A neural hierarchy for illusions of time: duration adaptation precedes multisensory integration.

Perceived time is inherently malleable. For example, adaptation to relatively long or short sensory events leads to a repulsive aftereffect such that subsequent events appear to be contracted or expanded (duration adaptation). Perceived visual duration can also be distorted via concurrent presentation of discrepant auditory durations (multisensory integration). The neural loci of both distortions remain unknown. In the current study we use a psychophysical approach to establish their relative positioning within the sensory processing hierarchy. We show that audiovisual integration induces marked distortions of perceived visual duration. We proceed to use these distorted durations as visual adapting stimuli yet find subsequent visual duration aftereffects to be consistent with physical rather than perceived visual duration. Conversely, the concurrent presentation of adapted auditory durations with nonadapted visual durations results in multisensory integration patterns consistent with perceived, rather than physical, auditory duration. These results demonstrate that recent sensory history modifies human duration perception prior to the combination of temporal information across sensory modalities and provides support for adaptation mechanisms mediated by duration selective neurons situated in early areas of the visual and auditory nervous system (Aubie, Sayegh, & Faure, 2012; Duysens, Schaafsma, & Orban, 1996; Leary, Edwards, & Rose, 2008).

Duration channels mediate human time perception.

The task of deciding how long sensory events seem to last is one that the human nervous system appears to perform rapidly and, for sub-second intervals, seemingly without conscious effort. That these estimates can be performed within and between multiple sensory and motor domains suggest time perception forms one of the core, fundamental processes of our perception of the world around us. Given this significance, the current paucity in our understanding of how this process operates is surprising. One candidate mechanism for duration perception posits that duration may be mediated via a system of duration-selective 'channels', which are differentially activated depending on the match between afferent duration information and the channels' 'preferred' duration. However, this model awaits experimental validation. In the current study, we use the technique of sensory adaptation, and we present data that are well described by banks of duration channels that are limited in their bandwidth, sensory-specific, and appear to operate at a relatively early stage of visual and auditory sensory processing. Our results suggest that many of the computational principles the nervous system applies to coding visual spatial and auditory spectral information are common to its processing of temporal extent.

Co-operative interactions between first- and second-order mechanisms in the processing of structure from motion.

Structure from motion (SFM) is the ability to perceive three-dimensional structure from stimuli containing only two-dimensional motion signals and this ability seems to be a result of high-level cortical processes. It has long been thought that local motion signals defined by second-order cues only weakly contribute to perception of SFM since performance on purely second-order SFM tasks is poor, relative to first-order stimuli. We hypothesized that the mechanisms responsible for deriving SFM were insensitive to low-level stimulus attributes such as the first- or second-order nature of the dots composing the stimulus, in other words: that they were "cue-invariant", but that large differences in sensitivity to local first- and second-order motions were responsible for previous findings. By manipulating the relative strength of first-order dots in an SFM stimulus that combines first- and second-order dots, we show that the two types of motion can separately support SFM and co-operatively interact to produce vivid three-dimensional percepts. This provides strong support that the mechanisms underlying SFM are cue-invariant.

A double dissociation between striate and extrastriate visual cortex for pattern motion perception revealed using rTMS.

The neural mechanisms underlying the integration and segregation of motion signals are often studied using plaid stimuli. These stimuli consist of two spatially coincident dynamic gratings of differing orientations, which are either perceived to move in two unique directions or are integrated by the visual system to elicit the percept of a checkerboard moving in a single direction. Computations pertaining to the motion of the individual component gratings are thought to take place in striate cortex (V1) whereas motion integration is thought to involve neurons in dorsal stream extrastriate visual areas, particularly V5/MT. By combining a psychophysical task that employed plaid stimuli with 1 Hz offline repetitive transcranial magnetic stimulation (rTMS), we demonstrated a double dissociation between striate and extrastriate visual cortex in terms of their contributions to motion integration. rTMS over striate cortex increased coherent motion percepts whereas rTMS over extrastriate cortex had the opposite effect. These effects were robust directly after the stimulation administration and gradually returned to baseline within 15 minutes. This double dissociation is consistent with previous patient data and the recent hypothesis that both coherent and transparent motion percepts are supported by the visual system simultaneously and compete for perceptual dominance.

Low-level mechanisms may contribute to paradoxical motion percepts.

A recent series of experiments demonstrated a surprising deterioration of visual motion discrimination with increasing stimulus size for stimuli of high contrast. This counterintuitive finding was explained as a result of surround suppression in visual area V5. Equally paradoxical was the finding that older observers showed better performance than younger observers. This second result was explained as an age-related reduction in surround suppression due to changes in GABA-mediated inhibition. Using an opponent motion stimulus, we find an analogous effect and also find that this effect is much reduced in older observers, to the point where they perform better than younger observers. Our long duration stimulus should be beyond the range at which surround-suppressed neurons in V5 are preferentially activated. Having normalized our stimuli relative to contrast threshold, we show that our results can be entirely explained by the relative contrast of the stimulus and speculate that contrast sensitivity may play a role in previously reported results. Our older observers' data similarly can be explained by the relative contrast of the stimulus. The difference between older and younger observers appears to be a result of a weakening of spatial summation at high contrast in younger observers, perhaps caused by earlier saturation of motion mechanisms.

