Contrast sensitivity for motion detection and direction discrimination in adolescents with autism spectrum disorders and their siblings

The magnocellular (M) pathway hypothesis proposes that impaired visual motion perception observed in individuals with Autism Spectrum Disorders (ASD) might be mediated by atypical functioning of the subcortical M pathway, as this pathway provides the bulk of visual input to cortical motion detectors. To test this hypothesis, we measured luminance and chromatic contrast sensitivity, thought to tap M and Parvocellular (P) pathway processing, respectively. We also tested the hypothesis that motion processing is impaired in ASD using a novel paradigm that measures motion processing while controlling for detectabilty. Specifically, this paradigm compares contrast sensitivity for detection of a moving grating with contrast sensitivity for direction-of-motion discrimination of that same moving grating. Contrast sensitivities from adolescents with ASD were compared to typically-developing adolescents, and also unaffected siblings of individuals with ASD (SIBS). The results revealed significant group differences on P, but not M, pathway processing, with SIBS showing higher chromatic contrast sensitivity than both participants with ASD and TD participants. This atypicality, unique to SIBS, suggests the possible existence of a protective factor in these individuals against developing ASD. The results also revealed impairments in motion perception in both participants with ASD and SIBS, which may be an endophenotype of ASD. This impairment may be driven by impairments in motion detectors and/or by reduced input from neural areas that project to motion detectors, the latter possibility being consistent with the notion of reduced connectivity between neural areas in ASD.     

The contribution of human cortical area V3A to the perception of chromatic motion: a transcranial magnetic stimulation study

Area V3A was identified in five human subjects on both a functional and retinotopic basis using functional magnetic resonance imaging techniques. V3A, along with other visual areas responsive to motion, was then targeted for disruption by repetitive transcranial magnetic stimulation (rTMS) whilst the participants performed a delayed speed matching task. The stimuli used for this task included chromatic, isoluminant motion stimuli that activated either the L?M or S?(L+M) cone‐opponent mechanisms, in addition to moving stimuli that contained only luminance contrast (L+M). The speed matching task was performed for chromatic and luminance stimuli that moved at slow (2°/s) or faster (8°/s) speeds. The application of rTMS to area V3A produced a perceived slowing of all chromatic and luminance stimuli at both slow and fast speeds. Similar deficits were found when rTMS was applied to V5/MT+. No deficits in performance were found when areas V3B and V3d were targeted by rTMS. These results provide evidence of a causal link between neural activity in human area V3A and the perception of chromatic isoluminant motion. They establish area V3A, alongside V5/MT+, as a key area in a cortical network that underpins the analysis of not only luminance but also chromatically‐defined motion.     

Attentional capture by colour and motion in cerebral achromatopsia

Cerebral achromatopsia is a rare condition in which damage to the ventromedial occipital area of the cortex results in the loss of colour experience. Nevertheless, cortically colour-blind patients can still use wavelength variation to perceive form and motion. In a series of six experiments we examined whether colour could also direct exogenous attention in an achromatopsic observer. We employed the colour singleton paradigm, the phi motion effect, and the correspondence process to assess attentional modulation. Although colour singletons failed to capture attention, a motion signal, based solely on chromatic information, was able to direct attention in the patient. We then show that the effect is abolished when the chromatic contours of stimuli are masked with simultaneous luminance contrast. We argue that the motion effect is dependent on chromatic contrast mediated via intact colour-opponent mechanisms. The results are taken as further evidence for the processing of wavelength variation in achromatopsia despite the absence of colour experience.     

