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Mapping motor representations with positron emission tomography

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Abstract

Brain activity was mapped in normal subjects during passive observation of the movements of an 'alien' hand and while imagining grasping objects with their own hand. None of the tasks required actual movement. Shifting from one mental task to the other greatly changed the pattern of brain activation. During observation of hand movements, activation was mainly found in visual cortical areas, but also in subcortical areas involved in motor behaviour, such as the basal ganglia and the cerebellum. During motor imagery, cortical and subcortical areas related to motor preparation and programming were strongly activated. These data support the notion that motor learning during observation of movements and mental practice involves rehearsal of neural pathways related to cognitive stages of motor control.
... Kavanagh and colleagues (2005) proposed that specific brain regions are activated when experiencing desires or cravings, similar to those activated during sensory imagery within the same sensory category. Indeed, the intention to initiate a movement leads to the activation of motion-related areas, such as the premotor cortex, or the parietal lobe and cerebellum (Decety et al. 1990(Decety et al. , 1994. In the same vein, the desire for music might lead to activation of brain regions associated with music imagery, i.e., the prefrontal cortex, the inferior frontal gyrus, or the superior temporal gyrus (Herholz et al. 2012). ...
... This notion is supported, among others, by research using imaging techniques that show that brain regions involved in action execution are also activated during mental imagery (Hardwick et al. 2018). In fact, the premotor cortex (PMC), supplementary motor areas (Gerardin et al. 2000;Johnson et al. 2002;Kuhtz-Buschbeck et al. 2003;Oostra et al. 2016;Orlandi et al. 2020), parietal regions (Decety et al. 1994;Sirigu et al. 1996;Pelgrims et al. 2009), cerebellum and basal ganglia (Decety et al. 1994;Grealy and Lee 2011;Heremans et al. 2011;Oostra et al. 2016) have been found active in various motor imagery tasks. The PMC and parietal areas would share a functional neural circuitry in the distributed Fronto-Parietal Network (dFPN) (Hétu et al. 2013;Ptak et al. 2017), enabling emulation. ...
... This notion is supported, among others, by research using imaging techniques that show that brain regions involved in action execution are also activated during mental imagery (Hardwick et al. 2018). In fact, the premotor cortex (PMC), supplementary motor areas (Gerardin et al. 2000;Johnson et al. 2002;Kuhtz-Buschbeck et al. 2003;Oostra et al. 2016;Orlandi et al. 2020), parietal regions (Decety et al. 1994;Sirigu et al. 1996;Pelgrims et al. 2009), cerebellum and basal ganglia (Decety et al. 1994;Grealy and Lee 2011;Heremans et al. 2011;Oostra et al. 2016) have been found active in various motor imagery tasks. The PMC and parietal areas would share a functional neural circuitry in the distributed Fronto-Parietal Network (dFPN) (Hétu et al. 2013;Ptak et al. 2017), enabling emulation. ...
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The literature has demonstrated the potential for detecting accurate electrical signals that correspond to the will or intention to move, as well as decoding the thoughts of individuals who imagine houses, faces or objects. This investigation examines the presence of precise neural markers of imagined motivational states through the combining of electrophysiological and neuroimaging methods. 20 participants were instructed to vividly imagine the desire to move, listen to music or engage in social activities. Their EEG was recorded from 128 scalp sites and analysed using individual standardized Low-Resolution Brain Electromagnetic Tomographies (LORETAs) in the N400 time window (400–600 ms). The activation of 1056 voxels was examined in relation to the 3 motivational states. The most active dipoles were grouped in eight regions of interest (ROI), including Occipital, Temporal, Fusiform, Premotor, Frontal, OBF/IF, Parietal, and Limbic areas. The statistical analysis revealed that all motivational imaginary states engaged the right hemisphere more than the left hemisphere. Distinct markers were identified for the three motivational states. Specifically, the right temporal area was more relevant for “Social Play”, the orbitofrontal/inferior frontal cortex for listening to music, and the left premotor cortex for the “Movement” desire. This outcome is encouraging in terms of the potential use of neural indicators in the realm of brain-computer interface, for interpreting the thoughts and desires of individuals with locked-in syndrome.
... The study of human brain activity during motor imagery (MI) plays an important role in clinical neurology and neuroscience and for this reason the neuronal representation of MI and motor execution has been studied intensively for years using brain imaging techniques such as functional magnetic resonance [39], EEG [40]- [42] and positron emission tomography [43]. It is well established that adults present 8-12 Hz (i.e. ) and 16-26 Hz (i.e. ) rhythms in the EEG recorded from the scalp over the primary sensorimotor cortex. ...
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The evaluation of time and frequency domain measures of coupling and causality relies on the parametric representation of linear multivariate processes. The study of temporal dependencies among time series is based on the identification of a Vector Autoregressive model. This procedure is pursued through the definition of a regression problem solved by means of Ordinary Least Squares (OLS) estimator. However, its accuracy is strongly influenced by the lack of data points and a stable solution is not always guaranteed. To overcome this issue, it is possible to use penalized regression techniques. The aim of this work is to compare the behavior of OLS with different penalized regression methods used for a connectivity analysis in different experimental conditions. Bias, accuracy in the reconstruction of network structure and computational time were used for this purpose. Different penalized regressions were tested by means of simulated data implementing different ground-truth networks under different amounts of data samples available. Then, the approaches were applied to real electroencephalographic signals (EEG) recorded from a healthy volunteer performing a motor imagery task. Penalized regressions outperform OLS in simulation settings when few data samples are available. The application on real EEG data showed how it is possible to use features extracted from brain networks for discriminating between two tasks even in conditions of data paucity. Penalized regression techniques can be used for brain connectivity estimation and can be exploited for the computation of all the connectivity estimators based on linearity assumption overcoming the limitations imposed by the classical OLS.
