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The blind brain: How (lack of) vision shapes the morphological and functional architecture of the human brain
No full textSince the early days, how we represent the world around us has been a matter of philosophical speculation. Over the last few decades, modern neuroscience, and specifically the development of methodologies for the structural and the functional exploration of the brain have made it possible to investigate old questions with an innovative approach. In this brief review, we discuss the main findings from a series of brain anatomical and functional studies conducted in sighted and congenitally blind individuals by our’s and others' laboratories. Historically, research on the ‘blind brain’ has focused mainly on the cross-modal plastic changes that follow sensory deprivation. More recently, a novel line of research has been developed to determine to what extent visual experience is truly required to achieve a representation of the surrounding environment. Overall, the results of these studies indicate that most of the brain fine morphological and functional architecture is programmed to develop and function independently from any visual experience. Distinct cortical areas are able to process information in a supramodal fashion, that is, independently from the sensory modality that carries that information to the brain. These observations strongly support the hypothesis of a modality-independent, i.e. more abstract, cortical organization, and may contribute to explain how congenitally blind individuals may interact efficiently with an external world that they have never seen
Modality-indipendent Classification of Action Feature in the Human Brain
No full textIntroduction:
The human Mirror System (hMS) transforms visual information into motor knowledge and thus mediates understanding of actions done by others. This feature relies on an abstract, supramodal sensory representation of motor acts; hMS is also recruited when individuals receive clues of the occurring action with no visual features (e.g. actions sound) [4] and is activated by action sounds also in congenitally blind individuals [8]. Here we applied a Multi Voxel Pattern Analysis (MVPA), recently used to discriminate Action Feature (AF) in visual stimuli [7], to classify a set of hand-made actions. Specifically, we tested the hypothesis that classification of action feature in the human brain is not strictly dependent from a given sensory modality but rather relies on the pattern information in specific supramodal regions.
Methods:
We used a fMRI (GE Signa 1.5T; TR 2.5s, 21 5-mm axial slices, 128x128 pixels) sparse sampling six-run block design to examine neural activity in 8 congenitally blind (6F, 44±16 yrs) and 14 sighted (5F, 32±13 yrs) right-handed healthy volunteers while they alternated between the auditory and visual (sighted only) presentation of hand-executed action or environmental stimuli, and the execution of a "virtual" tool or object manipulation task (Pantomime). After standard preprocessing using AFNI [2], BOLD responses to each stimulus were identified in cortical surface voxels. To separate action from environmental stimuli in blind (sounds only) and sighted (sounds and videos) subjects, we built three distinct linear Support Vector Machine (SVM) binary classifiers [5]. A Recursive Feature Elimination (RFE) algorithm was used to prune undiscriminative voxels [3]. To uncover all voxels potentially contributing to the supramodal representation of actions, a knock-out procedure was implemented, removing all overlapping voxels across the discriminative maps of each classifier [1]. Finally, the three SVM classifiers were applied to these common voxels.
Results:
The three SVM classifiers, trained separately, were able to identify the AF during learning with a mean accuracy (Acc) on cross-validation leave-one-subject-out of 94% in each experimental condition. Further, the three classifiers overall classified the motor pantomime as an action (recall [Rec] 75%).
In an across conditions evaluation, only the video classifier was able to significantly classify auditory stimuli in the sighted (Acc 57%, p<0.01; Rec 66%) and blind group (Acc 55%, p<0.05; Rec 57%).
The knock-out procedure removed overlapping voxels across discriminative maps, located mainly in hMS-related areas (left inferior and superior parietal, left ventral and dorsal premotor area, middle temporal cortex) and in bilateral striate and extrastriate, right temporo-parietal, dorsolateral and medial prefrontal cortex, bilateral precuneus and posterior cingulate. After this step, the video classifier was not able to identify auditory stimuli neither in sighted nor in blind subjects, even if still able to classify video stimuli, thus indicating that the classifier relies on a visual-specific AF.
Finally, using only common voxels, the video classifier achieved on auditory stimuli a 62% accuracy (p<0.0001; Rec 73%) and a 63% accuracy (p<0.0001; Rec 70%) in blind subjects; also the audio classifier trained on sighted identified action videos (Acc 57%, p<0.01; Rec 61%).
Conclusions:
For the first time, a MPVA-based classifier successfully discriminated the neural "space" of action representation, extracted the AF in the perceived stimuli, and thus separated actions from non-action stimuli with a distributed representation in a network including the hMS in both sighted and blind individuals independently from the sensory modality of stimuli. That the concept of an action in the brain relies on a more abstract neural representation contributes to explain how individuals deprived of sight since birth may learn by and interact effectively with others [6].
References:
1)Carlson TA (2003), ‘Patterns of Activity in the Categorical Representation of Objects’, J. Cog. Neorosci., vol. 15, no. 5, pp. 704–717.
2)Cox RW (1996), ‘AFNI: software for analysis and visualization of functional magnetic resonance neuroimages’, Comput Biomed Res, vol. 29, pp. 162-173.
