Luca Vizioli

Contextual Feedback to Superficial Layers of V1.

Summary Neuronal cortical circuitry comprises feedforward, lateral, and feedback projections, each of which terminates in distinct cortical layers [1–3]. In sensory systems, feedforward processing transmits signals from the external world into the cortex, whereas feedback pathways signal the brain’s inference of the world [4–11]. However, the integration of feedforward, lateral, and feedback inputs within each cortical area impedes the investigation of feedback, and to date, no technique has isolated the feedback of visual scene information in distinct layers of healthy human cortex. We masked feedforward input to a region of V1 cortex and studied the remaining internal processing. Using high-resolution functional brain imaging (0.8 mm3) and multivoxel pattern information techniques, we demonstrate that during normal visual stimulation scene information peaks in mid-layers. Conversely, we found that contextual feedback information peaks in outer, superficial layers. Further, we found that shifting the position of the visual scene surrounding the mask parametrically modulates feedback in superficial layers of V1. Our results reveal the layered cortical organization of external versus internal visual processing streams during perception in healthy human subjects. We provide empirical support for theoretical feedback models such as predictive coding [10, 12] and coherent infomax [13] and reveal the potential of high-resolution fMRI to access internal processing in sub-millimeter human cortex.

Neural repetition suppression to identity is abolished by other-race faces.

Human beings are remarkably skilled at recognizing faces, with the marked exception of other-race faces: the so-called “other-race effect.” As reported nearly a century ago [Feingold CA (1914) Journal of Criminal Law and Police Science 5:39–51], this face-recognition impairment is accompanied by the popular belief that other-race faces all look alike. However, the neural mechanisms underlying this high-level “perceptual illusion” are still unknown. To address this question, we recorded high-resolution electrophysiological scalp signals from East Asian (EA) and Western Caucasian (WC) observers as they viewed two EA or WC faces. The first adaptor face was followed by a target face of either the same or different identity. We quantified repetition suppression (RS), a reduction in neural activity in stimulus-sensitive regions following stimulus repetition. Conventional electrophysiological analyses on target faces failed to reveal any RS effect. However, to fully account for the paired nature of RS events, we subtracted the signal elicited by target to adaptor faces for each single trial and performed unbiased spatiotemporal data-driven analyses. This unique approach revealed stronger RS to same-race faces of same identity in both groups of observers on the face-sensitive N170 component. Such neurophysiological modulation in RS suggests efficient identity coding for same-race faces. Strikingly, OR faces elicited identical RS regardless of identity, all looking alike to the neural population underlying the N170. Our data show that sensitivity to race begins early at the perceptual level, providing, after nearly 100 y of investigations, a neurophysiological correlate of the “all look alike” perceptual experience.

Inverting faces elicits sensitivity to race on the N170 component: A cross-cultural study

Human beings are natural experts at processing faces, with some notable exceptions. Same-race faces are better recognized than other-race faces: the so-called other-race effect (ORE). Inverting faces impairs recognition more than for any other inverted visual object: the so-called face inversion effect (FIE). Interestingly, the FIE is stronger for same- compared to other-race faces. At the electrophysiological level, inverted faces elicit consistently delayed and often larger N170 compared to upright faces. However, whether the N170 component is sensitive to race is still a matter of ongoing debate. Here we investigated the N170 sensitivity to race in the framework of the FIE. We recorded EEG from Western Caucasian and East Asian observers while presented with Western Caucasian, East Asian and African American faces in upright and inverted orientations. To control for potential confounds in the EEG signal that might be evoked by the intrinsic and salient differences in the low-level properties of faces from different races, we normalized their amplitude-spectra, luminance and contrast. No differences on the N170 were observed for upright faces. Critically, inverted same-race faces lead to greater recognition impairment and elicited larger N170 amplitudes compared to inverted other-race faces. Our results indicate a finer-grained neural tuning for same-race faces at early stages of processing in both groups of observers.

