ABSTRACT
BACKGROUND: Making sense of others' actions relies on the activation of an action observation network (AON), which maps visual information about observed actions onto the observer's motor system. This motor resonance process manifests in the primary motor cortex (M1) as increased corticospinal excitability finely tuned to the muscles engaged in the observed action. Motor resonance in M1 is facilitated by projections from higher-order AON regions. However, whether manipulating the strength of AON-to-M1 connectivity affects motor resonance remains unclear. METHODS: We used transcranial magnetic stimulation (TMS) in 48 healthy humans. Cortico-cortical paired associative stimulation (ccPAS) was administered over M1 and the ventral premotor cortex (PMv), a key AON node, to induce spike-timing-dependent plasticity (STDP) in the pathway connecting them. Single-pulse TMS assessed motor resonance during action observation. RESULTS: Before ccPAS, action observation increased corticospinal excitability in the muscles corresponding to the observed movements, reflecting motor resonance in M1. Notably, ccPAS aimed at strengthening projections from PMv to M1 (PMvâM1) induced short-term enhancement of motor resonance. The enhancement specifically occurred with the ccPAS configuration consistent with forward PMvâM1 projections and dissipated 20 min post-stimulation; ccPAS administered in the reverse order (M1âPMv) and sham stimulation did not affect motor resonance. CONCLUSIONS: These findings provide the first evidence that inducing STDP to strengthen PMv input to M1 neurons causally enhances muscle-specific motor resonance in M1. Our study sheds light on the plastic mechanisms that shape AON functionality and demonstrates that exogenous manipulation of AON connectivity can influence basic mirror mechanisms that underlie social perception.
Subject(s)
Evoked Potentials, Motor , Motor Cortex , Neuronal Plasticity , Transcranial Magnetic Stimulation , Humans , Motor Cortex/physiology , Male , Female , Adult , Neuronal Plasticity/physiology , Evoked Potentials, Motor/physiology , Young Adult , Muscle, Skeletal/physiology , Pyramidal Tracts/physiology , Electromyography , Neural Pathways/physiologyABSTRACT
The left supramarginal gyrus (SMG) is a critical structure in tool use actions, including such simple acts as selection of appropriate grasps and, if necessary, their on-line corrections. Yet, its temporal contribution to initial planning of functional grasps of tools is largely unknown. We used MRI-guided, event-related transcranial magnetic stimulation (TMS) to determine the time point when SMG involvement in processing of tools for functional grasp decision was affected most. In Exp. 1, with 15 participants, triple-pulse (10 Hz) TMS was applied to either the left anterior-to-mid SMG (amSMG; subdivisions PFt/PF) or vertex at three different time points: starting from 17 ms (i.e., delivered at 17/117/217 ms), 117 ms (117/217/317 ms) or 217 ms (217/317/417 ms) after stimulus onset. In Exp. 2, with 12 participants, we applied single-pulse TMS to either left amSMG or the left rostral middle frontal gurus (rMFG; area 46) at these same time points relative to stimulus onset. Subject- and item-based analyses of response times (RTs) were performed. Whereas the amSMG and vertex stimulation with triple pulse has revealed differential effects on RTs in general, as well as on tool orientation processing, it gave only vague pointers as to their temporal contributions to the task. Yet, amSMG and rMFG stimulation with single pulse demonstrated that, while the processing in both of these areas can be enhanced at 17 ms and no doubt at 117 ms (as compared to 217 ms), the earliest stimulation facilitated amSMG (vs. rMFG) contribution, and the latest stimulation had the opposite effect, facilitating rMFG (vs. amSMG) contribution to planning functional grasps. These outcomes demonstrate that the critical role of SMG in tool-related actions can be invoked substantially earlier than previously thought.
Subject(s)
Functional Laterality/physiology , Hand Strength/physiology , Parietal Lobe/physiology , Psychomotor Performance/physiology , Transcranial Magnetic Stimulation , Adult , Female , Humans , Male , Neuronavigation , Reaction Time/physiology , Time Factors , Young AdultABSTRACT
A consolidated practice in cognitive neuroscience is to explore the properties of human visual working memory through the analysis of electromagnetic signals using cued change detection tasks. Under these conditions, EEG/MEG activity increments in the posterior parietal cortex scaling with the number of memoranda are often reported in the hemisphere contralateral to the objects' position in the memory array. This highly replicable finding clashes with several reported failures to observe compatible hemodynamic activity modulations using fMRI or fNIRS in comparable tasks. Here, we reconcile this apparent discrepancy by acquiring fMRI data on healthy participants and employing a cluster analysis to group voxels in the posterior parietal cortex based on their functional response. The analysis identified two distinct subpopulations of voxels in the intraparietal sulcus (IPS) showing a consistent functional response among participants. One subpopulation, located in the superior IPS, showed a bilateral response to the number of objects coded in visual working memory. A different subpopulation, located in the inferior IPS, showed an increased unilateral response when the objects were displayed contralaterally. The results suggest that a cluster of neurons in the inferior IPS is a candidate source of electromagnetic contralateral responses to working memory load in cued change detection tasks.
