Low Spatial Frequency Processing Research Articles

Towards a unified understanding of lateralized vision: A large-scale study investigating principles governing patterns of lateralization using a heterogeneous sample

While functional lateralization of the human brain has been a widely studied topic in the past decades, few studies to date have gone further than investigating lateralization of single, isolated processes. With the present study, we aimed to arrive at a more unified view by investigating lateralization patterns in face and word processing, and associated lower-level visual processing. We tested a large and heterogeneous participant group, and used a number of tasks that had been shown to produce replicable indices of lateralized processing of visual information of different types and complexity. Following Bayesian statistics, group-level analyses showed the expected right hemisphere (RH) lateralization for face, global form, low spatial frequency processing, and spatial attention, and left hemisphere (LH) lateralization for visual word and local feature processing. Compared to right-handed individuals, lateralization patterns of left-handed and especially those who are RH-dominant for language deviated from this ‘typical’ pattern. Our results support the notion that face and word processes come to be lateralized to homologue areas of the two hemispheres, under influence of the RH- and LH-specializations in global form, local feature, and low and high spatial frequency processing. As such, we present a more unified understanding of lateralized vision, providing evidence for the input asymmetry and causal complementarity principles of lateralized visual information processing. The absence of correlations between spatial attention and lateralization of the other processes supports the notion of their independent lateralization, conform the statistical complementarity principle.

Can the Cognitive Phenotype in Neurofibromatosis Type 1 (NF1) Be Explained by Neuroimaging? A Review.

Neurofibromatosis type 1 (NF1) is one of the most frequent monogenetic disorders. It can be associated with cognitive dysfunctions in several domains such as executive functioning, language, visual perception, motor skills, social skills, memory and/or attention. Neuroimaging is becoming more and more important for a clearer understanding of the neural basis of these deficits. In recent years, several studies have used different imaging techniques to examine structural, morphological and functional alterations in NF1 disease. They have shown that NF1 patients have specific brain characteristics such as Unidentified Bright Objects (UBOs), macrocephaly, a higher volume of subcortical structures, microstructure integrity alterations, or connectivity alterations. In this review, which focuses on the studies published after the last 2 reviews of this topic (in 2010 and 2011), we report on recent structural, morphological and functional neuroimaging studies in NF1 subjects, with special focus on those that examine the neural basis of the NF1 cognitive phenotype. Although UBOs are one of the most obvious and visible elements in brain imaging, correlation studies have failed to establish a robust and reproducible link between major cognitive deficits in NF1 and their presence, number or localization. In the same vein, the results among structural studies are not consistent. Functional magnetic resonance imaging (fMRI) studies appear to be more sensitive, especially for understanding the executive function deficit that seems to be associated with a dysfunction in the right inferior frontal areas and the middle frontal areas. Similarly, fMRI studies have found that visuospatial deficits could be associated with a dysfunction in the visual cortex and especially in the magnocellular pathway involved in the processing of low spatial frequency and high temporal frequency. Connectivity studies have shown a reduction in anterior-posterior “long-range” connectivity and a deficit in deactivation in default mode network (DMN) during cognitive tasks. In conclusion, despite the contribution of new imaging techniques and despite relative advancement, the cognitive phenotype of NF1 patients is not totally understood.

Influence of peripheral vision on object categorization in central vision

Predictive models of visual recognition state that predictions based on the rapid processing of low spatial frequencies (LSF) may guide the subsequent processing of high spatial frequencies (HSF). While the HSF signal necessarily comes from central vision, most of the LSF signal comes from peripheral vision. The present study aimed at understanding how LSF in peripheral vision may be used to generate predictive signals that guide visual processes in central vision. In two experiments, participants performed an object categorization task in central vision while a semantically congruent or incongruent scene background was displayed in peripheral vision. In Experiment 1, results showed a congruence effect when the peripheral scene was displayed before the object onset. In Experiment 2, results showed a congruence effect only when the peripheral scene was intact, thus carrying a semantic meaning, but not when it was phase-scrambled, thus carrying only low-level information. The study suggests that the low resolution of peripheral vision facilitates the processing of foveated objects in the visual scene, in line with predictive models of visual recognition.

