Daniela Bonino

Neural correlates of spatial working memory in humans: A functional magnetic resonance imaging study comparing visual and tactile processes

Recent studies of neural correlates of working memory components have identified both low-level perceptual processes and higher-order supramodal mechanisms through which sensory information can be integrated and manipulated. In addition to the primary sensory cortices, working memory relies on a widely distributed neural system of higher-order association areas that includes posterior parietal and occipital areas, and on prefrontal cortex for maintaining and manipulating information. The present study was designed to determine brain patterns of neural response to the same spatial working memory task presented either visually or in a tactile format, and to evaluate the relationship between spatial processing in the visual and tactile sensory modalities. Brain activity during visual and tactile spatial working memory tasks was measured in six young right-handed healthy male volunteers by using functional magnetic resonance imaging. Results indicated that similar fronto-parietal networks were recruited during spatial information processing across the two sensory modalities-specifically the posterior parietal cortex, the dorsolateral prefrontal cortex and the anterior cingulate cortex. These findings provide a neurobiological support to behavioral observations by indicating that common cerebral regions subserve generation of higher order mental representations involved in working memory independently from a specific sensory modality.

Imagery and spatial processes in blindness and visual impairment.

The objective of this review is to examine and evaluate recent findings on cognitive functioning (in particular imagery processes) in individuals with congenital visual impairments, including total blindness, low-vision and monocular vision. As one might expect, the performance of blind individuals in many behaviours and tasks requiring imagery can be inferior to that of sighted subjects; however, surprisingly often this is not the case. Interestingly, there is evidence that the blind often employ different cognitive mechanisms than sighted subjects, suggesting that compensatory mechanisms can overcome the limitations of sight loss. Taken together, these studies suggest that the nature of perceptual input on which we commonly rely strongly affects the organization of our mental processes. We also review recent neuroimaging studies on the neural correlates of sensory perception and mental imagery in visually impaired individuals that have cast light on the plastic functional reorganization mechanisms associated with visual deprivation.

Do We Really Need Vision? How Blind People “See” the Actions of Others

Observing and learning actions and behaviors from others, a mechanism crucial for survival and social interaction, engages the mirror neuron system. To determine whether vision is a necessary prerequisite for the human mirror system to develop and function, we used functional magnetic resonance imaging to compare brain activity in congenitally blind individuals during the auditory presentation of hand-executed actions or environmental sounds, and the motor pantomime of manipulation tasks, with that in sighted volunteers, who additionally performed a visual action recognition task. Congenitally blind individuals activated a premotor–temporoparietal cortical network in response to aurally presented actions that overlapped both with mirror system areas found in sighted subjects in response to visually and aurally presented stimuli, and with the brain response elicited by motor pantomime of the same actions. Furthermore, the mirror system cortex showed a significantly greater response to motor familiar than to unfamiliar action sounds in both sighted and blind individuals. Thus, the mirror system in humans can develop in the absence of sight. The results in blind individuals demonstrate that the sound of an action engages the mirror system for action schemas that have not been learned through the visual modality and that this activity is not mediated by visual imagery. These findings indicate that the mirror system is based on supramodal sensory representations of actions and, furthermore, that these abstract representations allow individuals with no visual experience to interact effectively with others.

Mind the blind brain to understand the sighted one! Is there a supramodal cortical functional architecture?

While most of the research in blind individuals classically has focused on the compensatory plastic rearrangements that follow loss of sight, novel behavioral, anatomical and functional brain studies in individuals born deprived of sight represent a powerful tool to understand to what extent the brain functional architecture is programmed to develop independently from any visual experience. Here we review work from our lab and others, conducted in sighted and congenitally blind individuals, whose results indicate that vision is not a mandatory prerequisite for the brain cortical organization to develop and function. Similar cortical networks subtend visual and/or non-visual perception of form, space and movement, as well as action recognition, both in sighted and in congenitally blind individuals. These findings support the hypothesis of a modality independent, supramodal cortical organization. Visual experience, however, does play a role in shaping specific cortical sub-regions, as loss of sight is accompanied also by cross-modal plastic phenomena. Altogether, studying the blind brain is opening our eyes on how the brain develops and works.

Increased BOLD Variability in the Parietal Cortex and Enhanced Parieto-Occipital Connectivity during Tactile Perception in Congenitally Blind Individuals

Previous studies in early blind individuals posited a possible role of parieto-occipital connections in conveying nonvisual information to the visual occipital cortex. As a consequence of blindness, parietal areas would thus become able to integrate a greater amount of multimodal information than in sighted individuals. To verify this hypothesis, we compared fMRI-measured BOLD signal temporal variability, an index of efficiency in functional information integration, in congenitally blind and sighted individuals during tactile spatial discrimination and motion perception tasks. In both tasks, the BOLD variability analysis revealed many cortical regions with a significantly greater variability in the blind as compared to sighted individuals, with an overlapping cluster located in the left inferior parietal/anterior intraparietal cortex. A functional connectivity analysis using this region as seed showed stronger correlations in both tasks with occipital areas in the blind as compared to sighted individuals. As BOLD variability reflects neural integration and processing efficiency, these cross-modal plastic changes in the parietal cortex, even if described in a limited sample, reinforce the hypothesis that this region may play an important role in processing nonvisual information in blind subjects and act as a hub in the cortico-cortical pathway from somatosensory cortex to the reorganized occipital areas.

