Communicative And Affective Components in Processing Auditory Vitality Forms: An fMRI Study.

In previous studies on auditory vitality forms, we found that listening to action verbs pronounced gently or rudely, produced, relative to a neutral robotic voice, activation of the dorso-central insula. One might wonder whether this insular activation depends on the conjunction of action verbs and auditory vitality forms, or whether auditory vitality forms are sufficient per se to activate the insula. To solve this issue, we presented words not related to actions such as concrete nouns (e.g.,"ball"), pronounced gently or rudely. No activation of the dorso-central insula was found. As a further step, we examined whether interjections, i.e., speech stimuli conveying communicative intention (e.g., "hello"), pronounced with different vitality forms, would be able to activate, relative to control, the insula. The results showed that stimuli conveying a communicative intention, pronounced with different auditory vitality forms activate the dorsal-central insula. These data deepen our understanding of the vitality forms processing, showing that insular activation is not specific to action verbs, but can be also activated by speech acts conveying communicative intention such as interjections. These findings also show the intrinsic social nature of vitality forms because activation of the insula was not observed in the absence of a communicative intention.

The middle cingulate cortex and dorso-central insula: A mirror circuit encoding observation and execution of vitality forms.

Actions with identical goals can be executed in different ways (gentle, rude, vigorous, etc.), which D. N. Stern called vitality forms [D. N. Stern, Forms of Vitality Exploring Dynamic Experience in Psychology, Arts, Psychotherapy, and Development (2010)]. Vitality forms express the agent's attitudes toward others. In a series of fMRI studies, we found that the dorso-central insula (DCI) is the region that is selectively active during both vitality form observation and execution. In one previous experiment, however, the middle cingulate gyrus also exhibited activation. In the present study, in order to assess the role of the cingulate cortex in vitality form processing, we adopted a classical vitality form paradigm, but making the control condition devoid of vitality forms using jerky movements. Participants performed two different tasks: Observation of actions performed gently or rudely and execution of the same actions. The results showed that in addition to the insula, the middle cingulate cortex (MCC) was strongly activated during both action observation and execution. Using a voxel-based analysis, voxels showing a similar trend of the blood-oxygen-level-dependent (BOLD) signal in both action observation and execution were found in the DCI and in the MCC. Finally, using a multifiber tractography analysis, we showed that the active sites in MCC and DCI are reciprocally connected.

The neural bases of tactile vitality forms and their modulation by social context.

People communicate using speech, gestures, and, less frequently, touches. An example of tactile communication is represented by handshake. Customs surrounding handshake vary in different cultures. In Western societies is mostly used when meeting, parting, as a sign of congratulations or at the end of a successful business. Despite its importance in social life, the neural mechanism underlying the affective components conveyed by handshake ("tactile vitality forms") is unknown. Here we combined functional magnetic resonance imaging (fMRI) and electromyography (EMG), to investigate the neural affective activations during handshakes. We demonstrated that handshake conveying gentle or aggressive tactile vitality forms produces a stronger activation of the dorso-central insula. The simultaneous presence of emotional facial expressions modulates the activation of this insular sector. Finally, we provide evidence that the cingulate cortex is involved in the processing of facial expressions conveying different vitality forms.

Two Neural Networks for Laughter: A Tractography Study.

Laughter is a complex motor behavior occurring in both emotional and nonemotional contexts. Here, we investigated whether the different functions of laughter are mediated by distinct networks and, if this is the case, which are the white matter tracts sustaining them. We performed a multifiber tractography investigation placing seeds in regions involved in laughter production, as identified by previous intracerebral electrical stimulation studies in humans: the pregenual anterior cingulate (pACC), ventral temporal pole (TPv), frontal operculum (FO), presupplementary motor cortex, and ventral striatum/nucleus accumbens (VS/NAcc). The primary motor cortex (M1) and two subcortical territories were also studied to trace the descending projections. Results provided evidence for the existence of two relatively distinct networks. A first network, including pACC, TPv, and VS/NAcc, is interconnected through the anterior cingulate bundle, the accumbofrontal tract, and the uncinate fasciculus, reaching the brainstem throughout the mamillo-tegmental tract. This network is likely involved in the production of emotional laughter. A second network, anchored to FO and M1, projects to the brainstem motor nuclei through the internal capsule. It is most likely the neural basis of nonemotional and conversational laughter. The two networks interact throughout the pre-SMA that is connected to both pACC and FO.

Understanding the attitude of others by hearing action sounds: the role of the insula.

