Abnormal visual motion processing in schizophrenia: a review of research progress

Motion processing represents a perceptual domain in which dynamic visual information is encoded to support the perception of movement. Research over the last decade has found a variety of abnormalities in the processing of motion information in schizophrenia. The abnormalities span from discrimination of basic motion features (such as speed) to integration of spatially distributed motion signals (such as coherent motion). Motion processing involves visual signals across space and time and thus presents a special opportunity to examine how spatial and temporal information is integrated in the visual system. This article surveys the behavioral and neuroimaging studies that probe into the spatial integration of motion information in schizophrenia. An emerging theme from these studies points to an imbalanced regulation of spatial interaction processes as a potential mechanism mediating different levels of abnormal motion processing in schizophrenia. The synthesis of these mechanism-driven studies suggests that further investigation of the neural basis and functional consequences of this abnormal motion processing are needed in order to render a basic biomarker for assessment and intervention of cognitive dysfunction in this mental disorder.     

Evolution of neural processing for visual perception in vertebrates

Visual perception requires both visual information and attention. This review compares, across classes of vertebrates, the functional and anatomical characteristics of (a) the neural pathways that process visual information about objects, and (b) stimulus selection pathways that determine the objects to which an animal attends. Early in the evolution of vertebrate species, visual perception was dominated by information transmitted via the midbrain (retinotectal) visual pathway, and attention was probably controlled primarily by a selection network in the midbrain. In contrast, in primates, visual perception is dominated by information transmitted via the forebrain (retinogeniculate) visual pathway, and attention is mediated largely by networks in the forebrain. In birds and nonprimate mammals, both the retinotectal and retinogeniculate pathways contribute critically to visual information processing, and both midbrain and forebrain networks play important roles in controlling attention. The computations and processing strategies in birds and mammals share some strikingly similar characteristics despite over 300 million years of independent evolution and being implemented by distinct brain architectures. The similarity of these functional characteristics suggests that they provide valuable advantages to visual perception in advanced visual systems. A schema is proposed that describes the evolution of the pathways and computations that enable visual perception in vertebrate species.     

Submillisecond unmasked subliminal visual stimuli evoke electrical brain responses

Subliminal perception is strongly associated to the processing of meaningful or emotional information and has mostly been studied using visual masking. In this study, we used high density 256‐channel EEG coupled with an liquid crystal display (LCD) tachistoscope to characterize the spatio‐temporal dynamics of the brain response to visual checkerboard stimuli (Experiment 1) or blank stimuli (Experiment 2) presented without a mask for 1 ms (visible), 500 µs (partially visible), and 250 µs (subliminal) by applying time‐wise, assumption‐free nonparametric randomization statistics on the strength and on the topography of high‐density scalp‐recorded electric field. Stimulus visibility was assessed in a third separate behavioral experiment. Results revealed that unmasked checkerboards presented subliminally for 250 µs evoked weak but detectable visual evoked potential (VEP) responses. When the checkerboards were replaced by blank stimuli, there was no evidence for the presence of an evoked response anymore. Furthermore, the checkerboard VEPs were modulated topographically between 243 and 296 ms post‐stimulus onset as a function of stimulus duration, indicative of the engagement of distinct configuration of active brain networks. A distributed electrical source analysis localized this modulation within the right superior parietal lobule near the precuneus. These results show the presence of a brain response to submillisecond unmasked subliminal visual stimuli independently of their emotional saliency or meaningfulness and opens an avenue for new investigations of subliminal stimulation without using visual masking. Hum Brain Mapp 36:1470–1483, 2015. © 2014 Wiley Periodicals, Inc.     

