Neural circuits underlying imitation learning of hand actions: an event-related fMRI study

The neural bases of imitation learning are virtually unknown. In the present study, we addressed this issue using an event-related fMRI paradigm. Musically naive participants were scanned during four events: (1) observation of guitar chords played by a guitarist, (2) a pause following model observation, (3) execution of the observed chords, and (4) rest. The results showed that the basic circuit underlying imitation learning consists of the inferior parietal lobule and the posterior part of the inferior frontal gyrus plus the adjacent premotor cortex (mirror neuron circuit). This circuit, known to be involved in action understanding, starts to be active during the observation of the guitar chords. During pause, the middle frontal gyrus (area 46) plus structures involved in motor preparation (dorsal premotor cortex, superior parietal lobule, rostral mesial areas) also become active. Given the functional properties of area 46, a model of imitation learning is proposed based on interactions between this area and the mirror neuron system.     

Somatosensory-Motor Adaptation of Orofacial Actions in Posterior Parietal and Ventral Premotor Cortices

Recent studies have provided evidence for sensory-motor adaptive changes and action goal coding of visually guided manual action in premotor and posterior parietal cortices. To extend these results to orofacial actions, devoid of auditory and visual feedback, we used a repetition suppression paradigm while measuring neural activity with functional magnetic resonance imaging during repeated intransitive and silent lip, jaw and tongue movements. In the motor domain, this paradigm refers to decreased activity in specific neural populations due to repeated motor acts and has been proposed to reflect sensory-motor adaptation. Orofacial movements activated a set of largely overlapping, common brain areas forming a core neural network classically involved in orofacial motor control. Crucially, suppressed neural responses during repeated orofacial actions were specifically observed in the left ventral premotor cortex, the intraparietal sulcus, the inferior parietal lobule and the superior parietal lobule. Since no visual and auditory feedback were provided during orofacial actions, these results suggest somatosensory-motor adaptive control of intransitive and silent orofacial actions in these premotor and parietal regions.     

Complex Visual Search in Children and Adolescents: Effects of Age and Performance on fMRI Activation

Complex visuospatial processing relies on distributed neural networks involving occipital, parietal and frontal brain regions. Effects of physiological maturation (during normal brain development) and proficiency on tasks requiring complex visuospatial processing have not yet been studied extensively, as they are almost invariably interrelated. We therefore aimed at dissociating the effects of age and performance on functional MRI (fMRI) activation in a complex visual search task. In our cross-sectional study, healthy children and adolescents (n = 43, 19 females, 7-17 years) performed a complex visual search task during fMRI. Resulting activation was analysed with regard to the differential effects of age and performance. Our results are compatible with an increase in the neural network''s efficacy with age: within occipital and parietal cortex, the core regions of the visual exploration network, activation increased with age, and more so in the right than in the left hemisphere. Further, activation outside the visual search network decreased with age, mainly in left inferior frontal, middle temporal, and inferior parietal cortex. High-performers had stronger activation in right superior parietal cortex, suggesting a more mature visual search network. We could not see effects of age or performance in frontal cortex. Our results show that effects of physiological maturation and effects of performance, while usually intertwined, can be successfully disentangled and investigated using fMRI in children and adolescents.     

FMRI supports the sensorimotor theory of motor resonance

The neural mechanisms mediating the activation of the motor system during action observation, also known as motor resonance, are of major interest to the field of motor control. It has been proposed that motor resonance develops in infants through Hebbian plasticity of pathways connecting sensory and motor regions that fire simultaneously during imitation or self movement observation. A fundamental problem when testing this theory in adults is that most experimental paradigms involve actions that have been overpracticed throughout life. Here, we directly tested the sensorimotor theory of motor resonance by creating new visuomotor representations using abstract stimuli (motor symbols) and identifying the neural networks recruited through fMRI. We predicted that the network recruited during action observation and execution would overlap with that recruited during observation of new motor symbols. Our results indicate that a network consisting of premotor and posterior parietal cortex, the supplementary motor area, the inferior frontal gyrus and cerebellum was activated both by new motor symbols and by direct observation of the corresponding action. This tight spatial overlap underscores the importance of sensorimotor learning for motor resonance and further indicates that the physical characteristics of the perceived stimulus are irrelevant to the evoked response in the observer.     