Mapping face recognition information use across cultures

Face recognition is not rooted in a universal eye movement information-gathering strategy. Western observers favor a local facial feature sampling strategy, whereas Eastern observers prefer sampling face information from a global, central fixation strategy. Yet, the precise qualitative (the diagnostic) and quantitative (the amount) information underlying these cultural perceptual biases in face recognition remains undetermined. To this end, we monitored the eye movements of Western and Eastern observers during a face recognition task, with a novel gaze-contingent technique: the Expanding Spotlight. We used 2° Gaussian apertures centered on the observers’ fixations expanding dynamically at a rate of 1° every 25 ms at each fixation – the longer the fixation duration, the larger the aperture size. Identity-specific face information was only displayed within the Gaussian aperture; outside the aperture, an average face template was displayed to facilitate saccade planning. Thus, the Expanding Spotlight simultaneously maps out the facial information span at each fixation location. Data obtained with the Expanding Spotlight technique confirmed that Westerners extract more information from the eye region, whereas Easterners extract more information from the nose region. Interestingly, this quantitative difference was paired with a qualitative disparity. Retinal filters based on spatial-frequency decomposition built from the fixations maps revealed that Westerners used local high-spatial-frequency information sampling, covering all the features critical for effective face recognition (the eyes and the mouth). In contrast, Easterners achieved a similar result by using global low-spatial-frequency information from those facial features. Our data show that the face system flexibly engages into local or global eye movement strategies across cultures, by relying on distinct facial information span and culturally tuned spatially filtered information. Overall, our findings challenge the view of a unique putative process for face recognition.

Contributions of cortical feedback to sensory processing in primary visual cortex

Closing the structure-function divide is more challenging in the brain than in any other organ (Lichtman and Denk, 2011). For example, in early visual cortex, feedback projections to V1 can be quantified (e.g., Budd, 1998) but the understanding of feedback function is comparatively rudimentary (Muckli and Petro, 2013). Focusing on the function of feedback, we discuss how textbook descriptions mask the complexity of V1 responses, and how feedback and local activity reflects not only sensory processing but internal brain states.

Neural microgenesis of personally familiar face recognition

Significance We addressed the open question of how the human brain recognizes personally familiar faces. A dynamic visual-stimulation paradigm revealed that familiar face recognition is achieved first and foremost in medial and anterior temporal regions of the extended face-processing system. These regions, including the amygdala, respond categorically to individual familiar faces. In contrast, activation in posterior core face-preferential regions is associated with the amount of visual information available, irrespective of familiarity. Through integration of core and extended face-processing systems, these observations provide a common framework for understanding the neural basis of familiar face recognition. Despite a wealth of information provided by neuroimaging research, the neural basis of familiar face recognition in humans remains largely unknown. Here, we isolated the discriminative neural responses to unfamiliar and familiar faces by slowly increasing visual information (i.e., high-spatial frequencies) to progressively reveal faces of unfamiliar or personally familiar individuals. Activation in ventral occipitotemporal face-preferential regions increased with visual information, independently of long-term face familiarity. In contrast, medial temporal lobe structures (perirhinal cortex, amygdala, hippocampus) and anterior inferior temporal cortex responded abruptly when sufficient information for familiar face recognition was accumulated. These observations suggest that following detailed analysis of individual faces in core posterior areas of the face-processing network, familiar face recognition emerges categorically in medial temporal and anterior regions of the extended cortical face network.

A Functional Magnetic Resonance Imaging Paradigm to Identify Distinct Cortical Areas of Facial Function: A Reliable Localizer

Background: Irreversible facial paralysis can be surgically treated by importing both a new neural and a new motor muscle supply. Various donor nerves can be used. If a nerve supply other than the facial nerve is used, the patient has to adapt to generate a smile. If branches of the fifth cranial nerve are used, the patient has to learn to clench teeth and smile. Currently, controversy exists regarding whether a patient develops a spontaneous smile if a nerve other than the facial nerve is used. The authors postulate that brain adaptation in facial palsy patients can occur because of neural plasticity. The authors aimed to determine whether functional magnetic resonance imaging could topographically differentiate activity between the facial nerve– and the trigeminal nerve–related cortical areas. Methods: A new paradigm of study using functional magnetic resonance imaging based on blood oxygen level–dependent signal activation was tested on 15 voluntary healthy subjects to find a sensitive localizer for teeth clenching and smiling. Subjects smiled to stimulate the facial nerve–related cortex, clenched their jaws to stimulate the trigeminal nerve–related cortex, and tapped their finger as a control condition. Results: Smiling and teeth clenching showed distinct and consistent areas of cortical activation. Trigeminal and facial motor cortex areas were found to be distinct areas with minimal overlapping. Conclusions: The authors successfully devised a functional magnetic resonance imaging paradigm effective for activating specific areas corresponding to teeth clenching and smiling. This will allow accurate mapping of cortical plasticity in facial reanimation patients. CLINICAL QUESTION/LEVEL OF EVIDENCE: Diagnostic, IV.