Subject(s)
Memory, Short-Term/physiology , Parietal Lobe/physiology , Pattern Recognition, Visual/physiology , Adult , Brain Mapping/methods , Cerebrovascular Circulation , Cluster Analysis , Cues , Female , Functional Laterality , Humans , Magnetic Resonance Imaging , Male , Neuropsychological Tests , Oxygen/bloodABSTRACT
The neural bases of haptically-guided grasp planning and execution are largely unknown, especially for stimuli having no visual representations. Therefore, we used functional magnetic resonance imaging (fMRI) to monitor brain activity during haptic exploration of novel 3D complex objects, subsequent grasp planning, and the execution of the pre-planned grasps. Haptic object exploration, involving extraction of shape, orientation, and length of the to-be-grasped targets, was associated with the fronto-parietal, temporo-occipital, and insular cortex activity. Yet, only the anterior divisions of the posterior parietal cortex (PPC) of the right hemisphere were significantly more engaged in exploration of complex objects (vs. simple control disks). None of these regions were re-recruited during the planning phase. Even more surprisingly, the left-hemisphere intraparietal, temporal, and occipital areas that were significantly invoked for grasp planning did not show sensitivity to object features. Finally, grasp execution, involving the re-recruitment of the critical right-hemisphere PPC clusters, was also significantly associated with two kinds of bilateral parieto-frontal processes. The first represents transformations of grasp-relevant target features and is linked to the dorso-dorsal (lateral and medial) parieto-frontal networks. The second monitors grasp kinematics and belongs to the ventro-dorsal networks. Indeed, signal modulations associated with these distinct functions follow dorso-ventral gradients, with left aIPS showing significant sensitivity to both target features and the characteristics of the required grasp. Thus, our results from the haptic domain are consistent with the notion that the parietal processing for action guidance reflects primarily transformations from object-related to effector-related coding, and these mechanisms are rather independent of sensory input modality.
ABSTRACT
Experimental evidence suggests the existence of a sophisticated brain circuit specifically dedicated to reach-to-grasp planning and execution, both in human and non-human primates (Castiello, 2005). Studies accomplished by means of neuroimaging techniques suggest the hypothesis of a dichotomy between a "reach-to-grasp" circuit, involving the anterior intraparietal area, the dorsal and ventral premotor cortices (PMd and PMv - Castiello and Begliomini, 2008; Filimon, 2010) and a "reaching" circuit involving the medial intraparietal area and the superior parieto-occipital cortex (Culham et al., 2006). However, the time course characterizing the involvement of these regions during the planning and execution of these two types of movements has yet to be delineated. A functional magnetic resonance imaging study has been conducted, including reach-to-grasp and reaching only movements, performed toward either a small or a large stimulus, and Finite Impulse Response model (Henson, 2003) was adopted to monitor activation patterns from stimulus onset for a time window of 10 s duration. Data analysis focused on brain regions belonging either to the reaching or to the grasping network, as suggested by Castiello and Begliomini (2008). Results suggest that reaching and grasping movements planning and execution might share a common brain network, providing further confirmation to the idea that the neural underpinnings of reaching and grasping may overlap in both spatial and temporal terms (Verhagen et al., 2013). But, although responsive for both actions, they show a significant predominance for either one of the two actions and such a preference is evident on a temporal scale.
ABSTRACT
Action observation activates the same motor areas as those involved in the performance of the observed actions and promotes functional recovery following stroke. Movement observation is now considered a promising tool for motor rehabilitation, by allowing patients to train their motor functions when voluntary movement is partially impaired. We asked chronic-stroke patients, affected by either left (LHD) or right hemisphere (RHD) lesions, to observe either a left or right hand, while grasping a small target (eliciting a precision grip) or a large target (eliciting a whole hand grasp directed towards a target object). To better understand the effects of action observation on damaged motor circuits, we used transcranial magnetic stimulation (TMS) to induce motor evoked potentials (MEP) from two muscles of the unaffected hand in 10 completely hemiplegic participants. Results revealed that LHD patients showed MEP facilitation on the right (contralesional) M1 during action observation of hand-object interactions. In contrast, results showed no facilitation of the left (contralesional) M1 in RHD patients. Our results confirm that action observation might have a positive influence on the recovery of motor functions after stroke. Activating the motor system by means of action observation might provide a mechanism for improving function, at least in LHD patients.