Cerebral Activations Related to Writing and Drawing with Each Hand

BackgroundWriting is a sequential motor action based on sensorimotor integration in visuospatial and linguistic functional domains. To test the hypothesis of lateralized circuitry concerning spatial and language components involved in such action, we employed an fMRI paradigm including writing and drawing with each hand. In this way, writing-related contributions of dorsal and ventral premotor regions in each hemisphere were assessed, together with effects in wider distributed circuitry. Given a right-hemisphere dominance for spatial action, right dorsal premotor cortex dominance was expected in left-hand writing while dominance of the left ventral premotor cortex was expected during right-hand writing.MethodsSixteen healthy right-handed subjects were scanned during audition-guided writing of short sentences and simple figure drawing without visual feedback. Tapping with a pencil served as a basic control task for the two higher-order motor conditions. Activation differences were assessed with Statistical Parametric Mapping (SPM).ResultsWriting and drawing showed parietal-premotor and posterior inferior temporal activations in both hemispheres when compared to tapping. Drawing activations were rather symmetrical for each hand. Activations in left- and right-hand writing were left-hemisphere dominant, while right dorsal premotor activation only occurred in left-hand writing, supporting a spatial motor contribution of particularly the right hemisphere. Writing contrasted to drawing revealed left-sided activations in the dorsal and ventral premotor cortex, Broca’s area, pre-Supplementary Motor Area and posterior middle and inferior temporal gyri, without parietal activation.DiscussionThe audition-driven postero-inferior temporal activations indicated retrieval of virtual visual form characteristics in writing and drawing, with additional activation concerning word form in the left hemisphere. Similar parietal processing in writing and drawing pointed at a common mechanism by which such visually formatted information is used for subsequent sensorimotor integration along a dorsal visuomotor pathway. In this, the left posterior middle temporal gyrus subserves phonological-orthographical conversion, dissociating dorsal parietal-premotor circuitry from perisylvian circuitry including Broca''s area.     

Distinct Parietal and Temporal Pathways to the Homologues of Broca's Area in the Monkey

The homologues of the two distinct architectonic areas 44 and 45 that constitute the anterior language zone (Broca's region) in the human ventrolateral frontal lobe were recently established in the macaque monkey. Although we know that the inferior parietal lobule and the lateral temporal cortical region project to the ventrolateral frontal cortex, we do not know which of the several cortical areas found in those regions project to the homologues of Broca's region in the macaque monkey and by means of which white matter pathways. We have used the autoradiographic method, which permits the establishment of the cortical area from which axons originate (i.e., the site of injection), the precise course of the axons in the white matter, and their termination within particular cortical areas, to examine the parietal and temporal connections to area 44 and the two subdivisions of area 45 (i.e., areas 45A and 45B). The results demonstrated a ventral temporo-frontal stream of fibers that originate from various auditory, multisensory, and visual association cortical areas in the intermediate superolateral temporal region. These axons course via the extreme capsule and target most strongly area 45 with a more modest termination in area 44. By contrast, a dorsal stream of axons that originate from various cortical areas in the inferior parietal lobule and the adjacent caudal superior temporal sulcus was found to target both areas 44 and 45. These axons course in the superior longitudinal fasciculus, with some axons originating from the ventral inferior parietal lobule and the adjacent superior temporal sulcus arching and forming a simple arcuate fasciculus. The cortex of the most rostral part of the inferior parietal lobule is preferentially linked with the ventral premotor cortex (ventral area 6) that controls the orofacial musculature. The cortex of the intermediate part of the inferior parietal lobule is linked with both areas 44 and 45. These findings demonstrate the posterior parietal and temporal connections of the ventrolateral frontal areas, which, in the left hemisphere of the human brain, were adapted for various aspects of language production. These precursor circuits that are found in the nonlinguistic, nonhuman, primate brain also exist in the human brain. The possible reasons why these areas were adapted for language use in the human brain are discussed. The results throw new light on the prelinguistic precursor circuitry of Broca's region and help understand functional interactions between Broca's ventrolateral frontal region and posterior parietal and temporal association areas.     

Polymodal motion processing in posterior parietal and premotor cortex: a human fMRI study strongly implies equivalencies between humans and monkeys

In monkeys, posterior parietal and premotor cortex play an important integrative role in polymodal motion processing. In contrast, our understanding of the convergence of senses in humans is only at its beginning. To test for equivalencies between macaque and human polymodal motion processing, we used functional MRI in normals while presenting moving visual, tactile, or auditory stimuli. Increased neural activity evoked by all three stimulus modalities was found in the depth of the intraparietal sulcus (IPS), ventral premotor, and lateral inferior postcentral cortex. The observed activations strongly suggest that polymodal motion processing in humans and monkeys is supported by equivalent areas. The activations in the depth of IPS imply that this area constitutes the human equivalent of macaque area VIP.     