Separate spatial and temporal frequency tuning to visual motion in human MT+ measured with ECoG

The human middle temporal complex (hMT+) has a crucial biological relevance for the processing and detection of direction and speed of motion in visual stimuli. Here, we characterized how neuronal populations in hMT+ encode the speed of moving visual stimuli. We evaluated human intracranial electrocorticography (ECoG) responses elicited by square‐wave dartboard moving stimuli with different spatial and temporal frequency to investigate whether hMT+ neuronal populations encode the stimulus speed directly, or whether they separate motion into its spatial and temporal components. We extracted two components from the ECoG responses: (1) the power in the high‐frequency band (HFB: 65–95 Hz) as a measure of the neuronal population spiking activity and (2) a specific spectral component that followed the frequency of the stimulus's contrast reversals (SCR responses). Our results revealed that HFB neuronal population responses to visual motion stimuli exhibit distinct and independent selectivity for spatial and temporal frequencies of the visual stimuli rather than direct speed tuning. The SCR responses did not encode the speed or the spatiotemporal frequency of the visual stimuli. We conclude that the neuronal populations measured in hMT+ are not directly tuned to stimulus speed, but instead encode speed through separate and independent spatial and temporal frequency tuning. Hum Brain Mapp 38:293–307, 2017. © 2016 Wiley Periodicals, Inc.     

Specificity of regions processing biological motion

Using functional magnetic resonance imaging and point light displays portraying six different human actions, we were able to show that several visual cortical regions, including human MT/V5 complex, posterior inferior temporal gyrus and superior temporal sulcus, are differentially active in the subtraction comparing biological motion to scrambled motion. Comparison of biological motion to three-dimensional rotation (of a human figure), articulated motion and translation suggests that human superior temporal sulcus activity reflects the action portrayed in the biological motion stimuli, whereas posterior inferior temporal gyrus responds to the figure and hMT/V5+ to the complex motion pattern present in biological motion stimuli. These results were confirmed with implied action stimuli.     

Lack of visual evoked potentials amplitude decrement during prolonged reversal and motion stimulation in migraineurs

ObjectiveWe evaluated response decrement during a short time repetitive low and high contrast reversal and low contrast motion stimulation in controls and migraineurs.MethodsA total of 39 migraine patients (out of which 19 were in the interictal period and without prophylactic treatment) and 36 healthy volunteers were examined using pattern-reversal (PR-VEP) and motion-onset (M-VEP) visual evoked potentials. Binocular stimulation lasted 2.5 min and the decrement assessment was blinded.ResultsEvidence of significant decrement was observed in healthy volunteers for high contrast PR-VEP amplitude of P100-N75 ratios between the fifth and first blocks (0.9; p = 0.001) with a linear decline (−0.7 μV/min, p = 0.001) and in the P100-N145 amplitude with linear decline (−0.5 μV/min, p = 0.004). Significant decrement was also observed for the ratio between the fifth and first block P1-N2 amplitudes in M-VEP (0.9, p = 0.006). No significant decrement was noted in the low contrast PR-VEP or among migraineurs.ConclusionsWe confirm differences in decrease of VEPs amplitude during short term examination between controls and migraineurs. We showed the decrement deficit also in the extrastriatal regions of the migraineurs’ visual cortex.SignificanceLow contrast and motion-onset stimuli in short time decrement assessment did not increase the test sensitivity.     

Early visual processing in neglect patients: A study with steady-state VEPs

Reliable steady-state visual evoked potentials (VEPs) were recorded in a group of 19 right brain-damaged patients with visuospatial hemineglect (Neglect), and two control groups: 15 left brain-damaged (LBD) patients and 12 right brain-damaged (RBD) patients without neglect. Moreover, VEPs were recorded in two rare cases of left brain damage and right visuospatial hemineglect. Stimuli were gratings phase-reversed at various temporal frequencies presented in the left and right visual field. In the Neglect group, VEPs to stimuli displayed in the left visual field (contralesional stimuli) had longer latencies. The delay was not present for the two control groups. As regards the VEP amplitudes, the Neglect group data showed a less distinctive pattern than in the case of latency. VEPs to stimuli contralateral to the lesion were smaller than those recorded for stimuli ipsilateral to the lesion in both Neglect and RBD groups. On the contrary, the VEP amplitudes for the two hemifields were comparable in the LBD group. In the case of left brain damage and neglect, VEPs to right visual field stimuli had longer latencies and lower amplitudes compared to the ipsilesional responses in both patients. Overall, the data support the view that, in most cases, early visual processing is not intact in the neglected hemifield.     

