision may also activate motor resonant responses has not been investigated. We examine the excitability modulation of motor pathways in response to grasping actions viewed in near peripheral vision; results are directly compared to responses to the same actions viewed in central vision (Borroni et al. in Eur J Neurosci 34:662-669, 2011. doi: 10.1111/j.1460-9568.2011.07779.x ). We hypothesize that actions observed in peripheral vision are effective in modulating the excitability of motor pathways, but that responses have a low kinematic specificity. While the neural resources of central vision provide the most accurate perception of biological motion, the decreased visual acuity in periphery may be sufficient to discriminate only general aspects of movement and perhaps to recognize the gist of visual scenes. Right-handed subjects observed a video of two grasping actions at 10° eccentricity in the horizontal plane. Motor-evoked potentials were elicited in the right OP and ADM muscles by TMS of the left primary motor cortex at different delays during the observed actions. Results show that actions viewed in near peripheral vision are effective in modulating the subliminal activation of motor circuits, but that responses are rough and inaccurate, and do not reflect the motor program encoding the observed action or its goal. We suggest that due to their limited kinematic accuracy, these subliminal motor responses may provide information about the general aspects of observed actions, rather than their specific execution.

The mirror neuron system and the strange case of Broca's area.

Mirror neurons, originally described in the monkey premotor area F5, are embedded in a frontoparietal network for action execution and observation. A similar Mirror Neuron System (MNS) exists in humans, including precentral gyrus, inferior parietal lobule, and superior temporal sulcus. Controversial is the inclusion of Broca's area, as homologous to F5, a relevant issue in light of the mirror hypothesis of language evolution, which postulates a key role of Broca's area in action/speech perception/production. We assess "mirror" properties of this area by combining neuroimaging and intraoperative neurophysiological techniques. Our results show that Broca's area is minimally involved in action observation and has no motor output on hand or phonoarticulatory muscles, challenging its inclusion in the MNS. The presence of these functions in premotor BA6 makes this area the likely homologue of F5 suggesting that the MNS may be involved in the representation of articulatory rather than semantic components of speech.

Mirroring avatars: dissociation of action and intention in human motor resonance.

Observation of others' actions induces a subliminal activation of motor pathways (motor resonance) that is mediated by the mirror neuron system and reflects the motor program encoding the observed action. Whether motor resonance represents the movements composing an action or also its motor intention remains of debate, as natural actions implicitly contain their motor intentions. Here, action and intention are dissociated using a natural and an impossible action with the same grasping intention: subjects observe an avatar grasping a ball using either a natural hand action ('palmar' finger flexion) or an impossible hand action ('dorsal' finger flexion). Motor-evoked potentials (MEPs), elicited by single transcranial magnetic stimulation of the hand area in the primary motor cortex, were used to measure the excitability modulation of motor pathways during observation of the two different hand actions. MEPs were recorded from the opponens pollicis (OP), abductor digiti minimi (ADM) and extensor carpi radialis (ECR) muscles. A significant MEP facilitation was found in the OP, during observation of the grasping phase of the natural action; MEPs in the ADM were facilitated during observation of the hand opening phase of the natural action and of both opening and grasping phases of the impossible action. MEPs in the ECR were not affected. As different resonant responses are elicited by the observation of the two different actions, despite their identical intention, we conclude that the mirror neuron system cannot utilize the observer's subliminal motor program in the primary motor cortex to encode action intentions.

The shape of motor resonance: right- or left-handed?

The human mirror neuron system is a fronto-parietal neural pathway which, when activated by action observation, gives rise to an internal simulation of the observed action (motor resonance). Here we demonstrate how handedness shapes the resonant response, by engaging right-handed (RH) and left-handed (LH) subjects in observation and execution of actions preferentially performed by the dominant hand. We hypothesize that since motor resonance reproduces subliminally the specific motor program for the observed action, it should be subject to motor constraints, such as handedness. A conjunction analysis for observed and executed actions revealed that handedness determines a lateralized activation of the areas engaged in motor resonance. Premotor-BA6 and parietal-BA40 are strongly left lateralized in RH subjects observing or moving their right hand, and to a lesser degree their left hand. Extremely LH subjects show a similar pattern of lateralization on the right, while more ambidextrous LH subjects show a more bilateral activation. The activation of a cortical network outside the mirror neuron system is also discussed.