... However, in the present case an inanimate device was used that only mimicked the spatiotemporal movements of a hand, and did not look or otherwise act human. The results of Meltzoff (1995) dovetail with the finding that there are certain neural systems activated by human actions and not similar movements produced by a mechanical device (Decety et al. 1994;Perani et al. 2001;Castiello et al. 2002), and the demonstration that infants process animate body parts differently from inanimate objects (e.g. Brooks & Meltzoff 2002). ...
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Humans, like other primates, are intensely social creatures. One of the main functions of our brains is to enable us to be as skilful in social interactions as we are in our interactions with the physical world. Any differences between human brains and those of our nearest relatives, the great apes, are likely to be linked to our unique achievements in social interaction and communication rather than our motor or perceptual skills. Unique to humans is the ability to mentalise (or mind read), that is to perceive and communicate mental states, such as beliefs and desires. A key problem facing neuroscience is to uncover the biological mechanisms underlying our ability to read other minds and to show how these mechanisms evolved. To solve this problem we need to do experiments in which people (or animals) interact with one another rather than behaving in isolation. Such experiments are now being conducted in increasing numbers and many of the leading exponents of such experiments have contributed to this volume. ‘The Neuroscience of Social Interactions’ will be an important step in uncovering the biological mechanisms underlying social interactions - undoubtedly one of the major programmes for neuroscience in the twenty-first century.
... Indeed, all these findings align with those studies examining cerebral activation related to observed or imagined prehension movements. These studies have consistently reported activation in areas such as the intraparietal sulcus, as well as the inferior and superior parietal lobules (Binkofski et al., 1998;Buccino et al., 2001;Decety et al., 1994;Grafton et al., 1996;Grèzes et al., 2003;Grèzes and Decety, 2002;Vingerhoets et al., 2009Vingerhoets et al., , 2010. Additional evidence from the SPL comes from monkey studies that show the involvement of this part of the brain in the encoding of object affordance. ...
... Motor imagery (MI) is a mental simulation or rehearsal of a movement without any motor output [1]. Previous research suggests that during MI, neural activity is similar to that during actual movements [2,3], and studies using transcranial magnetic stimulation (TMS) have shown that during MI, corticospinal excitability in the muscles involved in that movement is enhanced (e.g., Kasai et al. 1997, Fadiga et al., 1999 [4,5]. ...
... Indeed, the intention to initiate a movement leads to the activation of motion-related areas, such as the premotor cortex, or the parietal lobe and cerebellum (Decety et al., 1990(Decety et al., , 1994. In the same vein, the desire for music might lead to activation of brain regions associated with music imagery, i.e., the prefrontal cortex, the inferior frontal gyrus, or the superior temporal gyrus (Herholz et al., 2012). ...
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The literature has demonstrated the potential for detecting accurate electrical signals that correspond to the will or intention to move, as well as decoding the thoughts of individuals who imagine houses, faces or objects. This investigation examines the presence of precise neural markers of imagined motivational states through the combining of electrophysiological and neuroimaging methods. 20 participants were instructed to vividly imagine the desire to move, listen to music or engage in social activities. Their EEG was recorded from 128 scalp sites and analysed using individual standardized Low-Resolution Brain Electromagnetic Tomographies (LORETAs) in the N400 time window (400–600 ms). The activation of 1056 voxels was examined in relation to the 3 motivational states. The most active dipoles were grouped in eight regions of interest (ROI), including Occipital, Temporal, Fusiform, Premotor, Frontal, OBF/IF, Parietal, and Limbic areas. The statistical analysis revealed that all motivational imaginary states engaged the right hemisphere more than the left hemisphere. Distinct markers were identified for the three motivational states. Specifically, the right temporal area was more relevant for "Social Play", the orbitofrontal/inferior frontal cortex for listening to music, and the left premotor cortex for the "Movement" desire. This outcome is encouraging in terms of the potential use of neural indicators in the realm of brain-computer interface, for interpreting the thoughts and desires of individuals with locked-in syndrome.
... The ability to mentally recall a motor act without any overt movement is called motor imagery (MI) (Kosslyn et al. 1995). The movement simulation that occurs on a cognitive level can be seen as a way in which we express the mental representation of the body in action (Decety et al. 1994;Decety and Jeannerod 1996;Gentilucci et al. 1998;Parsons 1987;Sekiyama 1982). MI tasks can be used as a proxy for the exploration of the mental representations of the body (e.g. ...
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The mental representation of the body in action can be explored using motor imagery (MI) tasks. MI tasks can be allocated along a continuum going from more implicit to more explicit tasks, where the discriminant is the degree of action monitoring required to solve the tasks (which is the awareness of using the mental representation of our own body to monitor our motor imagery). Tasks based on laterality judgments, such as the Hand Laterality Task (HLT) and the Foot Laterality Task (FLT), provide an example of more implicit tasks (i.e., less action monitoring is required). While, an example of a more explicit task is the Mental Motor Chronometry task (MMC) for hands and feet, where individuals are asked to perform or imagine performing movements with their limbs (i.e., more action monitoring is required). In our study, we directly compared hands and feet at all these tasks for the first time, as these body districts have different physical features as well as functions. Fifty-five participants were asked to complete an online version of the HLT and FLT (more implicit measure), and an online version of the MMC task for hands and feet (more explicit measure). The mental representation of hands and feet in action differed only when the degree of action monitoring decreased (HLT ≠ FLT); we observed the presence of biomechanical constraints only for hands. Differently, when the degree of action monitoring increased hands and feet did not show any difference (MMC hands = MMC feet). Our results show the presence of a difference in the mental representation of hands and feet in action that specifically depends on the degree of action monitoring.
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