Faster, stronger, lateralized: Low spatial frequency information supports face processing

Face perception in adults depends on skilled processing of interattribute distances ('configural' processing), which is disrupted for faces presented in inverted orientation (face inversion effect or FIE). Children are not proficient in configural processing, and this might relate to an underlying immaturity to use facial information in low spatial frequency (SF) ranges, which capture the coarse information needed for configural processing. We hypothesized that during adolescence a shift from use of high to low SF information takes place. Therefore, we studied the influence of SF content on neural face processing in groups of children (9-10years), adolescents (14-15years) and young adults (21-29years) by measuring event-related potentials (ERPs) to upright and inverted faces which varied in SF content. Results revealed that children show a neural FIE in early processing stages (i.e. P1; generated in early visual areas), suggesting a superficial, global facial analysis. In contrast, ERPs of adults revealed an FIE at later processing stages (i.e. N170; generated in face-selective, higher visual areas). Interestingly, adolescents showed FIEs in both processing stages, suggesting a hybrid developmental stage. Furthermore, adolescents and adults showed FIEs for stimuli containing low SF information, whereas such effects were driven by both low and high SF information in children. These results indicate that face processing has a protracted maturational course into adolescence, and is dependent on changes in SF processing. During adolescence, sensitivity to configural cues is developed, which aids the fast and holistic processing that is so special for faces.

Orbital frontal cortex (OFC) is known to play a role in object recognition by generating "first-pass" hypotheses about the identity of naturalistic images based on low spatial frequency (SF) information. These hypotheses are evaluated by more detailed (and slower) ventral visual pathway processes. While it has been suggested on theoretical grounds, it remains unknown whether OFC also receives postrecognition feedback about stimulus identity. We used a novel paradigm in the context of functional magnetic resonance imaging that permits the first few hundred milliseconds of object recognition to be spread out over 120 s. OFC shows a robust response to low and relatively high SFs, whereas ventral stream regions display unimodal response distributions shifted toward high SFs. These findings in OFC were modulated by hemisphere, with right OFC differentially responding to low SFs and left OFC differentially responding to high SFs. Psychophysical experiments confirmed that the same ranges of SFs preferred by ventral stream regions are critical for determining the accuracy and speed of object recognition. Our findings indicate that OFC accesses global form (low SF information, right OFC) and object identity (high SF information, left OFC), and suggest that OFC receives feedback about the accuracy of its initial hypothesis regarding stimulus identity.

ABSTRACTCurrent models of visual perception suggest that, during scene categorization, low spatial frequencies (LSF) are rapidly processed and activate plausible interpretations of visual input. This coarse analysis would be used to guide subsequent processing of high spatial frequencies (HSF). The present study aimed to further examine how information from LSF and HSF interact and influence each other during scene categorization. In a first experimental session, participants had to categorize LSF and HSF filtered scenes belonging to two different semantic categories (artificial vs. natural). In a second experimental session, we used hybrid scenes as stimuli made by combining LSF and HSF from two different scenes which were semantically similar or dissimilar. Half of the participants categorized LSF scenes in hybrids, and the other half categorized HSF scenes in hybrids. Stimuli were presented for 30 or 100 ms. Session 1 results showed better performance for LSF than HSF scene categorization. Session 2 scene categorization was faster when participants attended and categorized LSF than HSF scene in hybrids. The semantic interference of a semantically dissimilar HSF scene on LSF scene categorization was greater than the semantic interference of a semantically dissimilar LSF scene on HSF scene categorization, irrespective of exposure duration. These results suggest a LSF advantage for scene categorization, and highlight the prominent role of HSF information when there is uncertainty about the visual stimulus, in order to disentangle between alternative interpretations.

The effects of picture manipulations on humans' and pigeons' performance were examined in a go/no-go discrimination of two perceptually similar categories, cat and dog faces. Four types of manipulation were used to modify the images. Mosaicization and scrambling were used to produce degraded versions of the training stimuli, while morphing and cell exchange were used to manipulate the relative contribution of positive and negative training stimuli to test stimuli. Mosaicization mainly removes information at high spatial frequencies, whereas scrambling removes information at low spatial frequencies to a greater degree. Morphing leads to complex transformations of the stimuli that are not concentrated at any particular spatial frequency band. Cell exchange preserves high spatial frequency details, but sometimes moves them into the "wrong" stimulus. The four manipulations also introduce high-frequency noise to differing degrees. Responses to test stimuli indicated that high and low spatial frequency information were both sufficient but not necessary to maintain discrimination performance in both species, but there were also species differences in relative sensitivity to higher and lower spatial frequency information.