Age-related macular degeneration changes the processing of visual scenes in the brain.

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.

Insensitivity to Fearful Emotion for Early ERP Components in High Autistic Tendency Is Associated with Lower Magnocellular Efficiency.

Low spatial frequency (LSF) visual information is extracted rapidly from fearful faces, suggesting magnocellular involvement. Autistic phenotypes demonstrate altered magnocellular processing, which we propose contributes to a decreased P100 evoked response to LSF fearful faces. Here, we investigated whether rapid processing of fearful facial expressions differs for groups of neurotypical adults with low and high scores on the Autistic Spectrum Quotient (AQ). We created hybrid face stimuli with low and high spatial frequency filtered, fearful, and neutral expressions. Fearful faces produced higher amplitude P100 responses than neutral faces in the low AQ group, particularly when the hybrid face contained a LSF fearful expression. By contrast, there was no effect of fearful expression on P100 amplitude in the high AQ group. Consistent with evidence linking magnocellular differences with autistic personality traits, our non-linear VEP results showed that the high AQ group had higher amplitude K2.1 responses than the low AQ group, which is indicative of less efficient magnocellular recovery. Our results suggest that magnocellular LSF processing of a human face may be the initial visual cue used to rapidly and automatically detect fear, but that this cue functions atypically in those with high autistic tendency.

The Neural Bases of the Semantic Interference of Spatial Frequency-based Information in Scenes.

Current models of visual perception suggest that during scene categorization, low spatial frequencies (LSF) are processed rapidly and activate plausible interpretations of visual input. This coarse analysis would then be used to guide subsequent processing of high spatial frequencies (HSF). The present fMRI study examined how processing of LSF may influence that of HSF by investigating the neural bases of the semantic interference effect. We used hybrid scenes as stimuli by combining LSF and HSF from two different scenes, and participants had to categorize the HSF scene. Categorization was impaired when LSF and HSF scenes were semantically dissimilar, suggesting that the LSF scene was processed automatically and interfered with categorization of the HSF scene. fMRI results revealed that this semantic interference effect was associated with increased activation in the inferior frontal gyrus, the superior parietal lobules, and the fusiform and parahippocampal gyri. Furthermore, a connectivity analysis (psychophysiological interaction) revealed that the semantic interference effect resulted in increasing connectivity between the right fusiform and the right inferior frontal gyri. Results support influential models suggesting that, during scene categorization, LSF information is processed rapidly in the pFC and activates plausible interpretations of the scene category. These coarse predictions would then initiate top-down influences on recognition-related areas of the inferotemporal cortex, and these could interfere with the categorization of HSF information in case of semantic dissimilarity to LSF.

Attention to local and global levels of hierarchical Navon figures affects rapid scene categorization.

In four experiments, we investigated how attention to local and global levels of hierarchical Navon figures affected the selection of diagnostic spatial scale information used in scene categorization. We explored this issue by asking observers to classify hybrid images (i.e., images that contain low spatial frequency (LSF) content of one image, and high spatial frequency (HSF) content from a second image) immediately following global and local Navon tasks. Hybrid images can be classified according to either their LSF, or HSF content; thus, making them ideal for investigating diagnostic spatial scale preference. Although observers were sensitive to both spatial scales (Experiment 1), they overwhelmingly preferred to classify hybrids based on LSF content (Experiment 2). In Experiment 3, we demonstrated that LSF based hybrid categorization was faster following global Navon tasks, suggesting that LSF processing associated with global Navon tasks primed the selection of LSFs in hybrid images. In Experiment 4, replicating Experiment 3 but suppressing the LSF information in Navon letters by contrast balancing the stimuli examined this hypothesis. Similar to Experiment 3, observers preferred to classify hybrids based on LSF content; however and in contrast, LSF based hybrid categorization was slower following global than local Navon tasks.

Affective and contextual values modulate spatial frequency use in object recognition.