Age-related changes in the dynamics of human albino visual pathways

A deficiency of melanin in the retinal pigment epithelium, which regulates the development of neural retina, leads to chiasmal misrouting such that the uncrossed pathway (to the ipsilateral hemisphere) is reduced relative to the crossed pathway (to the contralateral hemisphere). This study examines age-related changes in the flash and pattern appearance visual evoked potentials (VEP) of human albinos. Scalp recorded cortical VEPs to flash (FVEP) and pattern appearance stimulation were recorded in 58 albino (8 months to 60 years) and 34 normal subjects (4-55 years). VEPs were analysed by amplitude and latency. The contralateral hemisphere FVEP amplitude decreased with age in albino subjects, as in both hemispheres in normals. However, the ipsilateral hemisphere FVEP amplitude was significantly lower in young albino subjects, initially giving a marked interhemispheric asymmetry, but this normalized with age. Significant interhemispheric FVEP latency asymmetries were not observed. The contralateral pattern appearance VEP latency in albino subjects decreased with age, as in both hemispheres in normals; the ipsilateral latency increased significantly with age. Significant interhemispheric pattern appearance VEP amplitude asymmetries were not observed. These novel and unexpected observations indicate significant age-related changes in the retinocortical pathways of the human albino. These changes have implications for our understanding of development and plasticity of the central visual pathways.     

A robust and representative lower bound on object processing speed in humans

How early does the brain decode object categories? Addressing this question is critical to constrain the type of neuronal architecture supporting object categorization. In this context, much effort has been devoted to estimating face processing speed. With onsets estimated from 50 to 150 ms, the timing of the first face‐sensitive responses in humans remains controversial. This controversy is due partially to the susceptibility of dynamic brain measurements to filtering distortions and analysis issues. Here, using distributions of single‐trial event‐related potentials (ERPs), causal filtering, statistical analyses at all electrodes and time points, and effective correction for multiple comparisons, we present evidence that the earliest categorical differences start around 90 ms following stimulus presentation. These results were obtained from a representative group of 120 participants, aged 18–81, who categorized images of faces and noise textures. The results were reliable across testing days, as determined by test–retest assessment in 74 of the participants. Furthermore, a control experiment showed similar ERP onsets for contrasts involving images of houses or white noise. Face onsets did not change with age, suggesting that face sensitivity occurs within 100 ms across the adult lifespan. Finally, the simplicity of the face–texture contrast, and the dominant midline distribution of the effects, suggest the face responses were evoked by relatively simple image properties and are not face specific. Our results provide a new lower benchmark for the earliest neuronal responses to complex objects in the human visual system.     

Altered cortical visual processing in individuals with a spreading photoparoxysmal EEG response

Photosensitive individuals respond with epileptiform electroencephalography (EEG) discharges to intermittent photic stimulation. The pathogenetic mechanisms underlying this photoparoxysmal response (PPR) remain to be clarified. We investigated the involvement of magnocellular and parvocellular pathways in the processing of nonprovocative visual stimuli in healthy subjects with different phenotypic expressions of PPR (15 individuals with a local PPR, i.e. occipital discharges only, and 15 with a PPR propagating to anterior brain regions) and in 17 PPR-negative healthy controls using pattern-reversal visual evoked potentials (VEP). Checkerboard stimulation was performed at a low and a high spatial frequency to preferentially activate the magnocellular and parvocellular pathways. VEP habituation was also assessed over 15 blocks (each 100 trials) of recording. PPR-positive individuals with propagating PPR showed an increase in the N75-P100 and P100-N135 VEP components for both spatial frequencies, whereas individuals with a local PPR had normal VEP amplitudes. Individuals with propagating PPR also showed a stronger VEP habituation and reported more aversive sensations during continuous visual stimulation with the high spatial frequency checkerboard. The selective increase in VEP amplitudes in individuals with propagating PPR corroborates the notion that PPR with propagation is pathophysiologically distinct from local PPR. The increase in VEP amplitudes was independent of the spatial frequency of visual stimulation, indicating an increased neuronal excitability in both the parvocellular and magnocellular pathways. The stronger habituation in these individuals may reflect a compensatory mechanism to stabilize excitability in the visual system.     

