Emiliano Macaluso

Spatial attention and crossmodal interactions between vision and touch

In the present paper, we review several functional imaging studies investigating crossmodal interactions between vision and touch relating to spatial attention. We asked how the spatial unity of a multimodal event in the external world might be represented in the brain, where signals from different modalities are initially processed in distinct brain regions. The results highlight several links between visual and tactile spatial representations. First, we found that activity in the anterior part of the intraparietal sulcus was influenced by stimulus position independently of the modality of the stimulation. This is consistent with crossmodal interactions via sensory convergence from early modality-specific spatial maps to higher-order multimodal regions. Second, we found that stimulation in, or attention to, one modality could affect activity in areas dedicated to a different modality, in a spatially-specific manner. These spatial crossmodal effects in unimodal regions demonstrate congruous activity in anatomically distant brain areas that represent similar external locations, implicating a distributed network of spatial representations in crossmodal integration. Finally, the results suggest that the temporo-parietal junction may be involved in aspects of controlling spatial attention, for both vision and touch. A multimodal attentional system may influence activity in distinct brain areas representing common regions of space for different modalities, thus suggesting a link between spatial attention and crossmodal integration.

The Functional Neuroanatomy of Temporal Discrimination

Two identical stimuli, such as a pair of electrical shocks to the skin, are readily perceived as two separate events in time provided the interval between them is sufficiently long. However, as they are presented progressively closer together, there comes a point when the two separate stimuli are perceived as a single stimulus. Damage to posterior parietal cortex, peri-supplementary motor area (peri-SMA), and basal ganglia can disturb this form of temporal discrimination. Our aim was to establish, in healthy subjects, the brain areas that are involved in this process. During functional magnetic resonance imaging scanning, paired electrical pulses, separated by variable inter-stimulus intervals (5-110 msec), were delivered to different sites on one forearm (8-64 mm from the midline). Subjects were required to simply detect the stimulus (control task) or to identify a stimulus property. For temporal discrimination (TD), subjects reported whether they felt one or two stimuli. For spatial discrimination, they reported whether the stimuli were located on the right or left side of the forearm. Subjects reported their choice by pressing a button with the opposite hand. Our results showed that discrimination, as opposed to simply detection, activated several brain areas. Most were common to both discrimination tasks. These included regions of prefrontal cortex, right postcentral gyrus and inferior parietal lobule, basal ganglia, and cerebellum. However, activation of pre-SMA and anterior cingulate was found to be specific to the TD task. This suggests that these two frontal regions may play a role in the temporal processing of somatosensory events.

Supramodal Effects of Covert Spatial Orienting Triggered by Visual or Tactile Events

Event-related functional magnetic resonance imaging was used to identify brain areas involved in spatial attention and determine whether these operate unimodally or supramodally for vision and touch. On a trial-by-trial basis, a symbolic auditory cue indicated the most likely side for the subsequent target, thus directing covert attention to one side. A subsequent target appeared in vision or touch on the cued or uncued side. Invalidly cued trials (as compared with valid trials) activated the temporo-parietal junction and regions of inferior frontal cortex, regardless of target modality. These brain areas have been associated with multimodal spatial coding in physiological studies of the monkey brain and were linked to a change in the location that must be attended to in the present study. The intraparietal sulcus and superior frontal cortex were also activated in our task, again, regardless of target modality, but did not show any specificity for invalidly cued trials. These results identify a supramodal network for spatial attention and reveal differential activity for inferior circuits involving the temporo-parietal junction and inferior frontal cortex (specific to invalid trials) versus more superior intraparietal-frontal circuits (common to valid and invalid trials).

A Common Cortical Substrate Activated by Horizontal and Vertical Sound Movement in the Human Brain

Perception of movement in acoustic space depends on comparison of the sound waveforms reaching the two ears (binaural cues) as well as spectrotemporal analysis of the waveform at each ear (monaural cues). The relative importance of these two cues is different for perception of vertical or horizontal motion, with spectrotemporal analysis likely to be more important for perceiving vertical shifts. In humans, functional imaging studies have shown that sound movement in the horizontal plane activates brain areas distinct from the primary auditory cortex, in parietal and frontal lobes and in the planum temporale. However, no previous work has examined activations for vertical sound movement. It is therefore difficult to generalize previous imaging studies, based on horizontal movement only, to multidimensional auditory space perception. Using externalized virtual-space sounds in a functional magnetic resonance imaging (fMRI) paradigm to investigate this, we compared vertical and horizontal shifts in sound location. A common bilateral network of brain areas was activated in response to both horizontal and vertical sound movement. This included the planum temporale, superior parietal cortex, and premotor cortex. Sounds perceived laterally in virtual space were associated with contralateral activation of the auditory cortex. These results demonstrate that sound movement in vertical and horizontal dimensions engages a common processing network in the human cerebral cortex and show that multidimensional spatial properties of sounds are processed at this level.