Activation of motor pathways during observation and execution of hand movements.

Some neural properties of "motor resonance"--the subliminal activation of the motor system when observing actions performed by others--are investigated in humans. Two actions performed with the right hand are observed by experimental subjects: a finalized (transitive) action (reaching for and grasping a ball) and an intransitive action (cyclic up-and-down oscillation of the hand), while the H-reflex and Transcranial Magnetic Stimulation techniques are utilized to test the excitability of the observer's motor pathways to hand and forearm muscles (first dorsal interosseus, flexor digitorum superficialis, flexor carpi radialis). Results indicate that motor resonance: (1) is mainly mediated by the primary motor cortex; (2) involves the same forearm muscles as used in the execution of the observed movement; (3) is also recorded in the homologous muscles of the arm contralateral to the one observed; and (4) is evoked by both transitive and intransitive movements of the human hand, but not by similar movements of inanimate objects. The similarities and discrepancies between the resonant response in humans and the properties of monkey "mirror neurons" are discussed.

Bilateral motor resonance evoked by observation of a one-hand movement: role of the primary motor cortex.

In humans, observation of movement performed by others evokes a subliminal motor resonant response, probably mediated by the mirror neurone system, which reproduces the motor commands needed to execute the observed movement with good spatial and temporal fidelity. Motor properties of the resonant response were here investigated with the ultimate goal of understanding the principles operating in the transformation from observation to internal reproduction of movement. Motor resonance was measured as the modulation of excitability of spinal motoneurones, evoked by the observation of a cyclic flexion-extension of one hand. The first two experiments showed that the observation of a one-hand movement always evoked a bimanual resonant response independent of which hand was observed and that these bilateral responses were consistently phase-linked. H-reflexes simultaneously recorded in right and left flexor carpi radialis muscles were always modulated 'in-phase' with each other. The goal of the third experiment was to define the role of primary motor cortex in the bilateral resonant response. Bilateral H-reflexes were recorded during a temporary inactivation induced by transcranial magnetic stimulation over the left cortical hand motor area of observers. The finding that such cortical depression abolished the H-reflex modulation of only the right flexor carpi radialis motoneurones, leaving it unchanged on the left side, suggested that both primary motor areas were activated by the premotor cortex and transmit the resonant activation through crossed corticospinal pathways. The data provide further evidence that the subliminal activation of motor pathways induced by movement observation is organized according to general rules shared with the control of voluntary movement.

Cyclic time course of motor excitability modulation during the observation of a cyclic hand movement.

The observation of a sinusoidal flexion-extension of the wrist was utilized to determine the continuous time course and phase relation between observed movement and its effects on the observer's motor pathways. While observing movements performed by others, the observers' cortical motor areas and spinal circuits were activated, reflecting the specific temporal and muscular pattern of the actual movement (motor resonance). H-reflexes and motor-evoked potentials (MEPs) were elicited, respectively, by electrical stimulation of the median nerve and magnetic stimulation of the appropriate cortical area, in the right forearm muscle Flexor Carpi Radialis (FCR) of subjects who were observing a 1-Hz cyclic oscillation of the right prone hand executed by a different person. Observation elicited a parallel cyclic excitability modulation of the observer's H-reflex and MEP responses with identical period as the observed movement. Modulation was phase advanced, as is muscle activation with respect to the real movement. The same results were obtained when the observed hand oscillation was executed with different frequency (1.6 Hz) and when the hands of mover and observer were supine. No motor resonance was elicited by observing the oscillation of a metal platform. The excitability modulation of MEPs simultaneously monitored in both antagonists of the observer's forearm (FCR and Extensor Carpi Radialis, ECR) was in almost perfect phase opposition, reflecting their natural reciprocal activation during the execution of a hand oscillation. These findings suggest that during observation, motor pathways are modulated subliminally reproducing with high temporal fidelity the motor commands needed to execute the observed movement.