Somatosensory and visual evoked potentials in children with cerebral palsy: Correlations and discrepancies with MRI findings and clinical picture

Purpose: To determine if there is any association between the findings of visual evoked potentials (VEPs), somatosensory evoked potentials (SEPs), and magnetic resonance imaging (MRI) findings with the neurodevelopment and severity in children with cerebral palsy (CP). Methods: The present study included 15 children with spastic diplegic CP and five children with spastic hemiplegic CP and 42 healthy children as controls. The number of the controls was two-times greater than the study group to increase statistical power of this study. VEPs and SEPs were recorded in the CP children and compared with healthy controls. All MR scans were obtained using a 1.5 T MR scanner. Results: A significant difference was found in the latencies P100 (VEP) between the CP and controls. No correlations between increased P100 latencies and asphyxia, prematurity, the CP severity, MRI findings and mental retardation were noted. A significant difference in N13–N20 conductions (SEPs) between the subjects with CP and the control group was found. SEPs were positively correlated with mental retardation in CP children. The brain lesions in MRI showed a significant correlation with the CP severity scores and mental retardation. Conclusion: The differences in VEPs and SEPs were determined between CP children and healthy children. The MRI findings were positively correlated with the CP severity and mental retardation.     

Mechanisms of human motion perception: combining evidence from evoked potentials, behavioural performance and computational modelling

Based on single cell recordings in monkey, it has been suggested that neural activity can be related directly to psychophysically measured threshold behaviour. Here, we investigated in humans whether evoked potentials correlate with behavioural measurements like discrimination thresholds and reaction time. Subjects were asked to report the perceived direction of object motion stimuli which contained variable amounts of coherent motion. Simultaneously, we recorded evoked potentials with a multielectrode array, or measured the reaction time. We show here that motion coherence had a strong influence on both amplitude and latency of the evoked potential. Stronger motion signals evoked stronger and faster cortical responses. The latency reduction of the motion onset response with increasing coherence correlated very well with the concurrent decrease in reaction time. Taken together, these results suggest that temporal integration is an important step in analysing motion signals to generate a reliable behavioural response. We stimulated a two-dimensional array of correlation-type motion detectors with the same motion sequences, and analysed the distribution of local motion signals according to signal detection theory. Performance resembled that of human subjects when the decision strategy was optimized so as to exclude small signals and, in particular, when the ideal observer had some knowledge about a region of interest in which the object was to be expected.     

Brief report: postural reactivity to fast visual motion differentiates autistic from children with Asperger syndrome

The aim of the present study was to search for a sensorimotor marker (i.e., visuopostural tuning) that could be correlated with the severity of motor impairments in children with autistic spectrum disorders. Given that autistic children were previously reported to be posturally hypo-reactive to visually perceived environmental motion in comparison with normal control children (Gepner et al., 1995), we sought to determine whether children with Asperger syndrome (AS) would share the same postural hyporeactivity to visual motion. Three autistic children with mild to severe motor impairments, three AS children with soft motor signs, and nine normal control children were tested for overall postural instability and postural reactivity to environmental motion. Results indicate, first, that overall postural instability is significantly reduced in autistic children compared with both AS and normal children. Second, although postural oscillations in the fore-aft axis become more attuned to the oscillation frequency of an immersive dynamic visual display as visual speed is increased, in both control and AS subjects, this is not the case in autistic children. Despite the small number of subjects tested in this study, our data confirm the existence of a visuopostural detuning in autistic children. Third, they argue for a correlation between visuopostural tuning and severity of motor signs in children with autistic spectrum disorders. Finally, they suggest a differentiation between children with autism and children with AS with regard to postural reactivity to fast visual motion. Neurophysiological implications of these results are discussed. In particular, a visuocerebellar pathway deficit hypothesis in autism is proposed.     