The amblyopic deficit for global motion is spatial scale invariant.

Humans with amblyopia display anomalous performance for global motion discrimination. Attempts have been made to rule out an explanation based solely on the visibility loss in lower visual areas. However, it remains a possibility that the altered scale over which local motion is processed in V1 might lead to reduced efficiency of global motion processing in extra-striate cortex. We use stimuli composed of spatial frequency bandpass elements, equated for visibility, to show that the global motion deficit in amblyopia for both fellow and amblyopic eyes is still present once impairments in low-level processing have been factored out. This residual deficit appears to be spatial scale invariant and the relative deficit between the eyes shows a dependence on stimulus speed. We believe that this rules out an explanation of the amblyopic global motion deficit based solely on local motion input. We suggest instead that, in addition to low-level deficits, motion processing in a broadband, extra-striate, global motion mechanism is impaired in amblyopia.

Plaid perception is only subtly impaired in strabismic amblyopia.

Amblyopes exhibit a global motion anomaly that implicates processing beyond the local motion analysis of V1 possibly involving areas MT and MST in the extra-striate cortex. Here, we sought to further investigate this deficit by measuring the perception of moving plaid stimuli by amblyopic observers, since there is good physiological evidence that the motion of such stimuli is determined by processes beyond V1. The conditions under which the two moving components constituting the plaids were seen to cohere or move transparently over one another were investigated by manipulating their relative spatial frequencies. Percepts were measured using both short presentation durations, where both the percept and the direction of motion were reported, and long presentation durations where the bi-stability of the stimulus was directly measured. In addition, we measured the ability of amblyopic eyes to perceive globally coherent motion in a multiple aperture stimulus. We found a small increased tendency for both amblyopic and fellow-fixing eyes to perceive short duration plaid stimuli as coherent relative to control eyes, but no difference for long duration plaids. In addition, amblyopic eyes saw less coherence in multiple aperture stimuli than fellow-fixing eyes but were not reliably different from control eyes. We therefore conclude that the neural mechanisms underlying plaid perception are only subtly abnormal in amblyopia.

Global motion processing: The effect of spatial scale and eccentricity.

Here we examine how global translational motion sensitivity varies with the spatial frequency of the elements in local motion and on the eccentricity of stimulation. Using DC-balanced, spatially narrowband elements (radial log Gabors) matched in terms of multiples above contrast threshold, we show that global translational motion sensitivity is best at mid high spatial frequencies and worst at low spatial frequencies. Furthermore, we show that the lower global motion sensitivity of the periphery is due to differences in spatial scale/contrast that can be attributed to lower reaches of the visual pathway where the local motion signal is transduced. Thus, the efficiency of the global translational motion computation that occurs in extrastriate cortical areas does not vary across the visual field. This may not be directly applicable to global radial motion because there are known visual field anisotropies.

Biological motion perception is cue-invariant.

Previous work investigating whether biological motion is supported by local second-order motion has been contradictory, with different groups finding either a difference or no difference in performance compared to that obtained with first-order stimuli. Here we show psychophysically, using randomized-polarity and contrast-modulated stimuli, that detection of second-order biological motion walkers is worse for stimuli defined by second-order cues, but this difference is explained by a difference in visibility of the local motion in the stimuli. By mixing first-order and second-order dots within the same stimulus, we show that, when the two types of dot are equally visible, first-order noise dots can mask a second-order walker, and vice-versa. We also show that direction-discrimination of normal, inverted and scrambled walkers follow the same pattern for second-order as that obtained with first-order stimuli. These results are consistent with biological motion being processed by a mechanism that is cue-invariant.

Second-order optic flow deficits in amblyopia.

PURPOSE: Amblyopic observers show deficits for global motion discrimination that cannot be accounted for by their contrast sensitivity impairment. The processing of first- and second-order translational global motion is deficient, as is the processing of first-order optic flow, suggesting that cortical function in extrastriate areas is impaired. The authors sought to determine whether amblyopes show impairment in the processing of optic flow defined by second-order motion, whether these deficits are comparable in the two eyes, and whether these deficits are correlated with first-order deficits. METHODS: Eight amblyopic subjects (three strabismic, three strabismic-anisometropic, one anisometropic, one deprivation; mean age, 29 years) were tested. The authors used random dot kinematograms in which the dots were luminance or contrast modulations of background noise. The global pattern of dot motion within the stimulus area was translational, radial, or rotational. Coherence thresholds for direction discrimination were obtained across a range of dot modulation depths, allowing the separation of contrast and motion deficits. RESULTS: The present study showed that deficits in second-order optic flow processing were equivalent to those for first-order stimuli and that these were unrelated to the extent of the amblyopic contrast sensitivity deficit and were comparable in both eyes. Radial optic flow was more affected than rotational optic flow. CONCLUSIONS: Global motion impairment appeared to have a high-level binocular locus and was independent of the depth of the contrast deficit. Results also support the idea that global motion and optic flow processing are form-cue invariant.

Second-order optic flow processing.