Neural systems involved in "theory of mind"

What is the nature of our ability to understand and reason about the beliefs of others--the possession of a "theory of mind", or ToM? Here, we review findings from imaging and lesion studies indicating that ToM reasoning is supported by a widely distributed neural system. Some functional components of this system, such as language-related regions of the left hemisphere, the frontal lobes and the right temporal parietal cortex, are not solely dedicated to the computation of mental states. However, the system also includes a core, domain-specific component that is centred on the amygdala circuitry. We provide a framework in which impairments of ToM can be viewed in terms of abnormalities of the core system, the failure of a co-opted system that is necessary for performance on a particular set of tasks, or the absence of an experiential trigger for the emergence of ToM.     

Surface Vulnerability of Cerebral Cortex to Major Depressive Disorder

Major depressive disorder (MDD) is accompanied by atypical brain structure. This study first presents the alterations in the cortical surface of patients with MDD using multidimensional structural patterns that reflect different neurodevelopment. Sixteen first-episode, untreated patients with MDD and 16 matched healthy controls underwent a magnetic resonance imaging (MRI) scan. The cortical maps of thickness, surface area, and gyrification were examined using the surface-based morphometry (SBM) approach. Increase of cortical thickness was observed in the right posterior cingulate region and the parietal cortex involving the bilateral inferior, left superior parietal and right paracentral regions, while decreased thickness was noted in the parietal cortex including bilateral pars opercularis and left precentral region, as well as the left rostral-middle frontal regions in patients with MDD. Likewise, increased or decreased surface area was found in five sub-regions of the cingulate gyrus, parietal and frontal cortices (e.g., bilateral inferior parietal and superior frontal regions). In addition, MDD patients exhibited a significant hypergyrification in the right precentral and supramarginal region. This integrated structural assessment of cortical surface suggests that MDD patients have cortical alterations of the frontal, parietal and cingulate regions, indicating a vulnerability to MDD during earlier neurodevelopmental process.     

Viewing lip forms: cortical dynamics

Viewing other persons' actions automatically activates brain areas belonging to the mirror-neuron system (MNS) assumed to link action execution and observation. We followed, by magnetoencephalographic cortical dynamics, subjects who observed still pictures of lip forms, on-line imitated them, or made similar forms in a self-paced manner. In all conditions and in both hemispheres, cortical activation progressed in 20-70 ms steps from the occipital cortex to the superior temporal region (where the strongest activation took place), the inferior parietal lobule, and the inferior frontal lobe (Broca's area), and finally, 50-140 ms later, to the primary motor cortex. The signals of Broca's area and motor cortex were significantly stronger during imitation than other conditions. These results demonstrate that still pictures, only implying motion, activate the human MNS in a well-defined temporal order.     

Motor cognition: a new paradigm to study self-other interactions

Accumulative empirical evidence has been reviewed in support of the notion that the production and perception of action as well as the interpretation of others' actions are functionally connected, and indeed, rely on common distributed neural systems in the premotor and parietal cortices. We suggest that these neural systems sustain shared representations between self and other that are crucial in social interactions. The inferior parietal cortex plays a special role in the sense of agency, which is a fundamental aspect to navigate within this neural network. The role of other brain areas that implement and regulate these shared representations remains to be specified.     

Interpersonal Liking Modulates Motor-Related Neural Regions

Observing someone perform an action engages brain regions involved in motor planning, such as the inferior frontal, premotor, and inferior parietal cortices. Recent research suggests that during action observation, activity in these neural regions can be modulated by membership in an ethnic group defined by physical differences. In this study we expanded upon previous research by matching physical similarity of two different social groups and investigating whether likability of an outgroup member modulates activity in neural regions involved in action observation. Seventeen Jewish subjects were familiarized with biographies of eight individuals, half of the individuals belonged to Neo-Nazi groups (dislikable) and half of which did not (likable). All subjects and actors in the stimuli were Caucasian and physically similar. The subjects then viewed videos of actors portraying the characters performing simple motor actions (e.g. grasping a water bottle and raising it to the lips), while undergoing fMRI. Using multivariate pattern analysis (MVPA), we found that a classifier trained on brain activation patterns successfully discriminated between the likable and dislikable action observation conditions within the right ventral premotor cortex. These data indicate that the spatial pattern of activity in action observation related neural regions is modulated by likability even when watching a simple action such as reaching for a cup. These findings lend further support for the notion that social factors such as interpersonal liking modulate perceptual processing in motor-related cortices.     