Visual object recognition is of fundamental importance in our everyday interaction with the environment. Recent models of visual perception emphasize the role of top-down predictions facilitating object recognition via initial guesses that limit the number of object representations that need to be considered. Several results suggest that this rapid and efficient object processing relies on the early extraction and processing of low spatial frequencies (LSF). The present study aimed to investigate the SF content of visual object representations and its modulation by contextual and affective values of the perceived object during a picture-name verification task. Stimuli consisted of pictures of objects equalized in SF content and categorized as having low or high affective and contextual values. To access the SF content of stored visual representations of objects, SFs of each image were then randomly sampled on a trial-by-trial basis. Results reveal that intermediate SFs between 14 and 24 cycles per object (2.3–4 cycles per degree) are correlated with fast and accurate identification for all categories of objects. Moreover, there was a significant interaction between affective and contextual values over the SFs correlating with fast recognition. These results suggest that affective and contextual values of a visual object modulate the SF content of its internal representation, thus highlighting the flexibility of the visual recognition system.

Task and spatial frequency modulations of object processing: an EEG study.

Visual object processing may follow a coarse-to-fine sequence imposed by fast processing of low spatial frequencies (LSF) and slow processing of high spatial frequencies (HSF). Objects can be categorized at varying levels of specificity: the superordinate (e.g. animal), the basic (e.g. dog), or the subordinate (e.g. Border Collie). We tested whether superordinate and more specific categorization depend on different spatial frequency ranges, and whether any such dependencies might be revealed by or influence signals recorded using EEG. We used event-related potentials (ERPs) and time-frequency (TF) analysis to examine the time course of object processing while participants performed either a grammatical gender-classification task (which generally forces basic-level categorization) or a living/non-living judgement (superordinate categorization) on everyday, real-life objects. Objects were filtered to contain only HSF or LSF. We found a greater positivity and greater negativity for HSF than for LSF pictures in the P1 and N1 respectively, but no effects of task on either component. A later, fronto-central negativity (N350) was more negative in the gender-classification task than the superordinate categorization task, which may indicate that this component relates to semantic or syntactic processing. We found no significant effects of task or spatial frequency on evoked or total gamma band responses. Our results demonstrate early differences in processing of HSF and LSF content that were not modulated by categorization task, with later responses reflecting such higher-level cognitive factors.

Reach trajectories reveal delayed processing of low spatial frequency faces in developmental prosopagnosia

Developmental prosopagnosia (DP) is characterized by a selective deficit in face recognition despite normal cognitive and neurological functioning. Previous research has established configural processing deficits in DP subjects. Low spatial frequency (LSF) information subserves configural face processing. Using hybrid stimuli, here we examined the evolution of perceptual dynamics and integration of LSF information by DP subjects while they pointed to high spatial frequency (HSF) face targets. Permutation analysis revealed a 230-ms delay in LSF processing by DP subjects as compared to controls. This delayed processing is likely to contribute to the difficulties associated with face recognition in DP subjects and is reflective of their alleged reliance on local rather than global features in face perception. These results suggest that quick and efficient processing of LSF information is critical for the development of normal face perception.

Enabling global processing in simultanagnosia by psychophysical biasing of visual pathways

A fundamental aspect of visual cognition is our disposition to see the 'forest before the trees'. However, damage to the posterior parietal cortex, a critical brain region along the dorsal visual pathway, can produce a neurological disorder called simultanagnosia, characterized by a debilitating inability to perceive the 'forest' but not the 'trees' (i.e. impaired global processing despite intact local processing). This impairment in perceiving the global shape persists even though the ventral visual pathway, the primary recognition pathway, is intact in these patients. Here, we enabled global processing in patients with simultanagnosia using a psychophysical technique, which allowed us to bias stimuli such that they are processed predominantly by the intact ventral visual pathway. Our findings reveal that the impairment in global processing that characterizes simultanagnosia stems from a disruption in the processing of low-spatial frequencies through the dorsal pathway. These findings advance our understanding of the relationship between visuospatial attention and perception and reveal the neural mechanism mediating the disposition to see the 'forest before the trees'.