During social interactions, actions and words can be expressed in different ways, for example gently, vigorously or rudely communicating the positive or negative attitude of the agent. These forms of communication are called vitality forms and play a crucial role in social relations. While the neural bases of speech and actions vitality forms have been investigated, there is no information on how we recognize others' mood/attitude by hearing the sound of their actions. In the present fMRI study we investigated the neural basis of vitality forms while participants heard action sounds in two different conditions: sounds resulting from gentle and rude actions, sounds communicating the same actions without vitality forms (control stimuli). Results showed that hearing action sounds conveying rude and gentle vitality forms respect to the control stimuli produced a specific activation of the dorso-central insula. In addition, hearing both vitality forms action sounds and control stimuli produced the activation of the parieto-frontal circuit typically involved in the observation and the execution of arm actions. In conclusion, our data indicate that, the dorso-central insula is a key region involved in the processing of vitality forms regardless of the modality by which they are conveyed.

Insula Connections With the Parieto-Frontal Circuit for Generating Arm Actions in Humans and Macaque Monkeys.

It has been recently found that the human dorso-central insular cortex contributes to the execution and recognition of the affective component of hand actions, most likely through modulation of the activity of the parieto-frontal circuits. While the anatomical connections between the hand representation of the insula and, the parietal and frontal regions controlling reaching/grasping actions is well assessed in the monkey, it is unknown the existence of a homolog circuit in humans. In the present study, we performed a multifiber tractography investigation to trace the tracts possibly connecting the insula to the parieto-frontal circuits by locating seeds in the parietal, premotor, and prefrontal nodes of the reaching/grasping network, in both humans and monkeys. Results showed that, in both species, the insula is connected with the cortical action execution/recognition circuit by similar white matter tracts, running in parallel to the third branch of the superior longitudinal fasciculus and the anterior segment of the arcuate fasciculus.

Mirroring the Social Aspects of Speech and Actions: The Role of the Insula.

Action and speech may take different forms, being expressed, for example, gently or rudely. These aspects of social communication, named vitality forms, have been little studied in neuroscience. In the present functional magnetic resonance imaging study, we investigated the role of insula in processing action and speech vitality forms. In speech runs, participants were asked to listen or imaging themselves to pronounce action verbs gently or rudely. In action runs, they were asked to observe or imaging themselves to perform actions gently or rudely. The results showed that, relative to controls, there was an activation of the dorso-central insula in both tasks of speech and action runs. The insula sector specific for action vitality form was located slightly more dorsally than that of speech with a large overlap of their activations. The psycho-physiological interaction analysis showed that the insular sector involved in action vitality forms processing is connected with the left hemisphere areas controlling arm actions, whereas the sector involved in speech vitality forms processing is linked with right hemisphere areas related to speech prosody. We conclude that the central part of the insula is a key region for vitality forms processing regardless of the modality by which they are conveyed or expressed.

Multiple time courses of somatosensory responses in human cortex.

Here we show how anatomical and functional data recorded from patients undergoing stereo-EEG can be used to decompose the cortical processing following nerve stimulation in different stages characterized by specific topography and time course. Tibial, median and trigeminal nerves were stimulated in 96 patients, and the increase in gamma power was evaluated over 11878 cortical sites. All three nerve datasets exhibited similar clusters of time courses: phasic, delayed/prolonged and tonic, which differed in topography, temporal organization and degree of spatial overlap. Strong phasic responses of the three nerves followed the classical somatotopic organization of SI, with no overlap in either time or space. Delayed responses presented overlaps between pairs of body parts in both time and space, and were confined to the dorsal motor cortices. Finally, tonic responses occurred in the perisylvian region including posterior insular cortex and were evoked by the stimulation of all three nerves, lacking any spatial and temporal specificity. These data indicate that the somatosensory processing following nerve stimulation is a multi-stage hierarchical process common to all three nerves, with the different stages likely subserving different functions. While phasic responses represent the neural basis of tactile perception, multi-nerve tonic responses may represent the neural signature of processes sustaining the capacity to become aware of tactile stimuli.

Decomposing Tool-Action Observation: A Stereo-EEG Study.

A description of the spatiotemporal dynamics of human cortical activity during cognitive tasks is a fundamental goal of neuroscience. In the present study, we employed stereo-EEG in order to assess the neural activity during tool-action observation. We recorded from 49 epileptic patients (5502 leads) implanted with intracerebral electrodes, while they observed tool and hand actions. We deconstructed actions into 3 events-video onset, action onset, and tool-object contact-and assessed how different brain regions respond to these events. Video onset, with actions not yet visible, recruited only visual areas. Aligning the responses at action onset, yielded activity in the parietal-frontal manipulation circuit and, selectively for tool actions, in the left anterior supramarginal gyrus (aSMG). Finally, by aligning to the tool-object contact that signals the achievement of the main goal of the observed action, activations were found in SII and dorsal premotor cortex. In conclusion, our data show that during tool-action observation, in addition to the general action observation network there is a selective activation of aSMG, which exhibits internally different patterns of responsiveness. In addition, neural responses selective for the contact between the tool and the object were also observed.