Optic flow-large-field rotational and radial motion-is processed as efficiently as translational motion for first-order (luminance-defined) stimuli. However, it has been suggested recently that the same pattern does not hold for second-order (e.g. contrast-defined) stimuli. We used random dot kinematogram (RDK) stimuli to determine whether global processing of optic flow is as efficient as processing of global translational motion for both first- and second-order stimuli. For first-order stimuli, we found that coherence thresholds for radial and rotational motion were equivalent to thresholds for translational motion, supporting previous findings. For second-order stimuli we found, firstly, that given sufficient contrast, second-order optic flow can be processed as efficiently as first-order optic flow and, secondly, that rotational and translational second-order motion are processed with equal efficiency. This contradicts the suggestion that there is a loss of efficiency between integration of second-order global motion and second-order optic flow. The third interesting finding was that the processing of radial second-order motion appears to suffer from a deficit that is dependent upon both the contrast and spatial extent of the stimulus. Further experiments discounted the possibility that the observed deficit is caused by a centrifugal or centripetal bias, but demonstrated that a longer temporal integration period for radial second-order motion is responsible for the observed difference. For durations of approximately 850ms, all three types of motion are processed with equal efficiency.

Motion-detection thresholds for first- and second-order gratings and plaids.

The two-stage decomposition-recombination model of 2D motion perception has been criticised on the basis that the direction of plaid stimuli can be accurately discriminated at speeds so low that the direction of their Fourier components is not discriminable. The nature of this gap in performance between gratings and plaids was investigated across a range of spatial frequencies and durations for first- and second-order stimuli. Motion-detection thresholds were obtained using a 2AFC, constant stimuli procedure and it was found that although thresholds for detection of plaid motion were often lower than those for gratings, the gap in performance between first-order plaids and gratings was unreliable, varying in magnitude and occasionally direction with the spatial frequency of the stimulus, presentation duration and observer. Curiously, an analogous gap found between purely second-order gratings and second-order plaids was more reliable and stable. It has been suggested that the gap is the result of 'local motion detectors' or broadly tuned V1 cells. The data presented here suggest that second-order mechanisms are responsible for the gap and that first-order information may even disrupt it.

Interaction of first- and second-order signals in the extraction of global-motion and optic-flow.

The intention of this series of experiments was to determine the extent to which the pathways sensitive to first-order and second-order motion are independent of one another at, and above, the level of global motion integration. We used translational, radial and rotational motion stimuli containing luminance-modulated dots, contrast-modulated dots, or a mixture of both. Our results show that the two classes of motion stimuli interact perceptually in a global motion coherence task, and the extent of this interaction is governed by whether the two varieties of local motion signal produce an equivalent response in the pathways that encode each type of motion. This provides strong psychophysical evidence that global motion and optic flow processing are cue-invariant. The fidelity of the first-order motion signal was moderated by either reducing the luminance of the dots or by increasing the displacement of the dots on each positional update. The experiments were carried out with two different types of second-order elements (contrast-modulated dots and flicker-modulated dots) and the results were comparable, suggesting that these findings are generalisable to a variety of second-order stimuli. In addition, the interaction between the two different types of second-order stimuli was investigated and we found that the relative modulation depth was also crucial to whether the two populations interacted. We conclude that the relative output of local motion sensors sensitive to either first-order or second-order motion dictates their weight in subsequent cue-invariant global motion computations.

Impaired spatial and binocular summation for motion direction discrimination in strabismic amblyopia.

Amblyopia is characterised by visual deficits in both spatial vision and motion perception. While the spatial deficits are thought to result from deficient processing at both low and higher level stages of visual processing, the deficits in motion perception appear to result primarily from deficits involving higher level processing. Specifically, it has been argued that the motion deficit in amblyopia occurs when local motion information is pooled spatially and that this process is abnormally susceptible to the presence of noise elements in the stimulus. Here we investigated motion direction discrimination for abruptly presented two-frame Gabor stimuli in a group of five strabismic amblyopes and five control observers. Motion direction discrimination for this stimulus is inherently noisy and relies on the signal/noise processing of motion detectors. We varied viewing condition (monocular vs. binocular), stimulus size (5.3-18.5°) and stimulus contrast (high vs. low) in order to assess the effects of binocular summation, spatial summation and contrast on task performance. No differences were found for the high contrast stimuli; however the low contrast stimuli revealed differences between the control and amblyopic groups and between fellow fixing and amblyopic eyes. Control participants exhibited pronounced binocular summation for this task (on average a factor of 3.7), whereas amblyopes showed no such effect. In addition, the spatial summation that occurred for control eyes and the fellow eye of amblyopes was significantly attenuated for the amblyopic eyes relative to fellow eyes. Our results support the hypothesis that pooling of local motion information from amblyopic eyes is abnormal and highly sensitive to noise.

Ibn al-Haytham and psychophysics.

Persian scholar Ibn al-Haytham ('Alhazen') has rightly been credited with many advances in optics and vision science, but recent spurious claims that he is the 'founder of psychophysics' rest upon unsupported assertions, a conflation of psychophysics with the wider discipline of psychology, and semantic arguments over what it is to 'found' a school of thought.