Sounds prevent selective monitoring of high spatial frequency channels in vision

Prior knowledge about the spatial frequency (SF) of upcoming visual targets (Gabor patches) speeds up average reaction times and decreases standard deviation. This has often been regarded as evidence for a multichannel processing of SF in vision. Multisensory research, on the other hand, has often reported the existence of sensory interactions between auditory and visual signals. These interactions result in enhancements in visual processing, leading to lower sensory thresholds and/or more precise visual estimates. However, little is known about how multisensory interactions may affect the uncertainty regarding visual SF. We conducted a reaction time study in which we manipulated the uncertanty about SF (SF was blocked or interleaved across trials) of visual targets, and compared visual only versus audio–visual presentations. Surprisingly, the analysis of the reaction times and their standard deviation revealed an impairment of the selective monitoring of the SF channel by the presence of a concurrent sound. Moreover, this impairment was especially pronounced when the relevant channels were high SFs at high visual contrasts. We propose that an accessory sound automatically favours visual processing of low SFs through the magnocellular channels, thereby detracting from the potential benefits from tuning into high SF psychophysical-channels.

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

Distinct visual pathways are selectively tuned for processing specific spatial frequencies. Recently, Awasthi, Friedman, and Williams (2011) reported fast categorisation of faces at periphery, arguing for primacy of low spatial frequency (LSF) information in face processing. However, previous studies have also documented rapid categorization of places and natural scenes. Here, we tested if the LSF advantage is face specific or also involved in place perception. We used visually guided reaching as a continuous behavioral measure to examine the processing of LSF and high spatial frequency (HSF) hybrids, presented at the periphery. Subjects reached out and touched targets and their movements were recorded. The trajectories revealed that LSF interference was both 95ms earlier and stronger for faces than places and was lateralized to the left visual field. The early processing of LSF information supports the assumption that faces are prioritised and provides a (neural) framework for such specialised processing.

Processing of low spatial frequency faces at periphery in choice reaching tasks

Various aspects of face processing have been associated with distinct ranges of spatial frequencies. Configural processing of faces depends chiefly on low spatial frequency (LSF) information whereas high spatial frequency (HSF) supports feature based processing. However, it has also been argued that face processing has a foveal-bias (HSF channels dominate the fovea). Here we used reach trajectories as a continuous behavioral measure to study perceptual processing of faces. Experimental stimuli were LSF–HSF hybrids of male and female faces superimposed and were presented peripherally and centrally. Subject reached out to touch a specified sex and their movements were recorded. The reaching trajectories reveal that there is less effect of (interference by) LSF faces at fovea as compared to periphery while reaching to HSF targets. These results demonstrate that peripherally presented LSF information, carried chiefly by magnocellular channels, enables efficient processing of faces, possibly via a retinotectal (subcortical) pathway.

Parallel development of contour integration and visual contrast sensitivity at low spatial frequencies

Abstract It has been suggested that visual contrast sensitivity and contour integration functions exhibit a late maturation during adolescence. However, the relationship between these functions has not been investigated. The aim of this study was to assess the development of visual contrast sensitivity and contour integration in 152 healthy volunteers aged between 5 and 30 years. The results revealed a significant maturation of contrast sensitivity at low spatial frequencies (0.5, 1.2, and 1.9 cycles/degree) and contour integration. The largest developmental step was observed for both contrast sensitivity and contour integration tasks when the 5–8-year olds were compared with the 9–11-year olds. There was a significant correlation between the development of low spatial frequency contrast sensitivity and contour integration. These results raise the possibility that the development of low spatial frequency processing may affect attentional mechanisms, which may have an impact on early contour integration.

From Coarse to Fine? Spatial and Temporal Dynamics of Cortical Face Processing

Primary vision segregates information along 2 main dimensions: orientation and spatial frequency (SF). An important question is how this primary visual information is integrated to support high-level representations. It is generally assumed that the information carried by different SF is combined following a coarse-to-fine sequence. We directly addressed this assumption by investigating how the network of face-preferring cortical regions processes distinct SF over time. Face stimuli were flashed during 75, 150, or 300 ms and masked. They were filtered to preserve low SF (LSF), middle SF (MSF), or high SF (HSF). Most face-preferring regions robustly responded to coarse LSF, face information in early stages of visual processing (i.e., until 75 ms of exposure duration). LSF processing decayed as a function of exposure duration (mostly until 150 ms). In contrast, the processing of fine HSF, face information became more robust over time in the bilateral fusiform face regions and in the right occipital face area. The present evidence suggests the coarse-to-fine strategy as a plausible modus operandi in high-level visual cortex.