The subcortical visual pathway to the amygdala has long been considered a rapid and crude stream for processing emotionally salient information that is reliant on low spatial frequency (LSF) information. Recently, research has called this LSF dependency into question. To resolve this debate, we take advantage of an anatomical hemiretinal asymmetry, whereby the nasal hemiretina sends a higher proportion of information through the subcortical pathway than the temporal hemiretina. We recorded brain activity using electroencephalography (EEG) in human participants (N = 40) while they completed a monocular viewing paradigm. Pairs of faces (one fearful and one neutral, or both neutral) were projected simultaneously to the nasal and temporal hemiretina in three contrast-equated blocks; faces filtered to display only (i) LSF, (ii) high spatial frequency (HSF), or (iii) unfiltered information (broadband spatial frequency; BSF). BSF fearful faces were found to produce a greater naso-temporal asymmetry, with greater N170 amplitudes evoked by BSF faces in the nasal field, compared to HSF faces. Conversely, the naso-temporal asymmetry for LSF fearful faces did not differ between BSF and HSF. Collectively, these findings provide crucial evidence that the subcortical pathway carries combined spatial frequency visual signals, with a potential bias against HSF content.

Visual response latency of X- and Y-cells in the dorsal lateral geniculate nucleus of the cat

Individuals with body dysmorphic disorder (BDD) may have perceptual distortions for their appearance. Previous studies suggest imbalances in detailed relative to configural/holistic visual processing when viewing faces. No study has investigated the neural correlates of processing non-symptom-related stimuli. The objective of this study was to determine whether individuals with BDD have abnormal patterns of brain activation when viewing non-face/non-body object stimuli. Fourteen medication-free participants with DSM-IV BDD and 14 healthy controls participated. We performed functional magnetic resonance imaging (fMRI) while participants matched photographs of houses that were unaltered, contained only high spatial frequency (HSF, high detail) information or only low spatial frequency (LSF, low detail) information. The primary outcome was group differences in blood oxygen level-dependent (BOLD) signal changes. The BDD group showed lower activity in the parahippocampal gyrus, lingual gyrus and precuneus for LSF images. There were greater activations in medial prefrontal regions for HSF images, although no significant differences when compared to a low-level baseline. Greater symptom severity was associated with lower activity in the dorsal occipital cortex and ventrolateral prefrontal cortex for normal spatial frequency (NSF) and HSF images. Individuals with BDD have abnormal brain activation patterns when viewing objects. Hypoactivity in visual association areas for configural and holistic (low detail) elements and abnormal allocation of prefrontal systems for details are consistent with a model of imbalances in global versus local processing. This may occur not only for appearance but also for general stimuli unrelated to their symptoms.

Pinpointing the optimal spatial frequency range for automatic neural facial fear processing

In age-related macular degeneration (AMD), the processing of fine details in a visual scene, based on a high spatial frequency processing, is impaired, while the processing of global shapes, based on a low spatial frequency processing, is relatively well preserved. The present fMRI study aimed to investigate the residual abilities and functional brain changes of spatial frequency processing in visual scenes in AMD patients. AMD patients and normally sighted elderly participants performed a categorization task using large black and white photographs of scenes (indoors vs. outdoors) filtered in low and high spatial frequencies, and nonfiltered. The study also explored the effect of luminance contrast on the processing of high spatial frequencies. The contrast across scenes was either unmodified or equalized using a root-mean-square contrast normalization in order to increase contrast in high-pass filtered scenes. Performance was lower for high-pass filtered scenes than for low-pass and nonfiltered scenes, for both AMD patients and controls. The deficit for processing high spatial frequencies was more pronounced in AMD patients than in controls and was associated with lower activity for patients than controls not only in the occipital areas dedicated to central and peripheral visual fields but also in a distant cerebral region specialized for scene perception, the parahippocampal place area. Increasing the contrast improved the processing of high spatial frequency content and spurred activation of the occipital cortex for AMD patients. These findings may lead to new perspectives for rehabilitation procedures for AMD patients.