Excitability changes in human corticospinal projections to muscles moving hand and fingers while viewing a reaching and grasping action.

Excitability of the H-reflex in the relaxed flexor digitorum superficialis (FDS) muscle was tested in five subjects observing a reaching and grasping action. The amplitude of the FDS H-reflex was modulated with a peak occurring during the hand-opening phase of the observed movement. When the H-reflex was facilitated by subliminal transcranial magnetic stimulation (TMS), the modulation was larger than for an unconditioned reflex of similar size. This suggests that the primary motor cortex excitability is modulated by action viewing and reasonably causes the motoneuronal excitability changes. Moreover, motor evoked potentials (MEPs) were elicited by supraliminal TMS in FDS, flexor carpi radialis (FCR) and first dorsal interosseus (FDI) when observing the same movement. MEP amplitude was modulated in FDS with the same time-course as the H-reflex, the peak excitability occurring during hand opening. In FDI, however, the maximal excitability occurred during finger closing while in FCR no correlation was found with the movement phases. Finally the EMG activity of FCR, FDS and FDI was recorded while the subjects were actually performing a grasping movement similar to the one observed. In all subjects and for each muscle there was a clear-cut correspondence between the time-course of the excitability modulation of MEPs and the temporal pattern of EMG recruitment. In conclusion, the present study suggests that 'motor resonance' subliminally activates the same motor pathways that would be overtly recruited in each observer when actually performing the observed movement, reproducing the personal strategy adopted in the same task.

The role of the primary motor cortex in mental rotation: a TMS study.

Mental rotation (MR) is sustained by a network of brain regions, including parietal, pre-motor and primary motor (M1) cortices. However it is still not clear whether M1 is recruited only when individuals mentally rotate hands or whether it is also enhanced by MR of non-body parts. Here we report two experiments in which the involvement of M1 in MR of hands and letters was tested using TMS. In Experiments 1a and 1b participants were asked to judge whether two line drawings, depicting either hands or letters, were the same or mirror images of each other (N = 112). Subjects were presented with pairs of stimuli with the same orientation (baseline condition) in half of the trials, while in the other half the stimulus in the right visual field was rotated (rotation condition). They performed the same-different task in three experimental situations: TMS of the primary motor hand area delivered at 400 ms after stimulus onset, sham TMS, and no-TMS. We stimulated the left M1 in Experiment 1a, and the right in Experiment 1b. Results showed that in Experiment 1a participants were slower after TMS when they performed MR of hands but not of letters. In Experiment 1b we failed to find an effect of TMS on MR of hands and letters. While in Experiment 1 the stimulus to be rotated was always presented in the right visual field, in Experiment 2 it was presented either in the left or in the right visual field. Results showed that only when TMS was delivered to the left M1, participants' ability to mentally rotate right and left hands slowed down. Taken together, these findings suggest that the left but not the right M1 plays a critical role in MR of hands.

Excitability changes in resting forearm muscles during voluntary foot movements depend on hand position: a neural substrate for hand-foot isodirectional coupling.