A critical assessment of data quality and venous effects in ultra-high-resolution fMRI

Advances in hardware, pulse sequences, and reconstruction techniques have made it possible to perform functional magnetic resonance imaging (fMRI) at sub-millimeter resolution while maintaining high spatial coverage and acceptable signal-to-noise ratio. Here, we examine whether ultra-high-resolution fMRI can be exploited for routine use in neuroscience research. We conducted fMRI in human visual cortex during a simple event-related visual experiment (7T, gradient-echo EPI, 0.8-mm isotropic voxels, 2.2-s sampling rate, 84 slices), and developed analysis and visualization tools to assess the quality of the data. We make three main observations. First, we find that the acquired fMRI images, combined with appropriate surface-based processing, provide reliable and accurate measurements of fine-scale blood oxygenation level dependent (BOLD) activity patterns. Second, we show that the highly folded structure of cortex causes substantial biases on spatial resolution and data visualization. Third, we examine the well-recognized issue of venous contributions to fMRI signals. In a systematic assessment of large sections of cortex measured at a fine scale, we show that time-averaged T2*-weighted EPI intensity is a simple, robust marker of venous effects. These venous effects are unevenly distributed across cortex, are more pronounced in gyri and outer cortical depths, and are, to a certain degree, in consistent locations across subjects relative to cortical folding. Furthermore, we show that these venous effects are strongly correlated with BOLD responses evoked by the experiment. We conclude that ultra-high-resolution fMRI can provide robust information about fine-scale BOLD activity patterns, but special care must be exercised in visualizing and interpreting these patterns, especially with regards to the confounding influence of the brain’s vasculature. To help translate these methodological findings to neuroscience research, we provide practical suggestions for both high-resolution and standard-resolution fMRI studies.

Temporal multivariate pattern analysis (tMVPA): A single trial approach exploring the temporal dynamics of the BOLD signal.

Background: fMRI provides spatial resolution that is unmatched by non-invasive neuroimaging techniques. Its temporal dynamics however are typically neglected due to the sluggishness of the hemodynamic signal. New Methods: We present temporal multivariate pattern analysis (tMVPA), a method for investigating the temporal evolution of neural representations in fMRI data, computed on single-trial BOLD time-courses, leveraging both spatial and temporal components of the fMRI signal. We implemented an expanding sliding window approach that allows identifying the time-window of an effect. Results: We demonstrate that tMVPA can successfully detect condition-specific multivariate modulations over time, in the absence of mean BOLD amplitude differences. Using Monte-Carlo simulations and synthetic data, we quantified family-wise error rate (FWER) and statistical power. Both at the group and single-subject levels, FWER was either at or significantly below 5%. We reached the desired power with 18 subjects and 12 trials for the group level, and with 14 trials in the single-subject scenario. Comparison with existing methods: We compare the tMVPA statistical evaluation to that of a linear support vector machine (SVM). SVM outperformed tMVPA with large N and trial numbers. Conversely, tMVPA, leveraging on single trials analyses, outperformed SVM in low N and trials and in a single-subject scenario. Conclusion: Recent evidence suggesting that the BOLD signal carries finer-grained temporal information than previously thought, advocates the need for analytical tools, such as tMVPA, tailored to investigate BOLD temporal dynamics. The comparable performance between tMVPA and SVM, a powerful and reliable tool for fMRI, supports the validity of our technique.

Laminar communication in V1 at ultra-high field fMRI

Ultra-high field fMRI provides the unique opportunity to record brain activation at sub-millimeter resolution. It is thus possible to reconstruct different cortical depth layers within primary and early visual cortices. Here we investigated how neural activity transfers across different cortical depth layers in V1. Specifically we ask whether thalamo-cortical, and cortico-cortical triggered responses lead to different inter-laminar communication patterns. To address this issue we used previously recorded data (Muckli et al., 2014), that were acquired to investigate laminar sensitivity to cortico-cortical contextual information. Using a visual occlusion paradigm these data showed that in the absence of thalamic input to V1, outermost layers hold meaningful contextual information about the immediate visual environment.The current data set encloses the BOLD signal of 4 participants while they were viewing images of natural scenes. To isolate non-thalamic-related activity, retinal input to a selected portion of V1 was blocked by occluding the bottom right quadrant of the images. Our analysis focused on a subpopulation of V1 voxels obtained by retinotopically mapping the cortical representation of the occluded area. We used two simple linear encoding models to assess the preferential tuning of individual voxels to contextual information. This approach provided additional evidence that outermost layers exhibit the largest concentration of voxels sensitive to contextual information. We also iteratively trained support vector machines (SVM) on each layer and tested on the remaining 5, independently for feed-back (i.e. neural activity triggered by occluded images) and feed-forward (i.e. neural activity triggered by non-occluded images) signals. We found feed-forward cross-layer SVM accuracy was highest in the mid layers; and feed-back cross-layer SVM accuracy was highest in the outermost layers. In line with animal models, these results suggest that mid-layer communication is prominent during feed-forward processing, while outer layers interact mostly during feed-back. Meeting abstract presented at VSS 2015.