Neural Basis of Maternal Communication and Emotional Expression Processing during Infant Preverbal Stage

During the first year of life, exchanges and communication between a mother and her infant are exclusively preverbal and are based on the mothers ability to understand her infants needs and feelings (i.e., empathy) and on imitation of the infants facial expressions; this promotes a social dialog that influences the development of the infant self. Sixteen mothers underwent functional magnetic resonance imaging while observing and imitating faces of their own child and those of someone elses child. We found that the mirror neuron system, the insula and amygdala were more active during emotional expressions, that this circuit is engaged to a greater extent when interacting with ones own child, and that it is correlated with maternal reflective function (a measure of empathy). We also found, by comparing single emotions with each other, that joy expressions evoked a response mainly in right limbic and paralimbic areas; by contrast, ambiguous expressions elicited a response in left high order cognitive and motor areas, which might reflect cognitive effort.

The representation of space near the body through touch and vision

This review discusses how visual and the tactile signals are combined in the brain to ensure appropriate interactions with the space around the body. Visual and tactile signals converge in many regions of the brain (e.g. parietal and premotor cortices) where multisensory input can interact on the basis of specific spatial constraints. Crossmodal interactions can modulate also unisensory visual and somatosensory cortices, possibly via feed-back projections from fronto-parietal areas. These processes enable attentional selection of relevant locations in near body space, as demonstrated by studies of spatial attention in healthy volunteers and in neuropsychological patients with crossmodal extinction. These crossmodal spatial effects can be flexibly updated taking into account the position of the eyes and the limbs, thus reflecting the spatial alignment of visuo-tactile stimuli in external space. Further, studies that manipulated vision of body parts (alien, real or fake limbs) have demonstrated that passive viewing of the body can influence the perception of somatosensory stimuli, again involving areas in the premotor and parietal cortices. Finally, we discuss how tool-use can expand the region of visuo-tactile integration in near body space, emphasizing the flexibility of this system at the single-neuron level in the monkeys parietal cortex, with corresponding multisensory effects in normals and neuropsychological patients. We conclude that visuo-tactile crossmodal links dominate the representation of near body space and that this is implemented functionally in parietal and premotor brain regions. These integration processes mediate the orienting of spatial attention and generate an efficient and flexible representation the space around the body.

Grey and White Matter Changes at Different Stages of Alzheimer's Disease

This study investigates abnormalities of grey (GM) and white matter (WM) in Alzheimers disease (AD), by modeling the AD pathological process as a continuous course between normal aging and fully developed dementia, with amnesic mild cognitive impairment (aMCI) as an intermediate stage. All subjects (9 AD, 16 aMCI patients, and 13 healthy controls) underwent a full neuropsychological assessment and an MRI examination at 3 Tesla, including a volumetric scan and diffusion tensor (DT)-MRI. The volumes were processed to perform a voxel-based morphometric analysis of GM and WM volume, while DT-MRI data were analyzed using tract based spatial statistics, to estimate changes in fractional anisotropy and mean diffusivity data. GM and WM volume and mean diffusivity and fractional anisotropy were compared across the three groups, and their correlation with cognitive functions was investigated. While AD presented a pattern of widespread GM atrophy, tissue loss was more subtle in patients with aMCI. WM atrophy was mainly located in the temporal lobe, but evidence of WM microscopic damage, assessed by DT-MRI, was also observable in the thalamic radiations and in the corpus callosum. Memory and executive functions correlated with either GM volume or fractional anisotropy in fronto-temporal areas. In conclusion, this study shows a comprehensive assessment of the brain tissue damage across AD evolution, providing insights on different pathophysiological mechanisms (GM atrophy, Wallerian degeneration, and brain disconnection) and their possible association with clinical aspects of cognitive decline.