3)De Martino F (2008), ‘Combining multivariate voxel selection and support vector machines for mapping and classification of fMRI spatial patterns’, Neuroimage, vol. 43, pp. 44-58.
4)Galati G (2008), ‘A selective representation of the meaning of actions in the auditory mirror system’, Neuroimage, vol. 40, pp. 1274-1286.
5)Joachims T (1999), ‘Making large-Scale SVM Learning Practical. Advances in Kernel Methods - Support Vector Learning’, Schölkopf and Burges and Smola (ed.), MIT Press
6)Matteau I (2010), ‘Beyond visual, aural and haptic movement perception: hMT+ is activated by electrotactile motion stimulation of the tongue in sighted and in congenitally blind individuals’, Brain Res Bull, vol. 82, no. 5-6; pp. 264-270.
7)Oosterhof NN (2010), ‘Surface-based information mapping reveals crossmodal vision-action representations in human parietal and occipitotemporal cortex’, J Neurophysiol, vol. 104, pp. 1077-1089.
8)Ricciardi E (2009), ‘Do we really need vision? How blind people "see" the actions of others’, J Neurosci, vol. 29, pp. 9719-9724
Cholinergic enhancement differentially modulates neural response to encoding during face identity and face location working memory tasks.
No full textPotentiation of cholinergic transmission influences stimulus processing by enhancing signal detection through suppression and/or filtering out of irrelevant information (bottom-up modulation) and with top-down task-oriented executive mechanisms based on the recruitment of prefrontal and parietal attentional systems. The cholinergic system also plays a critical role in working memory (WM) processes and preferentially modulates WM encoding, likely through stimulus-processing mechanisms. Previous research reported increased brain responses in visual extrastriate cortical regions during cholinergic enhancement in the encoding phase of WM, independently addressing object and spatial encoding. The current study used functional magnetic resonance imaging to determine the effects of cholinergic enhancement on encoding of key visual processing features. Subjects participated in two scanning sessions, one during an intravenous (i.v.) infusion of saline and the other during an infusion of the acetylcholinesterase inhibitor physostigmine. In each scan session, subjects alternated between a face identity recognition and a spatial location WM. Enhanced cholinergic function increased neural activity in the ventral stream during encoding of face identity and in the dorsal stream during encoding of face location. Conversely, a reduction in brain response was found for scrambled sensorimotor control images. The cholinergic effects on neural activity in the ventral stream during encoding of face identity were stronger than those observed in the dorsal stream during encoding of face location, likely as a consequence of the role of acetylcholine in establishing the inherently relevant nature of face identity. Despite the limited sample-size, the results suggest the stimulus-dependent role of cholinergic system in signal detection, as they show that cholinergic potentiation enhances neural activity in regions associated with early perceptual processing in a selective manner depending on the attended stimulus feature
Increased BOLD variability and functional connectivity changes in congenitally blind individuals
No full textCholinergic enhancement modulates regional functional connectivity during a selective attention task
No full textCholinergic enhancement reduces functional connectivity and BOLD variability in visual extrastriate cortex during selective attention
Full text linkEnhancing cholinergic function improves performance on various cognitive tasks and alters neural responses in task specific brain regions. We have hypothesized that the changes in neural activity observed during increased cholinergic function reflect an increase in neural efficiency that leads to improved task performance. The current study tested this hypothesis by assessing neural efficiency based on cholinergically-mediated effects on regional brain connectivity and BOLD signal variability. Nine subjects participated in a double-blind, placebo-controlled crossover fMRI study. Following an infusion of physostigmine (1 mg/h) or placebo, echo-planar imaging (EPI) was conducted as participants performed a selective attention task. During the task, two images comprised of superimposed pictures of faces and houses were presented. Subjects were instructed periodically to shift their attention from one stimulus component to the other and to perform a matching task using hand held response buttons. A control condition included phase-scrambled images of superimposed faces and houses that were presented in the same temporal and spatial manner as the attention task; participants were instructed to perform a matching task. Cholinergic enhancement improved performance during the selective attention task, with no change during the control task. Functional connectivity analyses showed that the strength of connectivity between ventral visual processing areas and task-related occipital, parietal and prefrontal regions reduced significantly during cholinergic enhancement, exclusively during the selective attention task. Physostigmine administration also reduced BOLD signal temporal variability relative to placebo throughout temporal and occipital visual processing areas, again during the selective attention task only. Together with the observed behavioral improvement, the decreases in connectivity strength throughout task-relevant regions and {BOLD} variability within stimulus processing regions support the hypothesis that cholinergic augmentation results in enhanced neural efficiency. This article is part of a Special Issue entitled ‘Cognitive Enhancers’
Cholinergic Effects in Visual Areas during Object and Spatial Working Memory Encoding: an fMRI study
No full textBehavioral and Brain Effects of Cholinergic Enhancement of Selective Attention to Faces and Houses
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Cholinergic Enhancement Modulates Neural Activity on Large Scale Representations of Faces and Houses
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