Luminance,but not chromatic visual pathways,mediate amplification of conditioned danger signals in human visual cortex

Complex organisms rely on experience to optimize the function of perceptual and motor systems in situations relevant to survival. It is well established that visual cues reliably paired with danger are processed more efficiently than neutral cues, and that such facilitated sensory processing extends to low levels of the visual system. The neurophysiological mechanisms mediating biased sensory processing, however, are not well understood. Here we used grating stimuli specifically designed to engage luminance or chromatic pathways of the human visual system in a differential classical conditioning paradigm. Behavioral ratings and visual electroencephalographic steady‐state potentials were recorded in healthy human participants. Our findings indicate that the visuocortical response to high‐spatial‐frequency isoluminant (red–green) grating stimuli was not modulated by fear conditioning, but low‐contrast, low‐spatial‐frequency reversal of grayscale gratings resulted in pronounced conditioning effects. We conclude that sensory input conducted via the chromatic pathways into retinotopic visual cortex has limited access to the bi‐directional connectivity with brain networks mediating the acquisition and expression of fear, such as the amygdaloid complex. Conversely, luminance information is necessary to establish amplification of learned danger signals in hierarchically early regions of the visual system.     

Dynamics of macaque MT cell responses to grating triplets

Neurons in area MT are sensitive to the direction of motion of gratings and of plaids made by summing 2 gratings moving in different directions. MT component direction-selective (CDS) neurons respond to the individual gratings of a plaid. Pattern direction-selective (PDS) neurons on the other hand, combine component information and respond selectively to the resulting pattern motion. Adding a third grating creates a "triplaid," which contains 3 grating and 3 plaid motions and is perceptually multistable. To examine how direction-selective mechanisms parse the motion signals in triplaids, we recorded MT responses of anesthetized and awake macaques to stimuli in which 3 identical moving gratings whose directions were separated by 120° were introduced in 3 successive epochs, going from grating to plaid to triplaid. CDS and PDS neurons-selected based on their responses to gratings and plaids-had strikingly different tuning properties in the triplaid epoch. CDS neurons were strongly tuned for the direction of motion of individual gratings, but PDS neurons nearly lost their selectivity for either the gratings or the plaids in the stimulus. We explain this reduced motion selectivity with a model that relates pattern selectivity of PDS neurons to a broad pooling of V1 afferents with a near-cosine weighting profile. Because PDS neurons signal both component and pattern motion in gratings and plaids, their reduced selectivity for motion in triplaids may be what makes these stimuli perceptually multistable.     

Spatial attention has different effects on the magno- and parvocellular pathways.

Attention was directed to the left or to the right of the fixation point by the lateral presentation of a target on which the subject had to perform an attention demanding task. A (task-irrelevant) grating displayed in the left visual field was the visual evoked potential (VEP) stimulus. Gratings modulated either in luminance or colour contrast at various temporal frequencies were used in order to maximise the activation of magno- or parvocellular pathways. VEPs recorded in attended and unattended conditions were compared. For luminance stimuli, both latency and amplitude of VEPs were modified by attention. For chromatic stimuli, attention affected the amplitude but not the latency of VEPs. Spatial attention uses different mechanisms when magno- or parvocellular systems are involved.     

Stimulus-contrast-induced biases in activation order reveal interaction between V1/V2 and human MT+

The luminance contrast of a visual stimulus is known to modulate the response properties of areas V1 and the human MT complex (hMT+), but has not been shown to modulate interactions between these two areas. We examined the direction of information transfer between V1/V2 and hMT+ at different stimulus contrasts by measuring magnetoencephalographic (MEG) responses to moving and stationary stimuli presented centrally or peripherally. To determine the direction of information flow, the different response latencies among stimuli and hemispheres in V1/V2 was compared with those of hMT+. At high contrast, responses to stimulus motion and position began in V1/V2, and were followed in hMT+ with a delay between 34 and 55 ms. However, at low contrast, lateralized responses in hMT+ came first, with those in V1/V2 lagging with a delay of 27 ms. Also, at high contrast, stationary stimuli produced greater responses than motion stimuli in V1/V2, while the reverse was true in hMT+, whose response lagged behind the initial response in V1/V2. The same activation order was found using Mutual Information Analysis of the response variances for each condition. Here, the response variances in hMT+ mimicked and trailed those of V1/V2 at high contrast, whereas the reverse was true at low contrast. Such consistent interactions found using two different methodologies strongly supports a processing link between these two areas. The results also suggest that feedback from hMT+ for low-contrast stimuli compensates for unresolved processing in V1/V2 when the input of a visual image is weak.     

