João Castelhano

Functional parcellation of the operculo-insular cortex in perceptual decision making: An fMRI study

A current challenge in cognitive neuroscience is to provide an explicit separation of the neural correlates of abstract global decision variables from sensory and integrative ones. In particular, the insular cortex and the adjacent frontal operculum seem to have a crucial but still unclear role in evidence accumulation and decision signaling in perceptual decision-making tasks. Here, we have used a visual decision-making paradigm based on the detection of ambiguous two-tone (Mooney) face stimuli to assess the emergence of holistic percepts. These are constructed using global gestalt rules and not by gradual spatiotemporal increases in sensory evidence. Our paradigm (neurochronometric approach) enabled the experimental separation between multiple cognitive components in perceptual decision validated by both model-driven and data-driven analysis. This strategy allowed for the functional dissection of operculo-insular networks into task related complexes such as anterior (accumulator), middle (decision) and posterior (somatosensory/sensorimotor). We conclude that global perceptual integration based on holistic rules requires a distributed operculo-insular network.

To perceive or not perceive: the role of gamma-band activity in signaling object percepts.

The relation of gamma-band synchrony to holistic perception in which concerns the effects of sensory processing, high level perceptual gestalt formation, motor planning and response is still controversial. To provide a more direct link to emergent perceptual states we have used holistic EEG/ERP paradigms where the moment of perceptual “discovery” of a global pattern was variable. Using a rapid visual presentation of short-lived Mooney objects we found an increase of gamma-band activity locked to perceptual events. Additional experiments using dynamic Mooney stimuli showed that gamma activity increases well before the report of an emergent holistic percept. To confirm these findings in a data driven manner we have further used a support vector machine classification approach to distinguish between perceptual vs. non perceptual states, based on time-frequency features. Sensitivity, specificity and accuracy were all above 95%. Modulations in the 30–75 Hz range were larger for perception states. Interestingly, phase synchrony was larger for perception states for high frequency bands. By focusing on global gestalt mechanisms instead of local processing we conclude that gamma-band activity and synchrony provide a signature of holistic perceptual states of variable onset, which are separable from sensory and motor processing.

The dual facet of gamma oscillations: separate visual and decision making circuits as revealed by simultaneous EEG/fMRI.

It remains an outstanding question whether gamma‐band oscillations reflect unitary cognitive processes within the same task. EEG/MEG studies do lack the resolution or coverage to address the highly debated question whether single gamma activity patterns are linked with multiple cognitive modules or alternatively each pattern associates with a specific cognitive module, within the same coherent perceptual task. One way to disentangle these issues would be to provide direct identification of their sources, by combining different techniques. Here, we directly examined these questions by performing simultaneous EEG/fMRI using an ambiguous perception paradigm requiring holistic integration. We found that distinct gamma frequency sub‐bands reflect different neural substrates and cognitive mechanisms when comparing object perception states vs. no categorical perception. A low gamma sub‐band (near 40 Hz) activity was tightly related to the decision making network, and in particular the anterior insula. A high gamma sub‐band (∼60 Hz) could be linked to early visual processing regions. The demonstration of a clear functional topography for distinct gamma sub‐bands within the same task shows that distinct gamma‐band modulations underlie sensory processing and perceptual decision mechanisms. Hum Brain Mapp 35:5219–5235, 2014. 2014 Wiley Periodicals, Inc.

Neural correlates of visual integration in Williams syndrome: Gamma oscillation patterns in a model of impaired coherence

Williams syndrome (WS) is a clinical model of dorsal stream vulnerability and impaired visual integration. However, little is still known about the neurophysiological correlates of perceptual integration in this condition. We have used a 3D structure-from-motion (SFM) integrative task to characterize the neuronal underpinnings of 3D perception in WS and to probe whether gamma oscillatory patterns reflect changed holistic perception. Coherent faces were parametrically modulated in 3D depth (three different depth levels) to vary levels of stimulus ambiguity. We have found that the electrophysiological (EEG/ERP) correlates of such holistic percepts were distinct across groups. Independent component analysis demonstrated the presence of a novel component with a late positivity around 200 ms that was absent in controls. Source localization analysis of ERP signals showed a posterior occipital shift in WS and reduced parietal dorsal stream sources. Interestingly, low gamma-band oscillations (20-40 Hz) induced by this 3D perceptual integration task were significantly stronger and sustained during the stimulus presentation in WS whereas high gamma-band oscillations (60-90 Hz) were reduced in this clinical model of impaired visual coherence, as compared to controls. These observations suggest that dorsal stream processing of 3D SFM stimuli has distinct neural correlates in WS and different cognitive strategies are employed by these patients to reach visual coherence. Importantly, we found evidence for the presence of different sub-bands (20-40 Hz/60-90 Hz) within the gamma range which can be dissociated concerning the respective role on the coherent percept formation, both in typical and atypical development.

Oscillations or synchrony? disruption of neural synchrony despite enhanced gamma oscillations in a model of disrupted perceptual coherence

It has been hypothesized that neural synchrony underlies perceptual coherence. The hypothesis of loss of central perceptual coherence has been proposed to be at the origin of abnormal cognition in autism spectrum disorders and Williams syndrome, a neurodevelopmental disorder linked with autism, and a clearcut model for impaired central coherence. We took advantage of this model of impaired holistic processing to test the hypothesis that loss of neural synchrony plays a separable role in visual integration using EEG and a set of experimental tasks requiring coherent integration of local elements leading to 3-D face perception. A profound reorganization of brain activity was identified. Neural synchrony was reduced across stimulus conditions, and this was associated with increased amplitude modulation at 25–45 Hz. This combination of a dramatic loss of synchrony despite increased oscillatory activity is strong evidence that synchrony underlies central coherence. This is the first time, to our knowledge, that dissociation between amplitude and synchrony is reported in a human model of impaired perceptual coherence, suggesting that loss of phase coherence is more directly related to disruption of holistic perception.