An fMRI Study of Audiovisual Speech Perception Reveals Multisensory Interactions in Auditory Cortex

Research on the neural basis of speech-reading implicates a network of auditory language regions involving inferior frontal cortex, premotor cortex and sites along superior temporal cortex. In audiovisual speech studies, neural activity is consistently reported in posterior superior temporal Sulcus (pSTS) and this site has been implicated in multimodal integration. Traditionally, multisensory interactions are considered high-level processing that engages heteromodal association cortices (such as STS). Recent work, however, challenges this notion and suggests that multisensory interactions may occur in low-level unimodal sensory cortices. While previous audiovisual speech studies demonstrate that high-level multisensory interactions occur in pSTS, what remains unclear is how early in the processing hierarchy these multisensory interactions may occur. The goal of the present fMRI experiment is to investigate how visual speech can influence activity in auditory cortex above and beyond its response to auditory speech. In an audiovisual speech experiment, subjects were presented with auditory speech with and without congruent visual input. Holding the auditory stimulus constant across the experiment, we investigated how the addition of visual speech influences activity in auditory cortex. We demonstrate that congruent visual speech increases the activity in auditory cortex.     

Functional magnetic resonance imaging of macaque monkeys performing visually guided saccade tasks: comparison of cortical eye fields with humans

The frontal and parietal eye fields serve as functional landmarks of the primate brain, although their correspondences between humans and macaque monkeys remain unclear. We conducted fMRI at 4.7 T in monkeys performing visually-guided saccade tasks and compared brain activations with those in humans using identical paradigms. Among multiple parietal activations, the dorsal lateral intraparietal area in monkeys and an area in the posterior superior parietal lobule in humans exhibited the highest selectivity to saccade directions. In the frontal cortex, the selectivity was highest at the junction of the precentral and superior frontal sulci in humans and in the frontal eye field (FEF) in monkeys. BOLD activation peaks were also found in premotor areas (BA6) in monkeys, which suggests that the apparent discrepancy in location between putative human FEF (BA6, suggested by imaging studies) and monkey FEF (BA8, identified by microstimulation studies) partly arose from methodological differences.     

Task-switching Cost and Intrinsic Functional Connectivity in the Human Brain: Toward Understanding Individual Differences in Cognitive Flexibility

The human ability to flexibly alternate between tasks (i.e., task-switching) represents a critical component of cognitive control. Many functional magnetic resonance imaging (fMRI) studies have explored the neural basis of the task-switching. However, no study to date has examined how individual differences in intrinsic functional architecture of the human brain are related to that of the task-switching. In the present study, we took 11 task-switching relevant areas from a meta-analysis study as the regions of interests (ROIs) and estimated their intrinsic functional connectivity (iFC) with the whole brain. This procedure was repeated for 32 healthy adults based upon their fMRI scans during resting-state (rfMRI) to investigate the correlations between switching cost and the iFC strength across these participants. This analysis found that switch cost was negatively correlated with a set of iFC involved ROIs including left inferior frontal junction, bilateral superior posterior parietal cortex, left precuneus, bilateral inferior parietal lobule, right middle frontal gyrus and bilateral middle occipital gyrus. These connectivity profiles represent an intrinsic functional architecture of task-switching where the left inferior frontal junction plays a hub role in this brain-behavior association. These findings are highly reproducible in another validation independent sample and provide a novel perspective for understanding the neural basis of individual differences in task-switching behaviors reflected in the intrinsic architecture of the human brain.     

Neural responses during Valsalva maneuvers in obstructive sleep apnea syndrome.

The repetitive upper airway muscle atonic episodes and cardiovascular sequelae of obstructive sleep apnea (OSA) suggest dysfunction of specific neural sites that integrate afferent airway signals with autonomic and somatic outflow. We determined neural responses to the Valsalva maneuver by using functional magnetic resonance imaging. Images were collected during a baseline and three Valsalva maneuvers in 8 drug-free OSA patients and 15 controls. Multiple cortical, midbrain, pontine, and medullary regions in both groups showed intensity changes correlated to airway pressure. In OSA subjects, the left inferior parietal cortex, superior temporal gyrus, posterior insular cortex, cerebellar cortex, fastigial nucleus, and hippocampus showed attenuated signal changes compared with controls. Enhanced responses emerged in the left lateral precentral gyrus, left anterior cingulate, and superior frontal cortex of OSA patients. The anterior cingulate, cerebellar cortex, and posterior insula exhibited altered response timing patterns between control and OSA subjects. The response patterns in OSA subjects suggest deficits in particular neural pathways that normally mediate the Valsalva maneuver and compensatory actions in other structures.     

