Different memory systems in food-hoarding birds: A response to Pravosudov.

We recently showed that food-hoarding birds use familiarity processes more than recollection processes when remembering the spatial location of their caches (Smulders et al., Animal Cognition 26:1929-1943, 2023). Pravosudov (Learning & Behavior, https://doi.org/ https://doi.org/10.3758/s13420-023-00616-x , 2023) called our findings into question, claiming that our method is unable to distinguish between recollection and familiarity, and that associative learning tasks are a better way to study the memory for cache sites. In this response, we argue that our methods would have been more likely to detect recollection than familiarity, if Pravosudov's assertions were correct. We also point out that associative learning mechanisms may be good for building semantic knowledge, but are incompatible with the needs of cache site memory, which requires the unique encoding of caching events.

Understanding accommodative control in the clinic: Modeling latency and amplitude for uncorrected refractive error, presbyopia and cycloplegia.

Accommodation is the process of adjusting the eye's optical power so as to focus at different distances. Uncorrected refractive error and/or functional presbyopia mean that sharp focus may not be achievable for some distances, so observers experience sustained defocus. Here, we identify a problem with current models of accommodative control: They predict excessive internal responses to stimuli outside accommodative range, leading to unrealistic adaptation effects. Specifically, after prolonged exposure to stimuli outside range, current models predict long latencies in the accommodative response to stimuli within range, as well as unrealistic dynamics and amplitudes of accommodative vergence innervation driven by the accommodative neural controller. These behaviors are not observed empirically. To solve this issue, we propose that the input to blur-driven accommodation is not retinal defocus, but correctable defocus. Predictive models of accommodative control already estimate demand from sensed defocus, using a realistic "virtual plant" to estimate accommodation. Correctable defocus can be obtained by restricting this demand to values physically attainable by the eye. If we further postulate that correctable defocus is computed using an idealized virtual plant that retains a young accommodative range, we can explain why accommodative-convergence responses are observed for stimuli that are too near-but not too far-to focus on. We model cycloplegia as a change in gain, and postulate a form of neural myopia to explain the additional relaxation of accommodation often seen with cycloplegia. This model produces plausible predictions for the accommodative response and accommodative convergence signal in a wide range of clinically relevant situations.

Ocular accommodation and wavelength: The effect of longitudinal chromatic aberration on the stimulus-response curve.

The longitudinal chromatic aberration (LCA) of the eye creates a chromatic blur on the retina that is an important cue for accommodation. Although this mechanism can work optimally in broadband illuminants such as daylight, it is not clear how the system responds to the narrowband illuminants used by many modern displays. Here, we measured pupil and accommodative responses as well as visual acuity under narrowband light-emitting diode (LED) illuminants of different peak wavelengths. Observers were able to accommodate under narrowband light and compensate for the LCA of the eye, with no difference in the variability of the steady-state accommodation response between narrowband and broadband illuminants. Intriguingly, our subjects compensated more fully for LCA at nearer distances. That is, the difference in accommodation to different wavelengths became larger when the object was placed nearer the observer, causing the slope of the accommodation response curve to become shallower for shorter wavelengths and steeper for longer ones. Within the accommodative range of observers, accommodative errors were small and visual acuity normal. When comparing between illuminants, when accommodation was accurate, visual acuity was worst for blue narrowband light. This cannot be due to the sparser spacing for S-cones, as our stimuli had equal luminance and thus activated LM-cones roughly equally. It is likely because ocular LCA changes more rapidly at shorter wavelength and so the finite spectral bandwidth of LEDs corresponds to a greater dioptric range at shorter wavelengths. This effect disappears for larger accommodative errors, due to the increased depth of focus of the eye.

Focusing on mixed narrow band stimuli: Implications for mechanisms of accommodation and displays.