A neural architecture for visual motion perception: Group and element apparent motion

A neural network model of motion segmentation by visual cortex is described. The model's properties are illustrated by simulating on the computer data concerning group and element apparent motion, including the tendency for group motion to occur at longer ISIs and under conditions of short visual persistence. These phenomena challenge recent vision models because the switch between group and element motion is determined by changing the timing of image displays whose elements flash on and off but do not otherwise move through time. The model clarifies the dependence of short-range and long-range motion on a spatial scale. Its design specifies how sustained response cells and transient response cells cooperate and compete in successive processing stages to generate motion signals that are sensitive to direction-of-motion, yet insensitive to direction-of-contrast. Properties of beta motion, phi motion, gamma motion, and Ternus motion are explained. A number of prior motion models are clarified, transformed, and unified, including the Reichardt model, Marr-Ullman model, Burt-Sperling model, Nakayama-Loomis model, and NADEL model. Apparent motion and real motion generate testably different model properties. The model clarifies how preprocessing of motion signals by a motion OC Filter is joined to long-range cooperative motion mechanisms in a motion CC Loop to control phenomena such as induced motion, motion capture, and motion after effects. The total model system is a motion Boundary Contour System (BCS) that is computed in parallel with the static BCS of Grossberg and Mingolla before both systems cooperate to generate a boundary representation for 3-D visual form perception.     

Pain influences hedonic assessment of visual inputs

It is acknowledged that the emotional state created by visual inputs can modulate the way we feel pain; however, little is known about how acute pain influences the emotional assessment of what we see. In this study healthy subjects scored affective images while receiving painful or innocuous electrical shocks. Painful stimuli did not make unpleasant images more unpleasant, but rendered pleasant pictures significantly less pleasant. Brain responses to visual inputs (64-channels electroencephalogram) mirrored behavioural results, showing pain-induced effects in the orbitofrontal cortex, the subgenual portion of the cingulate gyrus, the anterior prefrontal and the temporal cortices, exclusively during presentation of pleasant images. In addition to this specific effect on pleasant pictures, pain also produced non-specific effects upon all categories of images, engaging cerebral areas associated with attention, alertness and motor preparation (middle-cingulate, supplemental motor, prefrontal cortex). Thus, pain appears to have a dual influence on visual processing: a non-specific effect related to orienting phenomena; and a more specific action exerted on supra-modal limbic areas involved in the production of affective states. The latter correlated with changes in the subjective appraisal of visual stimuli, and may underlie not only the change in their subjective assessment but also reactive processes aimed at coping with unpleasant contexts.     

Comparative study of visual evoked potentials in spinocerebellar ataxias and multiple sclerosis

Visual evoked potentials (VEPs) were delayed in 11 out of 18 patients with Friedreich's ataxia, in 1 out of 8 patients with Strumpell's hereditary spastic ataxia, in 2 out of 5 cases with cerebellar atrophy and in 42 out of 50 patients with multiple sclerosis (MS). Responses were normal in 5 cases with Pierre Marie's disease. Amplitude and temporal dispersion were statistically analyzed in the above-mentioned groups of patients with respect to controls. An abnormal temporal dispersion, also considered as interpeak N1P2, was frequently found in MS but only occasionally in spinocerebellar ataxias. Amplitude was statistically reduced in Friedreich's ataxia group, where an inverse relationship between latency and amplitude was found. No relation was found between VEP delay and duration of the disease, in any group considered.     

Role of primary visual cortex in the binocular integration of plaid motion perception

This study assessed the early mechanisms underlying perception of plaid motion. Thus, two superimposed gratings drifting in a rightward direction composed plaid stimuli whose global motion direction was perceived as the vector sum of the two components. The first experiment was aimed at comparing the perception of plaid motion when both components were presented to both eyes (dioptic) or separately to each eye (dichoptic). When components of the patterns had identical spatial frequencies, coherent motion was correctly perceived under dioptic and dichoptic viewing condition. However, the perceived direction deviated from the predicted direction when spatial frequency differences were introduced between components in both conditions. The results suggest that motion integration follows similar rules for dioptic and dichoptic plaids even though performance under dichoptic viewing did not reach dioptic levels. In the second experiment, the role of early cortical areas in the processing of both plaids was examined. As convergence of monocular inputs is needed for dichoptic perception, we tested the hypothesis that primary visual cortex (V1) is required for dichoptic plaid processing by delivering repetitive transcranial magnetic stimulation to this area. Ten minutes of magnetic stimulation disrupted subsequent dichoptic perception for approximately 15 min, whereas no significant changes were observed for dioptic plaid perception. Taken together, these findings suggest that V1 is not crucial for the processing of dioptic plaids but it is necessary for the binocular integration underlying dichoptic plaid motion perception.     

