Paola Borroni

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.

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.

Activation of motor pathways during observation and execution of hand movements

Abstract 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 observers 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.

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.

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.

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.

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 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 Brocas area, as homologous to F5, a relevant issue in light of the mirror hypothesis of language evolution, which postulates a key role of Brocas area in action/speech perception/production. We assess “mirror” properties of this area by combining neuroimaging and intraoperative neurophysiological techniques. Our results show that Brocas 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. Hum Brain Mapp 36:1010–1027, 2015.

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.

Erythropoietin effect on sensorimotor recovery after contusive spinal cord injury: an electrophysiological study in rats.

Spinal cord injury (SCI) is a debilitating clinical condition, characterized by a complex of neurological dysfunctions. It has been shown in rats that the acute administration of recombinant human erythropoietin (rhEPO) following a contusive SCI improves the recovery of hindlimb motor function, as measured with the locomotor BBB (Basso, Beattie, Bresnahan) scale. This scale evaluates overall locomotor activity, without testing whether the rhEPO-induced motor recovery is due to a parallel recovery of sensory and/or motor pathways. Aim of the present study was to utilize an electrophysiological test to evaluate, in a rat model of contusive SCI, the transmission of both ascending and descending pathways across the damaged cord at 2, 5, 7, 11, and 30 days after lesion, in animals treated with rhEPO (n=25) vs saline solution (n=25). Motor potentials evoked by epicortical stimulation were recorded in the spinal cord, and sensory-evoked potentials evoked by spinal stimulation were recorded at the cortical level. In the same animals BBB score and immunocytochemical evaluation of the spinal segments caudal to the lesion were performed. In rhEPO-treated animals results show a better general improvement both in sensory and motor transmission through spared spinal pathways, supposedly via the reticulo-spinal system, with respect to saline controls. This improvement is most prominent at relatively early times. Overall these features show a parallel time course to the changes observed in BBB score, suggesting that EPO-mediated spared spinal cord pathways might contribute to the improvement in transmission which, in turn, might be responsible for the recovery of locomotor function.