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

Clarifying the neurophysiological basis of the other-race effect

The other race effect (ORE) is a well-known phenomenon whereby individuals tend to identify more accurately faces from their same-race (SR) as opposed to faces from the other-race (OR). First reported by Feingold (1914), almost a hundred years ago, since then the ORE has found consistent support at the behavioural level. In spite of a general consensus regarding the robustness of this effect, theoretical accounts have thus far failed to reach an agreement concerning the causes underlying this phenomenon. Two main strands exist within the academic literature, differing on the alleged roots of the ORE. One regards this phenomenon as stemming from different levels of expertise individuals hold with SR and OR face (i.e. the expertise based accounts); the other advocates the importance of social cognitive factor (i.e. the social cognitive accounts). Neuroimaging data can provide important insights in understanding the basis of the ORE. These studies though have thus far failed to reach a degree of consistency. EEG data for example are highly contradictory. A number of studies report no race sensitivity on the N170 face preferential component, while others show that this component is in fact modulated by race. However, discrepancy is found even amongst the study reporting N170 modulation to race, with some showing larger N170 to SR faces, while others revealing the opposite pattern. Similarly, fMRI data show the same degree of inconsistency, especially with regards to the role played by the fusiform face area (FFA). The aim of this thesis is to clarify the neurphysiolological basis of the ORE in order to gain further insights into its origins. To this end three studies (two employing EEG and one fMRI) were designed to answer three main questions related to the ORE: when, how and where in the brain does this phenomenon occur. The first study investigates the conjoint effects of race and the face inversion effect (FIE - regarded as a marker of configural face processing) on the N170. Interestingly, no race modulations on this ERP component were observed for upright faces. Race however impacted upon the magnitude of the electrophysiological FIE, with SR faces leading to greater recognition impairment and eliciting larger N170 amplitudes compared to inverted OR faces. These results indicate that race impacts upon early perceptual stages of face processing and that SR and OR faces are processed in a qualitatively different manner. The second study exploites the advantages conferred by adaptation paradigm to test neural coding efficiency for faces of different races. An unbiased spatiotemporal data-driven analysis on the newly developed single-trial repetition suppression (srRS) index, which fully accounts for the paired nature of the design, revealed differential amounts of repetition suppression across races on the N170 time window. These data suggest the SR faces are coded more efficiently than OR faces and, in line with the previous results, that race is processed at early perceptual stages. The final study investigates whether and where in the brain faces are coded according to the laws predicted by valentine’s norm based multidimensional face space model. Representational Dissimilarity Matrices (RDM) showed that faces are coded as a function of experience within the dominant FFA according to the laws of valentine’s theoretical framework Importantly in all experiments I tested both Western Caucasian (WC) and East Asian (EA) observers viewing WC and EA faces. A crossover interaction between the race of the observers and that of the face stimuli is in fact crucial to genuinely relate any observed effect to race, and exclude potential low level confounds that may be intrinsic in the stimulus set. These data, taken together indicate that the ORE is an expertise based phenomenon and that it takes place at early perceptual level of face processing

Temporal Multivariate Pattern Analysis (tMVPA): a single trial approach exploring the temporal dynamics of the BOLD signal

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. 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. 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. 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. 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

Contextual Feedback to Superficial Layers of V1

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 mm(3)) 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

The neural microgenesis of personally 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 occipito-temporal 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

Eyes like it, brain likes it: Tracking the neural tuning of cultural diversity in eye movements for faces

Eye movement strategies deployed by humans to identify conspecifics are not universal. Westerners preferentially fixate the eyes and the mouth during face recognition, whereas strikingly Easterners focus more on the face central region. However, when, where and how Preferred Viewing Locations (PVLs) for high-level visual stimuli are coded in the human brain has never been directly investigated. Here, we simultaneously recorded eye-movements and electroencephalographic (EEG) signals of Westerners and Easterners during face identification of learnt identities. After defining 9 equidistant Viewing Positions (VPs) covering all facial internal features, we presented the learned faces centered on a random VP for 100ms. We then extracted from prior free-viewing fixation maps the average Z-scored fixation intensity for the nonoverlapping facial VP regions (VPZs). Finally, we computed a component-free data-driven spatio-temporal regression between the VPZs and EEG amplitudes. This analysis revealed a universal direct relationship between VPZ and EEG amplitudes over the face-sensitive N170 network at around 350ms, an effect unrelated to a burst of microsaccades occurring in this time-window. Our data show that the distinct cultural fixation preferences for faces are related to a universal post-perceptual tuning in the occipito-temporal cortex. Culture shapes visual information sampling, but does not regulate neural information coding