Chromatic mechanisms in striate cortex of macaque

We measured the responses of 305 neurons in striate cortex to moving sinusoidal gratings modulated in chromaticity and luminance about a fixed white point. Stimuli were represented in a 3-dimensional color space defined by 2 chromatic axes and a third along which luminance varied. With rare exceptions the chromatic properties of cortical neurons were well described by a linear model in which the response of a cell is proportional to the sum (for complex cells, the rectified sum) of the signals from the 3 classes of cones. For each cell there is a vector passing through the white point along which modulation gives rise to a maximal response. The elevation (theta m) and azimuth (phi m) of this vector fully describe the chromatic properties of the cell. The linear model also describes neurons in l.g.n. (Derrington et al., 1984), so most neurons in striate cortex have the same chromatic selectivity as do neurons in l.g.n. However, the distributions of preferred vectors differed in cortex and l.g.n.: Most cortical neurons preferred modulation along vectors lying close to the achromatic axis and those showing overt chromatic opponency did not fall into the clearly defined chromatic groups seen in l.g.n. The neurons most responsive to chromatic modulation (found mainly in layers IVA, IVC beta, and VI) had poor orientation selectivity, and responded to chromatic modulation of a spatially uniform field at least as well as they did to any grating. We encountered neurons with band-pass spatial selectivity for chromatically modulated stimuli in layers II/III and VI. Most had complex receptive fields. Neurons in layer II/III did not fall into distinct groups according to their chromatic sensitivities, and the chromatic properties of neurons known to lie within regions rich in cytochrome oxidase appeared no different from those of neurons in the interstices. Six neurons, all of which resembled simple cells, showed unusually sharp chromatic selectivity.     

Detailed spatiotemporal brain mapping of chromatic vision combining high‐resolution VEP with fMRI and retinotopy

Neuroimaging studies have identified so far, several color‐sensitive visual areas in the human brain, and the temporal dynamics of these activities have been separately investigated using the visual‐evoked potentials (VEPs). In the present study, we combined electrophysiological and neuroimaging methods to determine a detailed spatiotemporal profile of chromatic VEP and to localize its neural generators. The accuracy of the present co‐registration study was obtained by combining standard fMRI data with retinotopic and motion mapping data at the individual level. We found a sequence of occipito activities more complex than that typically reported for chromatic VEPs, including feed‐forward and reentrant feedback. Results showed that chromatic human perception arises by the combined activity of at the least five parieto‐occipital areas including V1, LOC, V8/VO, and the motion‐sensitive dorsal region MT+. However, the contribution of V1 and V8/VO seems dominant because the re‐entrant activity in these areas was present more than once (twice in V8/VO and thrice in V1). This feedforward and feedback chromatic processing appears delayed compared with the luminance processing. Associating VEPs and neuroimaging measures, we showed for the first time a complex spatiotemporal pattern of activity, confirming that chromatic stimuli produce intricate interactions of many different brain dorsal and ventral areas.     

Dysfunction of early-stage visual processing in schizophrenia.

