The Brain in (Willed) Action: A Meta-Analytical Comparison of Imaging Studies on Motor Intentionality and Sense of Agency

Voluntary actions can be fractionated in different phenomena: from the emergence of intentions and the ensuing motor plans and actions, to the anticipation and monitoring of their outcomes, to the appreciation of their congruency with intentions and to the eventual emergence of a sense of agency. It follows that motor intention and the sense of agency should occur at different stages in the normal generation of willed actions. Both these processes have been associated with a fronto-parietal motor network, but no study has investigated to what extent the two experiences can be dissociated for the brain regions involved. To this end, we assessed the PET/fMRI literature on agency and intentionality using a meta-analytic technique based on a hierarchical clustering algorithm. Beside a shared brain network involving the meso-frontal and prefrontal regions, the middle insula and subcortical structures, we found that motor intention and the sense of agency are functionally underpinned by separable sets of brain regions: an “intentionality network,” involving the rostral area of the mesial frontal cortex (middle cingulum and pre-supplementary motor area), the anterior insula and the parietal lobules, and a “self-agency network,” which involves the posterior areas of the mesial frontal cortex (the SMA proper), the posterior insula, the occipital lobe and the cerebellum. We were then able to confirm this functional organization by a subsequent seed-based fMRI resting-state functional connectivity analysis, with seeds derived from the intentionality/sense of agency specific clusters of the medial wall of the frontal lobe. Our results suggest the existence of a rostro-caudal gradient within the mesial frontal cortex, with the more anterior regions linked to the concept of motor intentionality and the brain areas located more posteriorly associated with the direct monitoring between the action and its outcome. This suggestion is reinforced by the association between the sense of agency and the activation of the occipital lobes, to suggest a direct comparison between the movement and its external (e.g., visual) consequences. The shared network may be important for the integration of intentionality and agency in a coherent appreciation of self-generated actions

Anatomical Modularity of Verbal Working Memory? Functional Anatomical Evidence from a Famous Patient with Short-Term Memory Deficits

Cognitive skills are the emergent property of distributed neural networks. The distributed nature of these networks does not necessarily imply a lack of specialization of the individual brain structures involved. However, it remains questionable whether discrete aspects of high-level behavior might be the result of localized brain activity of individual nodes within such networks. The phonological loop of working memory, with its simplicity, seems ideally suited for testing this possibility. Central to the development of the phonological loop model has been the description of patients with focal lesions and specific deficits. As much as the detailed description of their behavior has served to refine the phonological loop model, a classical anatomoclinical correlation approach with such cases falls short in telling whether the observed behavior is based on the functions of a neural system resembling that seen in normal subjects challenged with phonological loop tasks or whether different systems have taken over. This is a crucial issue for the cross correlation of normal cognition, normal physiology, and cognitive neuropsychology. Here we describe the functional anatomical patterns of JB, a historical patient originally described by Warrington et al. (1971), a patient with a left temporo-parietal lesion and selective short phonological store deficit. JB was studied with the H215O PET activation technique during a rhyming task, which primarily depends on the rehearsal system of the phonological loop. No residual function was observed in the left temporo-parietal junction, a region previously associated with the phonological buffer of working memory. However, Broca's area, the major counterpart of the rehearsal system, was the major site of activation during the rhyming task. Specific and autonomous activation of Broca's area in the absence of afferent inputs from the other major anatomical component of the phonological loop shows that a certain degree of functional independence or modularity exists in this distributed anatomical-cognitive system

Neural Correlates of Body Integrity Dysphoria

There are few things as irrefutable as the evidence that our limbs belong to us. However, persons with body integrity dysphoria (BID) [1] deny the ownership of one of their fully functional limbs and seek its amputation [2]. We tapped into the brain mechanisms of BID, examining sixteen men desiring the removal of the left healthy leg. The primary sensorimotor area of the to-be-removed leg and the core area of the conscious representation of body size and shape (the right superior parietal lobule [rSPL]) [3, 4] were less functionally connected to the rest of the brain. Furthermore, the left premotor cortex, reportedly involved in the multisensory integration of limb information [5-7], and the rSPL were atrophic. The more atrophic the rSPL, the stronger the desire for amputation, and the more an individual pretended to be an amputee by using wheelchairs or crutches to solve the mismatch between the desired and actual body. Our findings illustrate the pivotal role of the connectivity of the primary sensorimotor limb area in the mediation of the feeling of body ownership. They also delineate the morphometric and functional alterations in areas of higher-order body representation possibly responsible for the dissatisfaction with a standard body configuration. The neural correlates of BID may foster the understanding of other neuropsychiatric disorders involving the bodily self. Ultimately, they may help us understand what most of us take for granted, i.e., the experience of body and self as a seamless unity