Functional inhibition of the human middle temporal cortex affects non-visual motion perception: a repetitive transcranial magnetic stimulation study during tactile speed discrimination

The visual motion-responsive middle temporal complex (hMT+) is activated during tactile and aural motion discrimination in both sighted and congenitally blind individuals, suggesting a supramodal organization of this area. Specifically, non-visual motion processing has been found to activate the more anterior portion of the hMT+. In the present study, repetitive transcranial magnetic stimulation (rTMS) was used to determine whether this more anterior portion of hMT+ truly plays a functional role in tactile motion processing. Sixteen blindfolded, young, healthy volunteers were asked to detect changes in the rotation velocity of a random Braille-like dot pattern by using the index or middle finger of their right hand. rTMS was applied for 600 ms (10 Hz, 110% motor threshold), 200 ms after the stimulus onset with a figure-of-eight coil over either the anterior portion of hMT+ or a midline parieto-occipital site (as a control). Accuracy and reaction times were significantly impaired only when TMS was applied on hMT+, but not on the control area. These results indicate that the recruitment of hMT+ is necessary for tactile motion processing, and thus corroborate the hypothesis of a ‘supramodal’ functional organization for this sensory motion processing area.

Beyond motor scheme: a supramodal distributed representation in the action-observation network.

The representation of actions within the action-observation network is thought to rely on a distributed functional organization. Furthermore, recent findings indicate that the action-observation network encodes not merely the observed motor act, but rather a representation that is independent from a specific sensory modality or sensory experience. In the present study, we wished to determine to what extent this distributed and ‘more abstract’ representation of action is truly supramodal, i.e. shares a common coding across sensory modalities. To this aim, a pattern recognition approach was employed to analyze neural responses in sighted and congenitally blind subjects during visual and/or auditory presentation of hand-made actions. Multivoxel pattern analyses-based classifiers discriminated action from non-action stimuli across sensory conditions (visual and auditory) and experimental groups (blind and sighted). Moreover, these classifiers labeled as ‘action’ the pattern of neural responses evoked during actual motor execution. Interestingly, discriminative information for the action/non action classification was located in a bilateral, but left-prevalent, network that strongly overlaps with brain regions known to form the action-observation network and the human mirror system. The ability to identify action features with a multivoxel pattern analyses-based classifier in both sighted and blind individuals and independently from the sensory modality conveying the stimuli clearly supports the hypothesis of a supramodal, distributed functional representation of actions, mainly within the action-observation network.

The effects of visual control and distance in modulating peripersonal spatial representation.

In the presence of vision, finalized motor acts can trigger spatial remapping, i.e., reference frames transformations to allow for a better interaction with targets. However, it is yet unclear how the peripersonal space is encoded and remapped depending on the availability of visual feedback and on the target position within the individual’s reachable space, and which cerebral areas subserve such processes. Here, functional magnetic resonance imaging (fMRI) was used to examine neural activity while healthy young participants performed reach-to-grasp movements with and without visual feedback and at different distances of the target from the effector (near to the hand–about 15 cm from the starting position–vs. far from the hand–about 30 cm from the starting position). Brain response in the superior parietal lobule bilaterally, in the right dorsal premotor cortex, and in the anterior part of the right inferior parietal lobule was significantly greater during visually-guided grasping of targets located at the far distance compared to grasping of targets located near to the hand. In the absence of visual feedback, the inferior parietal lobule exhibited a greater activity during grasping of targets at the near compared to the far distance. Results suggest that in the presence of visual feedback, a visuo-motor circuit integrates visuo-motor information when targets are located farther away. Conversely in the absence of visual feedback, encoding of space may demand multisensory remapping processes, even in the case of more proximal targets.

Neural correlates of human-robot handshaking

Handshaking represents a complex motor and cognitive task that poses several challenges from both engineering and neuroscientific viewpoints. In particular, it is an intriguing application which can be profitably studied in the field of Human Robot Interaction (HRI). In this work an experimental paradigm is proposed to investigate the neural correlates of handshaking between humans and between humans and robots using functional Magnetic Resonance Imaging. More specifically the role of visual and haptic components during handshaking interaction will be studied. A wearable sensing glove will be used to monitor hand finger position and movement. Preliminary results will be reported and discussed.

Functional Exploration Studies of Supramodal Organization in the Human Extrastriate Cortex

In the context of the Touch-Hapsys project, our group investigated whether the two main components of the cortical visual systems, i.e., the ventral ”what” pathway and the dorsal ”where” pathways, are devoted merely to the processing of visual information or rather they are organized in a supramodal fashion, that is, they are able to process information independently from the sensory modality through which such an information reaches the brain. Sighted and congenitally blind individuals underwent fMRI scan examinations while performing distinct visual and/or tactile experimental tasks involving object recognition, movement detection and spatial localization. These functional studies revealed that both sighted subjects and individuals with no previous visual experience rely on these supramodal brain areas of the ventral and dorsal extrastriate cortex to acquire normal knowledge about objects and interact effectively with the surrounding world.