OBJECTIVE: Schizophrenia is associated with deficits in higher-order processing of visual information. This study evaluated the integrity of early visual processing in order to evaluate the overall pattern of visual dysfunction in schizophrenia. METHOD: Steady-state visual-evoked potential responses were recorded over the occipital cortex in patients with schizophrenia and in age- and sex-matched comparison volunteers. Visual-evoked potentials were obtained for stimuli composed of isolated squares that were modulated sinusoidally in luminance contrast, number of squares, or chromatic contrast in order to emphasize magnocellular or parvocellular visual pathway activity. RESULTS: Responses of patients to magnocellular-biased stimuli were significantly lower than those of comparison volunteers. These lower response levels were observed in conditions using both low luminance contrast and large squares that biased processing toward the magnocellular pathway. In contrast, responses to stimuli that biased processing toward the parvocellular pathway were not significantly different between schizophrenia patients and comparison volunteers. A significant interaction of group and stimulus type was observed in the condition using low luminance contrast. CONCLUSIONS: These findings suggest a dysfunction of lower-level visual pathways, which was more prominent for magnocellular than parvocellular biased stimuli. The magnocellular pathway helps in orienting toward salient stimuli. A magnocellular pathway deficit could contribute to higher-level visual cognitive deficits in schizophrenia.     

Global Motion Stimuli and Form-From-Motion Stimuli: Common Characteristics and Differential Activation Patterns

We used functional Magnetic Resonance Imaging (fMRI) to explore the areas underlying the processing of two similar motion stimuli that evoke different types of processing. The results indicated that while form-from-motion (FFM) stimuli activated both lateral occipital complex (LOC) and MT complex (MT+), only the LOC remained significantly activated when contrasted with a global motion stimulus (GMS) with different coherence levels. Because of the large number of common characteristics shared between the stimuli, this contrast enabled us to isolate the regions implicated in form processing. The GMS on the other hand only activated MT+, reaching maximal intensity for low coherence. Overall, these data illustrate how two similar motion stimuli can elicit the participation of different cortical visual regions.     

Breaking camouflage: responses of neurons in the middle temporal area to stimuli defined by coherent motion

Camouflaged animals remain inconspicuous only insofar as they remain static. This demonstrates that motion is a powerful cue for figure-ground segregation, allowing detection of moving objects even when their luminance and texture characteristics are matched to the background. We investigated the neural processes underlying this phenomenon by testing the responses of neurons in the middle temporal area (MT) to 'camouflaged' bars, which were rendered visible by motion. These responses were compared with those elicited by 'solid' bars, which also differed from background in terms of their mean luminance. Most MT neurons responded strongly to camouflaged bars, and signaled their direction of motion with precision, with direction-tuning curves being only slightly wider than those measured with solid bars. However, the tuning of most MT cells to stimulus length and speed depended on the type of stimulus - in comparison with solid bars, responses to camouflaged bars typically showed more extensive length summation, weak end-inhibition, and stronger attenuation at high speeds. Moreover, the emergence of direction selectivity was delayed in trials involving camouflaged bars, relative to solid bars. Comparison with results obtained in the first (V1) and second (V2) visual areas, using similar stimuli, indicates that neural computations performed in MT result in significantly stronger and more accurate signals about camouflaged objects, particularly in situations in which these are relatively large and slow moving. These computations are likely to represent an important step in enabling cue-invariant perception of moving objects, particularly in biologically relevant situations.     

Response latencies of neurons in visual areas MT and MST of monkeys with striate cortex lesions

Cortical area, MT (middle temporal area) is specialized for the visual analysis of stimulus motion in the brain. It has been suggested [Brain 118 (1995) 1375] that motion signals reach area MT via two dissociable routes, namely a 'direct' route which bypasses primary visual cortex (area, striate cortex (V1)) and is specialized for processing 'fast' motion (defined as faster than 6 degrees/s) with a relatively short latency, and an 'indirect' route via area V1 for processing 'slow' motion (slower than 6 degrees/s) with a relatively long latency. We tested this proposal by measuring the effects of unilateral V1 lesions on the magnitudes and latencies of responses to fast- and slow-motion (depicted by random dot kinematograms (RDK) ) of single neurons in areas MT and medial superior temporal area (MST) of anaesthetized macaque monkeys. In the unlesioned hemisphere contralateral to a V1 lesion, response magnitudes and latencies of MT neurons were similar to those previously reported from MT neurons in normal monkeys, and there was no significant association between slow movement and long response latency (>100 ms), or between fast movement and short latency (< or =100 ms). V1 lesions led to diminished response magnitudes and increased latencies in area MT of the lesioned hemisphere, but did not selectively abolish MT responses to slow moving stimuli, or abolish long-latency responses to either slow- or fast-moving stimuli. Response magnitudes and latencies in area MST, which receives visual inputs directly from area MT and is also specialized for visual analysis of motion, were unaffected by V1 lesions (though we have shown elsewhere that directionally-selective responses in both areas were impaired by V1 lesions). Overall, the results are incompatible with the hypothesis that there are dissociable routes to MT specialized for processing separately fast and slow motion.     