When associating hand and foot voluntary oscillations, isodirectional coupling is preferred irrespective of hand position (prone or supine). To investigate the neural correlates of this coupling modality, excitability of the motor projections innervating the resting forearm was tested during cyclic voluntary flexion-extensions of the ipsilateral foot. H-reflexes, in some experiments facilitated by subliminal Transcranial Magnetic Stimulation (TMS), and Compound Muscle Action Potentials (CMAPs), evoked by supraliminal TMS, were elicited in Flexor Carpi Radialis (FCR) and Extensor Carpi Radialis (ECR) muscles at five intervals during the foot movement cycle. With the hand prone, a sinusoidal excitability modulation was observed in wrist flexors and extensors, but reversed in phase: in FCR, excitability increased during plantar-flexion and decreased during dorsiflexion, while in ECR the opposite occurred. This reciprocal organisation was confirmed by the excitability modulation of CMAPs evoked simultaneously in the two antagonists. When the hand was supinated, the H-reflex modulation reversed in phase, i.e., FCR excitability increased during foot dorsiflexion and decreased during plantar-flexion. In both muscles and hand positions tested, when the muscle-to-movement phase-lag was increased by inertial loading of the foot, H-reflex excitability modulations remained phase linked to muscular contractions, not to movement. Together, these results suggest that the subliminal excitability modulation of hand movers has a common central origin with the parallel overt activation of foot movers, is reciprocally organised, and is direction- not muscle-dependent. It may therefore represent the neural substrate for isodirectional coupling of hand (prone or supine) with the foot.

Cyclic h-reflex modulation in resting forearm related to contractions of foot movers, not to foot movement.

During rhythmic voluntary oscillations of the foot, the excitability of the H-reflex in the Flexor Carpi Radialis (FCR) muscle of the resting prone forearm increases during the foot plantar-flexion and decreases during dorsiflexion. It is known that, when the two extremities are moved together, isodirectional (in-phase) coupling is the preferred form of movement association. Thus the above pattern of the H-reflex excitability modulation may favor the preferred coupling between the two limbs. To gain some clues about its origin, FCR H-reflex excitability was tested before and after modifying the phase relations between the activation [electromyogram (EMG)] of foot movers and foot movement, either by loading of the foot or by changing the movement frequency. After foot loading, the movement cycle was consistently delayed with respect to the onset of the EMG in Soleus (Sol) or Tibialis Anterior (TA) muscles. Simultaneously, the FCR H-reflex modulation advanced by that same amount with respect to the foot movement, thus remaining phase-locked to the EMG onsets. Similarly, when movement frequency was varied step-wise between 1.0 and 2.0 Hz, the foot movement was progressively delayed with respect to both the EMG onset (Sol and TA) and the FCR H-reflex modulation, so that the phase relation between the motor command to the foot and the H-modulation in the forearm remained constant. These results suggest that modulation of H-reflex in the forearm is tied to leg muscle contraction, rather than to foot kinematics, and point to a central, rather than kinesthetic, origin for the modulation.

Excitability changes in human corticospinal projections to forearm muscles during voluntary movement of ipsilateral foot.

Excitability of the H-reflex in the relaxed flexor carpi radialis (FCR) muscle was tested during voluntary oscillations of the ipsilateral foot at five evenly spaced delays during a 600 ms cycle. In some experiments the H-reflex was conditioned by transcranial magnetic stimulation (TMS). With the hand prone, the amplitude of the FCR H-reflex was modulated sinusoidally with the same period as the foot oscillation, the modulation peak occurring in coincidence with contraction of the foot plantar-flexor soleus and the trough during contraction of the extensor tibialis anterior. When the H-reflex was facilitated by TMS at short latency (conditioning-test interval: -2 to -3.5 ms), the modulation was larger than that occurring with an unconditioned reflex of comparable size. This suggests that both the peripheral and the corticospinal components of the facilitated response were modulated in parallel. When the H-reflex was tested 40-60 ms after conditioning, i.e. during the cortical "silent period" induced by TMS, no direct effect was produced on the reflex size but the foot-associated modulation was deeply depressed. These results suggest that the reflex modulation may depend on activity fluctuations in the cortical motor area innervating the forearm motoneurones. It is proposed that when the foot is rhythmically oscillated, along with the full activation of the foot cortical area a simultaneous lesser co-activation of the forearm area produces a subliminal cyclic modulation of cervical motoneurones excitability. Should the two limbs be moved together, the time course of this modulation would favour isodirectional movements of the prone hand and foot, indeed the preferential coupling observed when hand and foot are voluntarily oscillated.