A NOS1 variant implicated in cognitive performance influences evoked neural responses during a high density EEG study of early visual perception

Background: The nitric oxide synthasase‐1 gene (NOS1) has been implicated in mental disorders including schizophrenia and variation in cognition. The NOS1 variant rs6490121 identified in a genome wide association study of schizophrenia has recently been associated with variation in general intelligence and working memory in both patients and healthy participants. Whether this variant is also associated with variation in early sensory processing remains unclear. Methods: We investigated differences in the P1 visual evoked potential in a high density EEG study of 54 healthy participants. Given both NOS1's association with cognition and recent evidence that cognitive performance and P1 response are correlated, we investigated whether NOS1's effect on P1 response was independent of its effects on cognition using CANTAB's spatial working memory (SWM) task. Results: We found that carriers of the previously identified risk “G” allele showed significantly lower P1 responses than non‐carriers. We also found that while P1 response and SWM performance were correlated, NOS1 continued to explain a significant proportion of variation in P1 response even when its effects on cognition were accounted for. Conclusion: The schizophrenia implicated NOS1 variants rs6490121 influences visual sensory processing as measured by the P1 response, either as part of the gene's pleiotropic effects on multiple aspects of brain function, or because of a primary influence on sensory processing that mediates the effects already seen in higher cognitive processes. Hum Brain Mapp, 2011. © 2011 Wiley‐Liss, Inc.     

Luminance and chromatic visual evoked potentials in type I and type II diabetes: relationships with peripheral neuropathy

Abstract The objective of the study was to investigate the subclinical visual deficit in type I and II diabetes, and its relationship with peripheral neuropathy. Thirty-two healthy volunteers, 20 patients with type I diabetes and 30 patients with type II diabetes were studied in a clinical neurophysiology setting. Luminance (VEPs) and chromatic visual evoked potentials (CVEPs) were recorded, with white-black, grey-black, red-green and blue-yellow sinusoidal gratings. The peak latencies of the VEP positive wave and CVEP negative wave were recorded. Ten patients with type I and 8 with type II diabetes had peripheral neuropathy. VEPs were slower in patients with type II diabetes and CVEPs were slower in patients with type I and type II diabetes than in controls. Blue-yellow CVEPs were slower in type II than in type I diabetes. VEPs and red-green CVEPs were slower in patients with diabetes with neuropathy than in those without. In conclusion, we found that visual system impairment differs in diabetes with and without peripheral neuropathy.     

Automatic detection of violations of statistical regularities in the periphery is affected by the focus of spatial attention: A visual mismatch negativity study

We investigated the effect of spatial attention on an event‐related potential signature of automatic detection of violations of statistical regularities, namely, the visual mismatch negativity (vMMN). To vary the task‐field and the location of vMMN‐related stimulation, in the attentional field the stimuli of a tracking task with a steady and a moving (target) bar were presented. The target stimuli of the task appeared either relatively close or far from a passive (task‐irrelevant) oddball or equiprobable sequence at the lower part of the screen. Stimuli of the oddball sequence were shapes tilted either 45° (standard, p = 0.8) or 135° (deviant, p = 0.2), while the equiprobable sequence consisted of additional three shapes with identical number of lines to the oddball stimuli. Deviant stimuli in close proximity to a continuously attended field elicited larger vMMN than similar stimuli farther away from the stimulus field. In the condition with a smaller distance between the field of the tracking task and the vMMN‐related field, the deviant stimuli and the vMMN was followed by a posterior positivity. According to these results, spatial attention modulates vMMN and is capable of initiating further processing of the deviant stimuli.