Effect of Intentional Bias on Agency Attribution of Animated Motion: An Event-Related fMRI Study

Animated movements of simple geometric shapes can readily be interpreted as depicting social events in which animate agents are engaged in intentional activity. However, the brain regions associated with such intention have not been clearly elucidated. In this study, intentional bias was manipulated using shape and pattern animations while measuring associated brain activity using event-related functional magnetic resonance imaging (fMRI). Twenty-five higher-intention involved and twenty-five lower-intention involved animations were presented to participants. Behavioral results showed that the degree of agency attribution of the mental state increased as intentional involvement increased. fMRI results revealed that the posterior superior temporal sulcus (STS), inferior temporal gyrus (ITG), inferior frontal gyrus (IFG), premotor, temporal pole, supramarginal gyrus, and superior parietal lobule (SPL) were activated while participants viewed the high-intention animations. In contrast, occipital, lingual, and middle frontal gyri were activated while the participants viewed the low-intention animations. These findings suggest that as agent attribution increases, the visual brain changes its functional role to the intentional brain and becomes a flexible network for processing information about social interaction.     

Hemispheric dominance of cortical activity evoked by focal electrogustatory stimuli.

Functional magnetic resonance imaging was used to observe cortical hemodynamic responses to electric taste stimuli applied separately to the right and left sides of the tongue tip. In 11 right-handed normal adults activation occurred primarily in the insular cortex, superior temporal lobe, inferior frontal lobe, including premotor regions, and in inferior parts of the postcentral gyrus. Unexpectedly, the location and laterality of activation were largely identical regardless of the side of the tongue stimulated. Activation in the superior insula, the presumed location of primary gustatory cortex, was predominantly, but not exclusively, in the right hemisphere, whereas central (more inferior) insular activations were more evenly bilateral. Right hemispheric dominance of activation also occurred in premotor regions (Brodmann areas 6 and 44), whereas left hemispheric dominance occurred only in the superior temporal cortex (Brodmann areas 22/42). The electric taste-evoked hemodynamic response pattern was more consistent with activation of the gustatory system than activation of somatosensory systems. The results suggest that the sites for cortical processing of electric taste information are dependent on hemispheric specialization.     

Remapping for visual stability

Visual perception is based on both incoming sensory signals and information about ongoing actions. Recordings from single neurons have shown that corollary discharge signals can influence visual representations in parietal, frontal and extrastriate visual cortex, as well as the superior colliculus (SC). In each of these areas, visual representations are remapped in conjunction with eye movements. Remapping provides a mechanism for creating a stable, eye-centred map of salient locations. Temporal and spatial aspects of remapping are highly variable from cell to cell and area to area. Most neurons in the lateral intraparietal area remap stimulus traces, as do many neurons in closely allied areas such as the frontal eye fields the SC and extrastriate area V3A. Remapping is not purely a cortical phenomenon. Stimulus traces are remapped from one hemifield to the other even when direct cortico-cortical connections are removed. The neural circuitry that produces remapping is distinguished by significant plasticity, suggesting that updating of salient stimuli is fundamental for spatial stability and visuospatial behaviour. These findings provide new evidence that a unified and stable representation of visual space is constructed by redundant circuitry, comprising cortical and subcortical pathways, with a remarkable capacity for reorganization.     

Human Left Ventral Premotor Cortex Mediates Matching of Hand Posture to Object Use

Visuomotor transformations for grasping have been associated with a fronto-parietal network in the monkey brain. The human homologue of the parietal monkey region (AIP) has been identified as the anterior part of the intraparietal sulcus (aIPS), whereas the putative human equivalent of the monkey frontal region (F5) is located in the ventral part of the premotor cortex (vPMC). Results from animal studies suggest that monkey F5 is involved in the selection of appropriate hand postures relative to the constraints of the task. In humans, the functional roles of aIPS and vPMC appear to be more complex and the relative contribution of each region to grasp selection remains uncertain. The present study aimed to identify modulation in brain areas sensitive to the difficulty level of tool object - hand posture matching. Seventeen healthy right handed participants underwent fMRI while observing pictures of familiar tool objects followed by pictures of hand postures. The task was to decide whether the hand posture matched the functional use of the previously shown object. Conditions were manipulated for level of difficulty. Compared to a picture matching control task, the tool object – hand posture matching conditions conjointly showed increased modulation in several left hemispheric regions of the superior and inferior parietal lobules (including aIPS), the middle occipital gyrus, and the inferior temporal gyrus. Comparison of hard versus easy conditions selectively modulated the left inferior frontal gyrus with peak activity located in its opercular part (Brodmann area (BA) 44). We suggest that in the human brain, vPMC/BA44 is involved in the matching of hand posture configurations in accordance with visual and functional demands.