Episodic memory impairment in patients with Alzheimer's disease is correlated with entorhinal cortex atrophy: A voxel-based morphometry study

The aims of this study were to investigate the pattern of cortical atrophy and the relationships between memory performances and the brain regions in Alzheimer’s Disease (AD). optimized voxel-based morphometry (VBM) was applied to the MRI brain images of 18 probable AD and 18 healthy subjects (HS). Patients performed verbal and visuo-spatial episodic and shortterm memory tests. Contrasting of AD group with HS, and anatomobehavioural correlations were carried out in order to identify regional atrophic changes and neuro-cognitive aspects in AD group. We found evidence of gray matter (GM) volume reduction in AD in the medial temporal, parietal and frontal areas bilaterally and in the left anterior thalamic nuclei. Performance on the episodic memory delayed recall tests co-varied with GM volume in the left entorhinal cortex. The pattern of cortical atrophy likely reflects the heterogeneous level of dementia severity in our AD group. The anatomical region affected in the left hemisphere indicates a sufferance at multiple levels of the Polysynaptic Hippocampal Pathway, which is involved in declarative memory. Findings on the entorhinal cortex and the delayed memory scores support the role of the entorhinal cortex in episodic memory. Damage to the entorhinal cortex, deafferenting the hippocampus from neocortical inputs, interferes with episodic memory consolidation in AD patients.

Preparatory states in crossmodal spatial attention: spatial specificity and possible control mechanisms.

We used event-related functional magnetic resonance imaging to study the neural correlates of endogenous spatial attention for vision and touch. We examined activity associated with attention-directing cues (central auditory pure tones), symbolically instructing subjects to attend to one hemifield or the other prior to upcoming stimuli, for a visual or tactile task. In different sessions, subjects discriminated either visual or tactile stimuli at the covertly attended side, during bilateral visuotactile stimulation. To distinguish cue-related preparatory activity from any modulation of stimulus processing, unpredictably on some trials only the auditory cue was presented. The use of attend-vision and attend-touch blocks revealed whether preparatory attentional effects were modality-specific or multimodal. Unimodal effects of spatial attention were found in somatosensory cortex for attention to touch, and in occipital areas for attention to vision, both contralateral to the attended side. Multimodal spatial effects (i.e. effects of attended side irrespective of task-relevant modality) were detected in contralateral intraparietal sulcus, traditionally considered a multimodal brain region; and also in the middle occipital gyrus, an area traditionally considered purely visual. Critically, all these activations were observed even on cue-only trials, when no visual or tactile stimuli were subsequently presented. Endogenous shifts of spatial attention result in changes of brain activity prior to the presentation of target stimulation (baseline shifts). Here, we show for the first time the separable multimodal and unimodal components of such preparatory activations. Additionally, irrespective of the attended side and modality, attention-directing auditory cues activated a network of superior frontal and parietal association areas that may play a role in voluntary control of spatial attention for both vision and touch.

Action anticipation beyond the action observation network: a functional magnetic resonance imaging study in expert basketball players.

The ability to predict the actions of others is quintessential for effective social interactions, particularly in competitive contexts (e.g. in sport) when knowledge about upcoming movements allows anticipating rather than reacting to opponents. Studies suggest that we predict what others are doing by using our own motor system as an internal forward model and that the fronto‐parietal action observation network (AON) is fundamental for this ability. However, multiple‐duty cells dealing with action perception and execution have been found in a variety of cortical regions. Here we used functional magnetic resonance imaging to explore, in expert basketball athletes and novices, whether the ability to make early predictions about the fate of sport‐specific actions (i.e. free throws) is underpinned by neural regions beyond the classical AON. We found that, although involved in action prediction, the fronto‐parietal AON was similarly activated in novices and experts. Importantly, athletes exhibited relatively greater activity in the extrastriate body area during the prediction task, probably due to their expert reading of the observed action kinematics. Moreover, experts exhibited higher activation in the bilateral inferior frontal gyrus and in the right anterior insular cortex when producing errors, suggesting that they might become aware of their own errors. Correct action prediction induced higher posterior insular cortex activity in experts and higher orbito‐frontal activity in novices, suggesting that body awareness is important for performance monitoring in experts, whereas novices rely more on higher‐order decision‐making strategies. This functional reorganization highlights the tight relationship between action anticipation, error awareness and motor expertise leading to body‐related processing and differences in decision‐making processes.