Subject(s)
Evoked Potentials, Motor/physiology , Motor Cortex/physiology , Stroke/physiopathology , Transcranial Magnetic Stimulation , Aged , Female , Hand/physiology , Hand Strength/physiology , Humans , Male , Middle Aged , Muscle, Skeletal/physiology , Psychomotor Performance/physiologyABSTRACT
BACKGROUND: Anticipatory planning, the ability to anticipate future perceptual-motor demands of a goal-oriented action sequence, is essential for flexible, purposeful behavior. Once an action goal has been defined, movement details necessary to achieve that goal can be selected. Here, we investigate if anticipatory planning takes place even when multi-step actions are being carried out. How, we may ask, are the cerebral circuits involved in movement selection influenced by anticipated object-center task demands? Transcranial magnetic stimulation (TMS) was used to investigate how changes in corticospinal excitability (CSE) are dependent on anticipated task variables of intended future actions. Specifically, single- and paired-pulse TMS was used to evaluate corticospinal excitability during the action selection phase preparatory to grasp execution. RESULTS: We found that during the premovement phase, there is an object- and muscle-specific modulation in the intrinsic hand muscle that will be used during a forthcoming grasping action. Depending on whether the participants were instructed to perform a single- or double-step movement sequence, modulation of the corticospinal output to the appropriate hand muscles was dependent on what object was to be grasped and what type of movement was being prepared. No modulation in excitability was observed during one-step movements. CONCLUSIONS: Anticipation of intended task demands plays an important role in controlling multi- step actions during which ongoing behavior may need to be adjusted. This finding supports the notion that the cortico-cortical mechanism involving movement planning is specific for an object's properties as well as for the goal of the movement sequence.
Subject(s)
Anticipation, Psychological/physiology , Psychomotor Performance/physiology , Pyramidal Tracts/physiology , Adult , Electromyography , Evoked Potentials, Motor/physiology , Female , Hand/innervation , Hand/physiology , Hand Strength/physiology , Humans , Male , Muscle, Skeletal/physiology , Transcranial Magnetic StimulationABSTRACT
Grasp-related responses in neurons of the macaque rostral inferior parietal lobule [PF/PFG and the anterior intraparietal area (AIP)] are modulated by task context. Event-related functional MRI was used to determine whether this is true in putative homologs of the human cortex, the rostral inferior parietal lobule (rIPL) and the anterior intraparietal sulcus (aIPS). Fifteen healthy, right-handed adults were required to select prospectively the most comfortable way to grasp a horizontally oriented handle using the cued hand (left or right). In the "no-rotation" condition, the task was simply to grasp the handle, whereas in the "rotation" condition, the goal was to plan to grasp and rotate it into a vertical orientation with the cued end (medial or lateral) pointing downward. In both conditions, participants remained still and indicated their grip preferences by pressing foot pedals. As in overt grasping, participants' grip preferences were significantly influenced by anticipation of the demands associated with handle rotation. Activity within the aIPS and rIPL increased bilaterally in both the rotation and no-rotation conditions. Importantly, these responses were significantly greater in the rotation vs. no-rotation condition. Similar context effects were detected in the presupplementary motor area, caudal intraparietal sulcus/superior parietal lobule, and bilateral dorsal and left ventral premotor cortices. Grasp representations within the rIPL and aIPS are sensitive to predicted task demands and play a role in context-sensitive grip selection. Moreover, the findings provide additional evidence that areas involved in the sensorimotor control of grasp also contribute to feedforward planning.
Subject(s)
Cues , Hand Strength/physiology , Motor Cortex/physiology , Parietal Lobe/physiology , Psychomotor Performance/physiology , Adult , Female , Hand/physiology , Humans , Male , Photic Stimulation/methods , Prospective Studies , Young AdultABSTRACT
The aim of this study was to investigate in humans the effects of acupuncture upon upper-limb motor-evoked potentials (MEPs), elicited by transcranial magnetic stimulation of the primary motor cortex. It is known that peripheral sensory stimulation can be used to induce short- and long-term changes in motor cortex excitability. Data show that the simple insertion of the needle is an adequate somatosensory stimulus to induce a significant modulation of MEP amplitude, the sign of which (facilitation or inhibition) is specific to the investigated muscle and to the point of needle insertion. Moreover, MEP changes in upper-limb muscles are also observed following needling of lower-limb sites, revealing the presence of long-distance effects of acupuncture. Finally, the modulation in muscle excitability considerably outlasts the time period of needle application, demonstrating the induction of long-term plastic changes in the central nervous system. In addition, results have shown that the effects on muscle excitability are not restricted to the stimulation of well-coded acupoints, as described in traditional Chinese medicine, but they can also be induced by needling of nonacupoints, normally not used for therapeutic purposes. The possible neuronal mechanisms underlying the observed effects of acupuncture are discussed in relation to the available neurophysiological data regarding the interlimb reflexes and the changes in the representational cortical maps induced in humans by a prolonged somatosensory stimulation.