Distinct functional properties of the vertical and horizontal saccadic network in Health and Parkinson's disease: An eye-tracking and fMRI study.

Saccadic behaviour ranges from reflexive (e.g., prosaccade) to goal oriented voluntary movements (e.g., antisaccade). Behavioural asymmetries between vertical and horizontal saccades have been described both in normal individuals (greater delay of vertical prosaccades) and in disease states such as Parkinsons disease (PD) (prosaccades are short and antisaccades are delayed, especially in the vertical plane, possibly due to a frontostriatal deficit). Importantly, the cortical mechanisms for the generation of vertical saccades are largely unknown, both in health and disease, when compared with their horizontal counterpart. Moreover, studies exploring saccadic neural correlates and putative compensatory mechanisms at a functional level in PD are scarce. We investigated horizontal and vertical prosaccades and antisaccades in an eye tracking paradigm in 19 PD patients off medication and 22 healthy controls, followed by a block-design functional Magnetic Resonance Imaging (fMRI) study, consisting of two runs (prosaccade, antisaccade) of 6 blocks each (3 vertical, 3 horizontal). While saccade metrics were not significantly different between groups, PD showed left frontal underactivation during horizontal prosaccades and right parietal overactivation during horizontal and vertical prosaccades and horizontal antisaccades. Moreover, controls showed greater deactivation of the default-mode network (DMN) during antisaccades. Vertical prosaccades were associated with greater right frontal and cerebellar activity in controls, and cuneus hypoactivity in PD. Vertical antisaccades were associated with greater DMN deactivation in both groups and left frontal hypoactivity in PD. Putative functional compensatory changes in the right parietal cortex in PD patients may help to keep saccadic behaviour at the same level as the healthy controls. We provide first time evidence showing that functional cortical asymmetries between vertical and horizontal saccades occur distinctively in PD patients and healthy controls.

Perceptual Decision Making

An exciting area in cognitive neuroscience concerns the investigation of neural mechanisms underlying the emergence of visual perceptual representations. Multistable interpretations of the visual world are striking phenomena that may occur when the retinal image is compatible with multiple perceptual solutions. This occurs even when the physical pattern of retinal stimulation remains constant. Perceptual decision making is thus defined by the choice of an interpretation among a set of potentially ambiguous alternatives based on peripheral sensory evidence. We discuss current multimodal approaches to investigate the neural correlates of competition between multistable alternative neural representations and the generation of antagonistic perceptual interpretations.

Developmental dissociation of visual dorsal stream parvo and magnocellular representations and the functional impact of negative retinotopic BOLD responses

Localized neurodevelopmental defects provide an opportunity to study structure-function correlations in the human nervous system. This unique multimodal case report of epileptogenic dysplasia in the visual cortex allowed exploring visual function across distinct pathways in retinotopic regions and the dorsal stream, in relation to fMRI retinotopic mapping and spike triggered BOLD responses. Pre-surgical EEG/video monitoring, MRI/DTI, EEG/fMRI, PET and SPECT were performed to characterize structure/function correlations in this patient with a very early lesion onset. In addition, we included psychophysical methods (assessing parvo/konio and magnocellular pathways) and retinotopic mapping. We could identify dorsal stream impairment (with extended contrast sensitivity deficits within the input magno system contrasting with more confined parvocellular deficits) with disrupted active visual field input representations in regions neighboring the lesion. Simultaneous EEG/fMRI identified perilesional and retinotopic bilaterally symmetric BOLD deactivation triggered by interictal spikes, which matched the contralateral spread of magnocellular dysfunction revealed in the psychophysical tests. Topographic changes in retinotopic organization further suggested long term functional effects of abnormal electrical discharges during brain development. We conclude that fMRI based visual field cortical mapping shows evidence for retinotopic dissociation between magno and parvocellular function well beyond striate cortex, identifiable in high level dorsal visual representations around visual area V3A which is consistent with the effects of epileptic spike triggered negative BOLD.

The anterior versus posterior hippocampal oscillations debate in human spatial navigation: evidence from an electrocorticographic case study

Hippocampal oscillations have been regularly described as playing a dominant role in spatial memory and navigation in rodents. In humans, the relative role of anterior versus posterior rhythms during navigational memory is not established.

Feature analysis for correlation studies of simultaneous EEG-fMRI data: A proof of concept for neurofeedback approaches.

The identification and interpretation of facial expressions is an important feature of social cognition. This characteristic is often impaired in various neurodevelopmental disorders. Recent therapeutic approaches to intervene in social communication impairments include neurofeedback (NF). In this study, we present a NF real-time functional Magnetic Resonance Imaging (rt-fMRI), combined with electroencephalography (EEG) to train social communication skills. In this sense, we defined the right Superior Temporal Sulcus as our target region-of-interest. To analyze the correlation between the fMRI regions of interest and the EEG data, we transposed the sources located at the nearest cortical location to the target region. We extracted a set of 75 features from EEG segments and performed a correlation analysis with the brain activations extracted from rt-fMRI in the right pSTS region. The finding of significant correlations of simultaneously measured signals in distinct modalities (EEG and fMRI) is promising. Future studies should address whether the observed correlation levels between local brain activity and scalp measures are sufficient to implement NF approaches.