Is the early modulation of brain activity by fearful facial expressions primarily mediated by coarse low spatial frequency information?

Rapidly decoding the emotional content of a face is an important skill for successful social behavior. Several Event Related brain Potential (ERP) have indicated that emotional expressions already influence brain activity as early as 100 ms. Some studies hypothesized that this early brain response to fear depends on coarse-magnocellular inputs, which are primarily driven by Low Spatial Frequency (LSF) cues. Until now however, evidence is inconclusive probably due to the divergent methods used to match luminance and contrast across spatial frequencies and emotional stimuli. In the present study, we measured ERPs to LSF and HSF faces with fearful or neutral expressions when contrast and luminance was matched across SF or not. Our findings clearly show that fearful facial expressions increases the amplitude of P1 (only for contrast-luminance equated images) and N170 in comparison to neutral faces but only in LSF faces, irrespective of contrast or luminance equalization, further suggesting that LSF information plays a crucial role in the early brain responses to fear. Furthermore, we found that, irrespective of luminance or contrast equalization, N170 occurred faster when perceiving LSF faces than HSF faces, again emphasizing the primacy of LSF processing in early face perception.

Abnormal spatial frequency processing in high-functioning children with pervasive developmental disorder (PDD)

Objective Basic abnormalities in visual information processing could be associated with the local visual bias often found in subjects with PDD. Therefore, the present study investigated the existence of deficits in spatial frequency processing at an early sensory level in children with PDD. Methods Visual evoked potentials (VEPs) and VEP dipole sources elicited by high and low spatial frequency gratings were analyzed in high-functioning children with PDD and matched controls. Results Around 80 ms (N80-latency) children with PDD did not show the same robust differences between high and low spatial frequencies in VEP amplitude and VEP brain sources as controls, because of atypical processing of high frequencies. Analyses at the P1-latency (130 ms) revealed that, although similar inferior–medial brain sources were activated for the processing of both spatial frequencies in the PDD and control group, source strength in response to both frequencies was weaker in the PDD compared to control group. Moreover, additional superior–lateral brain sources were activated during the processing of both frequencies in the PDD group. Conclusions Decreased specialized processing of high and low spatial frequencies might be a robust characteristic of PDD. Early in processing abnormalities in high spatial frequency processing seem to occur in PDD. At a later phase in processing there seems to be both atypical high and low spatial frequency processing. Considering that the processing of specific spatial frequencies plays an important role in the processing of global and local aspects of hierarchical stimuli and faces and of emotions, present data suggest that peculiarities in PDD subjects with respect to these stimuli might be related to an abnormality in more fundamental visual processes. Significance A basic abnormality in visual frequency processing is established in children with PDD.

Hemispheric processing of categorical and coordinate spatial relations in the absence of low spatial frequencies.

Right-handed participants performed the categorical and coordinate spatial relation judgments on stimuli presented to either the left visual field - right hemisphere (LVF-RH) or the right visual field - left hemisphere (RVF-LH). The stimulus patterns were formulated either by bright dots or contrast-balanced dots. When the stimuli were bright, an RVF-LH advantage was observed for the categorical task, whereas an LVF-RH advantage was observed for the coordinate task. When the stimuli were contrast balanced, the RVF-LH advantage was observed for the categorical task, but the LVF-RH advantage was eliminated for the coordinate task. Because the contrast-balanced dots are largely devoid by of low spatial frequency content, these results suggest that processing of low spatial frequency is responsible for the right hemisphere advantage for the coordinate spatial processing.

Temporal integration of form as a function of subject handedness and retinal locus of presentation

Two experiments are reported examining differences in perceptual processing as a function of subject handedness. Experiment 1 compared performance in the left vs right visual fields of right-vs left-handed subjects. Only right-handed subjects exhibited an interaction of visual field with spatial frequency (as mediated by interflash interval), suggesting that left-handers are not differentially lateralized for high vs low spatial frequency processing. Experiment 2 examined foveal performance in left-handers vs right-handers with or without familial sinistrality. Subjects with personal or familial sinistrality exhibited superior performance when the processing of low frequencies was required, suggesting that sinistrality may confer an advantage in the processing of lower spatial frequencies.