Brain Abnormalities in Individuals with a Desire for a Healthy Limb Amputation: Somatosensory, Motoric or Both? A Task-Based fMRI Verdict

Body integrity dysphoria (BID), a long-lasting desire for the amputation of physically healthy limbs, is associated with reduced fMRI resting-state functional connectivity of somatosensory cortices. Here, we used fMRI to evaluate whether these findings could be replicated and expanded using a task-based paradigm. We measured brain activations during somatosensory stimulation and motor tasks for each of the four limbs in ten individuals with a life-long desire for the amputation of the left leg and fourteen controls. For the left leg, BID individuals had reduced brain activation in the right superior parietal lobule for somatosensory stimulation and in the right paracentral lobule for the motor task, areas where we previously found reduced resting-state functional connectivity. In addition, for somatosensory stimulation only, we found a robust reduction in activation of somatosensory areas SII bilaterally, mostly regardless of the stimulated body part. Areas SII were regions of convergent activations for signals from all four limbs in controls to a significantly greater extent than in subjects with BID. We conclude that BID is associated with altered integration of somatosensory and, to a lesser extent, motor signals, involving limb-specific cortical maps and brain regions where the first integration of body-related signals is achieved through convergence

The What, the When, and the Whether of Intentional Action in the Brain: A Meta-Analytical Review

In their attempt to define discrete subcomponents of intentionality, Brass and Haggard (2008) proposed their What, When, and Whether model (www-model) which postulates that the content, the timing and the possibility of generating an action can be partially independent both at the cognitive level and at the level of their neural implementation. The original proposal was based on a limited number of studies, which were reviewed with a discursive approach. To assess whether the model stands in front of the more recently published data, we performed a systematic review of the literature with a meta-analytic method based on a hierarchical clustering (HC) algorithm. We identified 15 PET/fMRI studies well-suited for this quest. HC revealed the existence of a rostro-caudal gradient within the medial prefrontal cortex, with the more anterior regions (the anterior cingulum) involved in more abstract decisions of whether to execute an action and the more posterior ones (the middle cingulum or the SMA) recruited in specifying the content and the timing components of actions. However, in contrast with the original www-model, this dissociation involves also brain regions well outside the median wall of the frontal lobe, in a component specific manner: the supramarginal gyrus for the what component, the pallidum and the thalamus for the when component, the putamen and the insula for the whether component. We then calculated co-activation maps on the three component-specific www clusters of the medial wall of the frontal/limbic lobe: to this end, we used the activation likelihood approach that we applied on the imaging studies on action contained in the BrainMap.org database. This analysis confirmed the main findings of the HC analyses. However, the BrainMap.org data analyses also showed that the aforementioned segregations are generated by paradigms in which subjects act in response to conditional stimuli rather than while driven by their own intentions. We conclude that the available data confirm that the neural underpinnings of intentionality can be fractionated in discrete components that are partially independent. We also suggest that intentionality manifests itself in discrete components through the boosting of general purpose action-related regions specialized for different aspects of action selection and inhibition

Effects of Orthographic Consistency on Bilingual Reading: Human and Computer Simulation Data

English serves as today’s lingua franca, a role not eased by the inconsistency of its orthography. Indeed, monolingual readers of more consistent orthographies such as Italian or German learn to read more quickly than monolingual English readers. Here, we assessed whether long-lasting bilingualism would mitigate orthography-specific differences in reading speed and whether the order in which orthographies with a different regularity are learned matters. We studied high-proficiency Italian-English and English-Italian bilinguals, with at least 20 years of intensive daily exposure to the second language and its orthography and we simulated sequential learning of the two orthographies with the CDP++ connectionist model of reading. We found that group differences in reading speed were comparatively bigger with Italian stimuli than with English stimuli. Furthermore, only Italian bilinguals took advantage of a blocked presentation of Italian stimuli compared to when stimuli from both languages were presented in mixed order, suggesting a greater ability to keep language-specific orthographic representations segregated. These findings demonstrate orthographic constraints on bilingual reading, whereby the level of consistency of the first learned orthography affects later learning and performance on a second orthography. The computer simulations were consistent with these conclusions