Functional Segregation within Pars Opercularis of the Inferior Frontal Gyrus: Evidence from fMRI Studies of Imitation and Action Observation

Ahmanson-Lovelace Brain Mapping Center, 660 Charles Young Dr. South, Los Angeles, CA 90095, USA.
Cerebral Cortex (Impact Factor: 8.67). 07/2005; 15(7):986-94. DOI: 10.1093/cercor/bhh199
Source: PubMed


Recent neuroimaging studies have suggested that the inferior frontal gyrus (IFG) is important for action observation and imitation. In order to further explore the role of IFG in action observation and imitation, we pooled data from seven functional magnetic resonance imaging studies involving observation and imitation of simple finger movements performed in our laboratory. For imitation we found two peaks of activation in the pars opercularis, one in its dorsal sector and the other in its ventral sector. The dorsal sector of the pars opercularis was also activated during action observation, whereas the ventral sector was not. In addition, the pars triangularis was activated during action observation but not during imitation. This large dataset suggests a functional parcellation of the IFG that we discuss in terms of human mirror areas and the computational motor control architecture of internal models.

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    • "These studies have, thus, suggested that this brain area may include, in addition to the more commonly postulated mouth motor representation, a representation of hand and finger actions, a feature that would reinforce the homology with F5 in the macaque and further support the mirror hypothesis of language evolution. Several studies have also reported the bilateral activation of BA44 during hand and mouth action observation, hence the proposal to include this area in the MNS [Molnar-Szakacs et al., 2005, Tettamanti et al., 2005]. However, in these studies, the definition of areas activated during action observation was not matched to execution, so that one of the fundamental parameters of the definition of " mirror " function, that is, activation of neural substrates by both observation and execution, was not verified [Dinstein et al., 2007; Turella et al., 2009]. "
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    ABSTRACT: 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. Hum Brain Mapp, 2014. © 2014 Wiley Periodicals, Inc.
    Full-text · Article · Oct 2014 · Human Brain Mapping
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    • "Afterwards, we explored specific cortical and spinal circuits during MO, and focused at the delays of interest (500 ms and Control). Therefore, a different modulation of excitability might be present at different time points (Fadiga et al., 1995; Brighina et al., 2000; Strafella and Paus, 2000; Baldissera et al., 2001; Clark et al., 2004; Molnar-Szakacs et al., 2005; Montagna et al., 2005; Alaerts et al., 2009b; Koch et al., 2010; Catmur et al., 2011; Donne et al., 2011). ICF, a marker of cortical excitability, was found to be elevated in our study, suggesting that some cortical circuits were boosted by MO at 500 ms after movement-onset, in agreement with data obtained in monkeys during execution and observation (Vigneswaran et al., 2013). "
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    ABSTRACT: Although observation of a movement increases the excitability of the motor system of the observer, it does not induce a motor replica. What is the mechanism for replica suppression? We performed a series of experiments, involving a total of 66 healthy humans, to explore the excitability of different M1 circuits and the spinal cord during observation of simple movements. Several strategies were used. In the first and second experimental blocks, we used several delay times from movement onset to evaluate the time-course modulation of the cortico-spinal excitability (CSE), and its potential dependency on the duration of the movement observed; in order to do this single pulse transcranial magnetic stimulation (TMS) over M1 was used. In subsequent experiments, at selected delay times from movement-onset, we probed the excitability of the cortico-spinal circuits using three different approaches: (i) electric cervicomedullary stimulation (CMS), to test spinal excitability, (ii) paired-pulse TMS over M1, to evaluate the cortical inhibitory-excitatory balance (short intracortical inhibition (SICI) and intracortical facilitation (ICF)], and (iii) continuous theta-burst stimulation (cTBS), to modulate the excitability of M1 cortical circuits. We observed a stereotyped response in the modulation of CSE. At 500 ms after movement-onset the ICF was increased; although the most clear-cut effect was a decrease of CSE. The compensatory mechanism was not explained by changes in SICI, but by M1-intracortical circuits targeted by cTBS. Meanwhile, the spinal cord maintained the elevated level of excitability induced when expecting to observe movements, potentially useful to facilitate any required response to the movement observed.
    Full-text · Article · Sep 2014 · Frontiers in Behavioral Neuroscience
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    • "Activation of iFG pars opercularis was reported by studies investigating the processing of tool stimuli [3], [27] and when access to action concepts was required [44]–[46]. Furthermore, activation of pars opercularis and premotor cortex was reported in neuroimaging studies investigating neural correlates of action observation [47], [48], with left-hemispheric activation of ventrolateral premotor cortex in tasks requiring access to object representations and right-hemispheric recruitment during tasks requiring analysis of movements [47]. Recruitment of iFG pars opercularis has also been interpreted to reflect the extraction of action goals during grasp observation [33]. "
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    ABSTRACT: Tools represent a special class of objects, as functional details of tools can afford certain actions. In addition, information gained via prior experience with tools can be accessed on a semantic level, providing a basis for meaningful object interactions. Conceptual representations of tools also encompass knowledge about tool manipulation which can be acquired via direct (active manipulation) or indirect (observation of others manipulating objects) motor experience. The present study aimed to explore the impact of observation of manipulation on the neural processing of previously unfamiliar, manipulable objects. Brain activity was assessed by means of functional magnetic resonance imaging while participants accomplished a visual matching task involving pictures of the novel objects before and after they received object-related training. Three training session in which subjects observed an experimenter manipulating one set of objects and visually explored another set of objects were used to make subjects familiar with the tools and to allow the formation of new tool representations. A control object set was not part of the training. Training-related brain activation increases were found for observed manipulation objects compared to not trained objects in a left-hemispheric network consisting of inferior frontal gyrus (iFG) pars opercularis and triangularis and supramarginal/angular gyrus. This illustrates that direct manipulation experience is not required to elicit tool-associated activation changes in the action system. While the iFG activation might indicate a close relationship between the areas involved in tool representation and those involved in observational knowledge acquisition, the parietal activation is discussed in terms of non-semantic effects of object affordances and hand-tool spatial relationships.
    Full-text · Article · Jun 2014 · PLoS ONE
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