Understanding the internal states of others by listening to action verbs.

The internal state of others can be understood observing their actions or listening to their voice. While the neural bases of action style (vitality forms) have been investigated, there is no information on how we recognize others' internal state by listening to their speech. Here, using fMRI technique, we investigated the neural correlates of auditory vitality forms while participants listened to action verbs in three different conditions: human voice pronouncing the verbs in a rude and gentle way, robot voice pronouncing the same verbs without vitality forms, and a scrambled version of the same verbs pronounced by human voice. In agreement with previous studies on vitality forms encoding, we found specific activation of the central part of insula during listening to human voice conveying specific vitality forms. In addition, when listening both to human and robot voices there was an activation of the posterior part of the left inferior frontal gyrus and of the parieto-premotor circuit typically described to be activated during observation and execution of arm actions. Finally, the superior temporal gyrus was activated bilaterally in all three conditions. We conclude that, the central part of insula is a key region for vitality forms processing allowing the understanding of the vitality forms regardless of the modality by which they are conveyed.

Stereoscopically Observing Manipulative Actions.

The purpose of this study was to investigate the contribution of stereopsis to the processing of observed manipulative actions. To this end, we first combined the factors "stimulus type" (action, static control, and dynamic control), "stereopsis" (present, absent) and "viewpoint" (frontal, lateral) into a single design. Four sites in premotor, retro-insular (2) and parietal cortex operated specifically when actions were viewed stereoscopically and frontally. A second experiment clarified that the stereo-action-specific regions were driven by actions moving out of the frontoparallel plane, an effect amplified by frontal viewing in premotor cortex. Analysis of single voxels and their discriminatory power showed that the representation of action in the stereo-action-specific areas was more accurate when stereopsis was active. Further analyses showed that the 4 stereo-action-specific sites form a closed network converging onto the premotor node, which connects to parietal and occipitotemporal regions outside the network. Several of the specific sites are known to process vestibular signals, suggesting that the network combines observed actions in peripersonal space with gravitational signals. These findings have wider implications for the function of premotor cortex and the role of stereopsis in human behavior.

A human homologue of monkey F5c.

Area F5c is a monkey premotor area housing mirror neurons which responds more strongly to grasping observation when the actor is visible than when only the actor's hand is visible. Here we used this characteristic fMRI signature of F5c in seven imaging experiments - one in macaque monkeys and six in humans - to identify the human homologue of monkey F5c. By presenting the two grasping actions (actor, hand) and varying the low level visual characteristics, we localized a putative human homologue of area F5c (phF5c) in the inferior part of precentral sulcus, bilaterally. In contrast to monkey F5c, phF5c is asymmetric, with a right-sided bias, and is activated more strongly during the observation of the later stages of grasping when the hand is close to the object. The latter characteristic might be related to the emergence, in humans, of the capacity to precisely copy motor acts performed by others, and thus imitation.

The representation of tool use in humans and monkeys: common and uniquely human features.

Though other species of primates also use tools, humans appear unique in their capacity to understand the causal relationship between tools and the result of their use. In a comparative fMRI study, we scanned a large cohort of human volunteers and untrained monkeys, as well as two monkeys trained to use tools, while they observed hand actions and actions performed using simple tools. In both species, the observation of an action, regardless of how performed, activated occipitotemporal, intraparietal, and ventral premotor cortex, bilaterally. In humans, the observation of actions done with simple tools yielded an additional, specific activation of a rostral sector of the left inferior parietal lobule (IPL). This latter site was considered human-specific, as it was not observed in monkey IPL for any of the tool videos presented, even after monkeys had become proficient in using a rake or pliers through extensive training. In conclusion, while the observation of a grasping hand activated similar regions in humans and monkeys, an additional specific sector of IPL devoted to tool use has evolved in Homo sapiens, although tool-specific neurons might reside in the monkey grasping regions. These results shed new light on the changes of the hominid brain during evolution.

When pliers become fingers in the monkey motor system.