Convergence of parvocellular and magnocellular information channels in the primary visual cortex of the macaque

We investigated whether responses of single cells in the striate cortex of anaesthetized macaque monkeys exhibit signatures of both parvocellular (P) and magnocellular (M) inputs from the dorsal lateral geniculate nucleus (dLGN). We used a palette of 128 isoluminant hues at four different saturation levels to test responses to chromatic stimuli against a white background. Spectral selectivity with these isoluminant stimuli was taken as an indication of P inputs. The presence of magnocellular inputs to a given cortical cell was deduced from its responses to a battery of tests, including assessment of achromatic contrast sensitivity, relative strengths of chromatic and luminance borders in driving the cell at different velocities and conduction velocity of their retino-geniculo-cortical afferents. At least a quarter of the cells in our cortical sample appear to receive convergent P and M inputs. We cannot however, exclude the possibility that some of these cells could be receiving a convergent input from the third parallel channel from the dLGN, namely the koniocellular (K) rather than the P channel. The neurons with convergent P and M inputs were recorded not only from supragranular and infragranular layers but also from the principal geniculate input recipient layer 4. Thus, our results challenge classical ideas of strict parallelism between different information streams at the level of the primate striate cortex.     

Mechanisms of time-based figure-ground segregation

Figure-ground segregation can rely on purely temporal information, that is, on short temporal delays between positional changes of elements in figure and ground (Kandil, F.I. & Fahle, M. (2001) Eur. J. Neurosci., 13, 2004-2008). Here, we investigate the underlying mechanisms by measuring temporal segregation thresholds for various kinds of motion cues. Segregation can rely on monocular first-order motion (based on luminance modulation) and second-order motion cues (contrast modulation) with a high temporal resolution of approximately 20 ms. The mechanism can also use isoluminant motion with a reduced temporal resolution of 60 ms. Figure-ground segregation can be achieved even at presentation frequencies too high for human subjects to inspect successive frames individually. In contrast, when stimuli are presented dichoptically, i.e. separately to both eyes, subjects are unable to perceive any segregation, irrespective of temporal frequency. We propose that segregation in these displays is detected by a mechanism consisting of at least two stages. On the first level, standard motion or flicker detectors signal local positional changes (flips). On the second level, a segregation mechanism combines the local activities of the low-level detectors with high temporal precision. Our findings suggest that the segregation mechanism can rely on monocular detectors but not on binocular mechanisms. Moreover, the results oppose the idea that segregation in these displays is achieved by motion detectors of a higher order (motion-from-motion), but favour mechanisms sensitive to short temporal delays even without activation of higher-order motion detectors.     