Modulation of task-related electrophysiological responses by socially relevant stimuli

Human faces induce stronger involuntary orienting responses than other visual objects. We recently reported a significant increase in anti-saccade error rates for faces compared to cars and noise patterns, as well as faster pro-saccades compared to the other visual categories (Morand et al., 2010). However, when and where this preferential orienting response is taking place at the neural level remains to be clarified. To address this issue, we investigated the neural dynamics preceding the onset of pro-and anti-saccades elicited by human faces and non-face visual objects normalized for their low-level visual properties (i.e., amplitude spectra and contrast). We simultaneously recorded high-density evoked potentials (ERPs) and eye movements in adult observers as they performed randomly interleaved pro- and anti-saccades to a lateralized target. Pro- and anti-saccades directed to the same visual field significantly modulated the electrophysiological signals within the 100–140 ms time-period following target onset. These amplitude modulations were associated with distinct electrical scalp topographies. Faces triggering pro-saccades directed to the left and anti-saccades directed to the right (presented in the LVF) modulated the neurophysiological signals over the temporo-occipital electrodes (PO8 and P9) at 130–140 ms, which correspond to the right and left counterparts of the face-sensitive N170 component respectively. These neurophysiological modulations were not accompanied with topographic changes, but with an increase in response amplitude for faces. Our data show distinct electrophysiological signatures for pro- and anti-saccades occurring as early as 100 ms after target onset. We believe these to reflect distinct cortical networks, probably recruiting the FEF and DLPFC in their respective role in saccade programming. Critically, faces, compared to other visual objects impact upon saccade programming at several stages by modulating the magnitude of the cortical networks active prior to both pro- and anti-saccades execution. These observations provide the neural dynamics and mapping of the involuntary orienting responses for faces

Multivoxel Pattern of Blood Oxygen Level Dependent Activity can be sensitive to stimulus specific fine scale responses

At ultra-high field, fMRI voxels can span the sub-millimeter range, allowing the recording of blood oxygenation level dependent (BOLD) responses at the level of fundamental units of neural computation, such as cortical columns and layers. This sub-millimeter resolution, however, is only nominal in nature as a number of factors limit the spatial acuity of functional voxels. Multivoxel Pattern Analysis (MVPA) may provide a means to detect information at finer spatial scales that may otherwise not be visible at the single voxel level due to limitations in sensitivity and specificity. Here, we evaluate the spatial scale of stimuli specific BOLD responses in multivoxel patterns exploited by linear Support Vector Machine, Linear Discriminant Analysis and Naïve Bayesian classifiers across cortical depths in V1. To this end, we artificially misaligned the testing relative to the training portion of the data in increasing spatial steps, then investigated the breakdown of the classifiers' performances. A one voxel shift led to a significant decrease in decoding accuracy (p < 0.05) across all cortical depths, indicating that stimulus specific responses in a multivoxel pattern of BOLD activity exploited by multivariate decoders can be as precise as the nominal resolution of single voxels (here 0.8 mm isotropic). Our results further indicate that large draining vessels, prominently residing in proximity of the pial surface, do not, in this case, hinder the ability of MVPA to exploit fine scale patterns of BOLD signals. We argue that tailored analytical approaches can help overcoming limitations in high-resolution fMRI and permit studying the mesoscale organization of the human brain with higher sensitivities

Lowering the thermal noise barrier in functional brain mapping with magnetic resonance imaging

Functional magnetic resonance imaging (fMRI) has become an indispensable tool for investigating the human brain. However, the inherently poor signal-to-noise-ratio (SNR) of the fMRI measurement represents a major barrier to expanding its spatiotemporal scale as well as its utility and ultimate impact. Here we introduce a denoising technique that selectively suppresses the thermal noise contribution to the fMRI experiment. Using 7-Tesla, high-resolution human brain data, we demonstrate improvements in key metrics of functional mapping (temporal-SNR, the detection and reproducibility of stimulus-induced signal changes, and accuracy of functional maps) while leaving the amplitude of the stimulus-induced signal changes, spatial precision, and functional point-spread-function unaltered. We demonstrate that the method enables the acquisition of ultrahigh resolution (0.5 mm isotropic) functional maps but is also equally beneficial for a large variety of fMRI applications, including supra-millimeter resolution 3- and 7-Tesla data obtained over different cortical regions with different stimulation/task paradigms and acquisition strategies