The capacity to use tools is a fundamental evolutionary achievement. Its essence stands in the capacity to transfer a proximal goal (grasp a tool) to a distal goal (e.g., grasp food). Where and how does this goal transfer occur? Here, we show that, in monkeys trained to use tools, cortical motor neurons, active during hand grasping, also become active during grasping with pliers, as if the pliers were now the hand fingers. This motor embodiment occurs both for normal pliers and for "reverse pliers," an implement that requires finger opening, instead of their closing, to grasp an object. We conclude that the capacity to use tools is based on an inherently goal-centered functional organization of primate cortical motor areas.

The anthropomorphic brain: the mirror neuron system responds to human and robotic actions.

In humans and monkeys the mirror neuron system transforms seen actions into our inner representation of these actions. Here we asked if this system responds also if we see an industrial robot perform similar actions. We localised the motor areas involved in the execution of hand actions, presented the same subjects blocks of movies of humans or robots perform a variety of actions. The mirror system was activated strongly by the sight of both human and robotic actions, with no significant differences between these two agents. Finally we observed that seeing a robot perform a single action repeatedly within a block failed to activate the mirror system. This latter finding suggests that previous studies may have failed to find mirror activations to robotic actions because of the repetitiveness of the presented actions. Our findings suggest that the mirror neuron system could contribute to the understanding of a wider range of actions than previously assumed, and that the goal of an action might be more important for mirror activations than the way in which the action is performed.

Listening to action-related sentences modulates the activity of the motor system: a combined TMS and behavioral study.

Transcranial magnetic stimulation (TMS) and a behavioral paradigm were used to assess whether listening to action-related sentences modulates the activity of the motor system. By means of single-pulse TMS, either the hand or the foot/leg motor area in the left hemisphere was stimulated in distinct experimental sessions, while participants were listening to sentences expressing hand and foot actions. Listening to abstract content sentences served as a control. Motor evoked potentials (MEPs) were recorded from hand and foot muscles. Results showed that MEPs recorded from hand muscles were specifically modulated by listening to hand-action-related sentences, as were MEPs recorded from foot muscles by listening to foot-action-related sentences. This modulation consisted of an amplitude decrease of the recorded MEPs. In the behavioral task, participants had to respond with the hand or the foot while listening to actions expressing hand and foot actions, as compared to abstract sentences. Coherently with the results obtained with TMS, when the response was given with the hand, reaction times were slower during listening to hand-action-related sentences, while when the response was given with the foot, reaction times were slower during listening to foot-action-related sentences. The present data show that processing verbally presented actions activates different sectors of the motor system, depending on the effector used in the listened-to action.

Reafferent copies of imitated actions in the right superior temporal cortex.

Imitation is a complex phenomenon, the neural mechanisms of which are still largely unknown. When individuals imitate an action that already is present in their motor repertoire, a mechanism matching the observed action onto an internal motor representation of that action should suffice for the purpose. When one has to copy a new action, however, or to adjust an action present in one's motor repertoire to a different observed action, an additional mechanism is needed that allows the observer to compare the action made by another individual with the sensory consequences of the same action made by himself. Previous experiments have shown that a mechanism that directly matches observed actions on their motor counterparts exists in the premotor cortex of monkeys and humans. Here we report the results of functional magnetic resonance experiments, suggesting that in the superior temporal sulcus, a higher order visual region, there is a sector that becomes active both during hand action observation and during imitation even in the absence of direct vision of the imitator's hand. The motor-related activity is greater during imitation than during control motor tasks. This newly identified region has all the requisites for being the region at which the observed actions, and the reafferent motor-related copies of actions made by the imitator, interact.

The cortical motor system.

The cortical motor system of primates is formed by a mosaic of anatomically and functionally distinct areas. These areas are not only involved in motor functions, but also play a role in functions formerly attributed to higher order associative cortical areas. In the present review, we discuss three types of higher functions carried out by the motor cortical areas: sensory-motor transformations, action understanding, and decision processing regarding action execution. We submit that generating internal representations of actions is central to cortical motor function. External contingencies and motivational factors determine then whether these action representations are transformed into actual actions.

I know what you are doing. a neurophysiological study.

In the ventral premotor cortex of the macaque monkey, there are neurons that discharge both during the execution of hand actions and during the observation of the same actions made by others (mirror neurons). In the present study, we show that a subset of mirror neurons becomes active during action presentation and also when the final part of the action, crucial in triggering the response in full vision, is hidden and can therefore only be inferred. This implies that the motor representation of an action performed by others can be internally generated in the observer's premotor cortex, even when a visual description of the action is lacking. The present findings support the hypothesis that mirror neuron activation could be at the basis of action recognition.