Form-from-motion: MEG evidence for time course and processing sequence

The neural mechanisms and role of attention in the processing of visual form defined by luminance or motion cues were studied using magnetoencephalography. Subjects viewed bilateral stimuli composed of moving random dots and were instructed to covertly attend to either left or right hemifield stimuli in order to detect designated target stimuli that required a response. To generate form-from-motion (FFMo) stimuli, a subset of the dots could begin to move coherently to create the appearance of a simple form (e.g., square). In other blocks, to generate form-from-luminance (FFLu) stimuli that served as a control, a gray stimulus was presented superimposed on the randomly moving dots. Neuromagnetic responses were observed to both the FFLu and FFMo stimuli and localized to multiple visual cortical stages of analysis. Early activity in low-level visual cortical areas (striate/early extrastriate) did not differ for FFLu versus FFMo stimuli, nor as a function of spatial attention. Longer latency responses elicited by the FFLu stimuli were localized to the ventral-lateral occipital cortex (LO) and the inferior temporal cortex (IT). The FFMo stimuli also generated activity in the LO and IT, but only after first eliciting activity in the lateral occipital cortical region corresponding to MT/V5, resulting in a 50-60 msec delay in activity. All of these late responses (MT/V5, LO, and IT) were significantly modulated by spatial attention, being greatly attenuated for ignored FFLu and FFMo stimuli. These findings argue that processing of form in IT that is defined by motion requires a serial processing of information, first in the motion analysis pathway from V1 to MT/V5 and thereafter via the form analysis stream in the ventral visual pathway to IT.     

Chromatic edges, surfaces and constancies in cerebral achromatopsia

We tested achromatopsic observer, MS, on a number of tasks to establish the extent to which he can process chromatic contour. Stimuli, specified in terms of cone-contrast, were presented in a three-choice oddity paradigm. First we show that MS is able to discriminate the magnitude of chromatic and luminance contrast, but performance is inferior to that of normal observers. Moreover, MS can discriminate isoluminant borders of different chromatic composition. These abilities are not the result of unintended luminance differences and are abolished when chromatic borders are masked by sharp luminance change. In simple displays, local cone-contrast signals can make a significant contribution to surface colour appearance in normal observers. In more complex displays, the perception of a surface's colour becomes largely independent of the local contrast to its background, via processes presumed to be similar to the edge integration and anchoring stages of Land's Retinex algorithm. We show that in simple displays the percepts of both MS and normal observers are dominated by local chromatic-contrast. But, although the percepts of normal observers change in line with the predictions of retinex theory in more complex displays, those of MS do not, remaining dominated by local contrast signals. We conclude that MS has lost the ability to perform edge integration and that this loss is closely related to his absence of colour experience.     

A simple cell model with dominating opponent inhibition for robust image processing.

The extraction of oriented contrast information by cortical simple cells is a fundamental step in early visual processing. The orientation selectivity originates at least partly from the input of lateral geniculate nuclei neurons with properly aligned receptive fields. In the present article, we investigate the feedforward interactions between on- and off-pathways. Based on physiological evidence we propose a push-pull model with dominating opponent inhibition (DOI). We show that the model can account for empirical data on simple cells, such as contrast-invariant orientation tuning, sharpening of orientation tuning with increasing inhibition, and strong response decrements to stimuli with luminance gradient reversal. With identical parameter settings, we apply the model for the processing of synthetic and real world images. We show that the model with DOI can robustly extract oriented contrast information from noisy input. More important, noise is adaptively suppressed, i.e. the model simple cells do not respond to homogeneous regions of different noise levels, while remaining sensitive to small contrast changes. The image processing results reveal a possible functional role of the strong inhibition as observed empirically, namely to adaptively suppress responses to noisy input.     

Dynamics of directional selectivity in MT receptive field centre and surround

We studied receptive field organization of motion-sensitive neurons in macaque middle temporal cortical area (MT), by mapping direction selectivity in space and in time. Stimuli consisted of pseudorandom sequences of single motion steps presented simultaneously at many different receptive field locations. Spatio-temporal receptive field profiles were constructed by cross-correlating stimuli and spikes. The resulting spike-triggered averages revealed centre-surround organization. The temporal dynamics of the receptive fields were generally biphasic with increased probability for the preferred direction at short latency (50-70 ms) and decreased probability at longer latency (80-100 ms). The response latency of the receptive field surround was on average 16 ms longer than that of the centre. Our results show that surround input and biphasic behaviour reflect two different mechanisms, which make MT cells specifically sensitive to motion contrast in space and time.