Cerebral regions and hemispheric specialization for processing spatial frequencies during natural scene recognition. An event-related fMRI study

Low spatial frequency filtering modulates early brain processing of affective complex pictures

Understanding how the human visual system recognizes objects is one of the key challenges in neuroscience. Inspired by a large body of physiological evidence, a general class of recognition models has emerged, which is based on a hierarchical organization of visual processing, with succeeding stages being sensitive to image features of increasing complexity. However, these models appear to be incompatible with some well-known psychophysical results. Prominent among these are experiments investigating recognition impairments caused by vertical inversion of images, especially those of faces. It has been reported that faces that differ 'featurally' are much easier to distinguish when inverted than those that differ 'configurally'; a finding that is difficult to reconcile with the physiological models. Here, we show that after controlling for subjects' expectations, there is no difference between 'featurally' and 'configurally' transformed faces in terms of inversion effect. This result reinforces the plausibility of simple hierarchical models of object representation and recognition in the cortex.

People with schizophrenia demonstrate perceptual organization impairments, and these are thought to contribute to their face processing difficulties. We examined the neural substrates of emotionally neutral face processing in schizophrenia by investigating neural activity under three stimulus conditions: faces characterized by the full spectrum of spatial frequencies, faces with low spatial frequency information removed [high spatial frequency (HSF) condition], and faces with high spatial frequency information removed [low spatial frequency (LSF) condition]. Face perception in the HSF condition is more reliant on local feature processing whereas perception in the LSF condition requires greater reliance on global form processing. Past studies of perceptual organization in schizophrenia indicate that patients perform relatively more poorly with degraded stimuli but also that, when global information is absent, patients may perform better than controls because of their relatively increased ability to initially process individual features. Therefore, we hypothesized that people with schizophrenia (n=14) would demonstrate greater face processing difficulties than controls (n=13) in the LSF condition, whereas they would demonstrate a smaller difference or superior performance in the HSF condition. In a gender-discrimination task, behavioral data indicated high levels of accuracy for both groups, with a trend toward an interaction involving higher patient performance in the HSF condition and poorer patient performance in the LSF condition. Patients demonstrated greater activity in the fusiform gyrus compared to controls in both degraded conditions. These data suggest that impairments in basic integration abilities may be compensated for by relatively increased activity in this region.

The decomposition by the human visual system of visual scenes into a range of spatial frequencies is necessary for the categorization of the objects present in the visual scene. This decomposition of spatial frequencies may be particularly important for the processing of emotions. Experiments in the field of behavioral (Schyns & Oliva, 1999) and cognitive neuroscience (Vuilleumier, Armony, Driver, & Dolan, 2003) suggest that low spatial frequencies (LSF) are better than high spatial frequencies (HSF) for the categorization of emotional facial expressions (EFE). The aim of this study was to determine whether LSF information is more useful than HSF information for the categorization of emotions. We tested this hypothesis using artificial neural networks (ANN) subject to both unsupervised and supervised learning. The results indicated better emotion categorization with LSF information, thus suggesting that the HSF signal, which is also present in the BSF signal, acts as a source of noisy information during classification tasks in artificial neural systems.

Past research has suggested that mindfulness training reduces automaticity while processing socio-emotional stimuli. The present study aimed to analyze how mindfulness practice may reduce the use of prior knowledge during the recognition of emotional facial expressions. Based on a predictive brain model, we hypothesized that mindfulness practice would reduce the top-down processing of low spatial frequency information. This experiment compared the performance of a mindfulness group (n = 32) and a waitlist control group (n = 30) in an emotional Stroop task before and after an 8-week training course. The emotional Stroop task comprised two emotional facial expressions (joy or anger) topped with a congruent or incongruent word, and was primed by facial expressions filtered in two spatial frequency bands: high spatial frequency (HSF) or low spatial frequency (LSF). Having measured the reaction time, the results showed a significant interaction between group (mindfulness vs. control) and session (before vs. after training; p = 0.04; R2 = 0.001), irrespective of spatial frequency channels. Breaking down the interaction showed that mindfulness-trained participants responded significantly faster than the controls to any type of information. The interaction Group by Session by Priming was not significant. These results are in line with research underlining the effects of mindfulness-based interventions on global attentional control. More precisely, the global reduced reaction time did not support lower top-down predictive coding abilities specifically driven by low spatial frequency channels, but indicated a better general sensitivity to the perceptual environment.