The eye has considerable chromatic aberration, meaning that the accommodative demand varies with wavelength. Given this, how does the eye accommodate to light of differing spectral content? Previous work is not conclusive but, in general, the eye focuses in the center of the visible spectrum for broadband light, and it focuses at a distance appropriate for individual wavelengths for narrowband light. For stimuli containing two colors, there are also mixed reports. This is the second of a series of two papers where we investigate accommodation in relation to chromatic aberration Fernandez-Alonso, Finch, Love, and Read (2024). In this paper, for the first time, we measure how the eye accommodates to images containing two narrowband wavelengths, with varying relative luminance under monocular conditions. We find that the eye tends to accommodate between the two extremes, weighted by the relative luminance. At first sight, this seems reasonable, but we show that image quality would be maximized if the eye instead accommodated on the more luminous wavelength. Next we explore several hypotheses as to what signal the eye might be using to drive accommodation and compare these with the experimental data. We show that the data is best explained if the eye seeks to maximize contrast at low spatial frequencies. We consider the implication of these results for both the mechanism behind accommodation, and for modern displays containing narrowband illuminants.

Hoarding titmice predominantly use Familiarity, and not Recollection, when remembering cache locations.

Scatter-hoarding birds find their caches using spatial memory and have an enlarged hippocampus. Finding a cache site could be achieved using either Recollection (a discrete recalling of previously experienced information) or Familiarity (a feeling of "having encountered something before"). In humans, these two processes can be distinguished using receiver operating characteristic (ROC) curves. ROC curves for olfactory memory in rats have shown the hippocampus is involved in Recollection, but not Familiarity. We test the hypothesis that food-hoarding birds, having a larger hippocampus, primarily use Recollection to find their caches. We validate a novel method of constructing ROC curves in humans and apply this method to cache retrieval by coal tits (Periparus ater). Both humans and birds mainly use Familiarity in finding their caches, with lower contribution of Recollection. This contribution is not significantly different from chance in birds, but a small contribution cannot be ruled out. Memory performance decreases with increasing retention interval in birds. The ecology of food-hoarding Parids makes it plausible that they mainly use Familiarity in the memory for caches. The larger hippocampus could be related to associating cache contents and temporal context with cache locations, rather than Recollection of the spatial information itself.

A computational model of stereoscopic prey capture in praying mantises.

We present a simple model which can account for the stereoscopic sensitivity of praying mantis predatory strikes. The model consists of a single "disparity sensor": a binocular neuron sensitive to stereoscopic disparity and thus to distance from the animal. The model is based closely on the known behavioural and neurophysiological properties of mantis stereopsis. The monocular inputs to the neuron reflect temporal change and are insensitive to contrast sign, making the sensor insensitive to interocular correlation. The monocular receptive fields have a excitatory centre and inhibitory surround, making them tuned to size. The disparity sensor combines inputs from the two eyes linearly, applies a threshold and then an exponent output nonlinearity. The activity of the sensor represents the model mantis's instantaneous probability of striking. We integrate this over the stimulus duration to obtain the expected number of strikes in response to moving targets with different stereoscopic disparity, size and vertical disparity. We optimised the parameters of the model so as to bring its predictions into agreement with our empirical data on mean strike rate as a function of stimulus size and disparity. The model proves capable of reproducing the relatively broad tuning to size and narrow tuning to stereoscopic disparity seen in mantis striking behaviour. Although the model has only a single centre-surround receptive field in each eye, it displays qualitatively the same interaction between size and disparity as we observed in real mantids: the preferred size increases as simulated prey distance increases beyond the preferred distance. We show that this occurs because of a stereoscopic "false match" between the leading edge of the stimulus in one eye and its trailing edge in the other; further work will be required to find whether such false matches occur in real mantises. Importantly, the model also displays realistic responses to stimuli with vertical disparity and to pairs of identical stimuli offering a "ghost match", despite not being fitted to these data. This is the first image-computable model of insect stereopsis, and reproduces key features of both neurophysiology and striking behaviour.

Second-order cues to figure motion enable object detection during prey capture by praying mantises.

Detecting motion is essential for animals to perform a wide variety of functions. In order to do so, animals could exploit motion cues, including both first-order cues-such as luminance correlation over time-and second-order cues, by correlating higher-order visual statistics. Since first-order motion cues are typically sufficient for motion detection, it is unclear why sensitivity to second-order motion has evolved in animals, including insects. Here, we investigate the role of second-order motion in prey capture by praying mantises. We show that prey detection uses second-order motion cues to detect figure motion. We further present a model of prey detection based on second-order motion sensitivity, resulting from a layer of position detectors feeding into a second layer of elementary-motion detectors. Mantis stereopsis, in contrast, does not require figure motion and is explained by a simpler model that uses only the first layer in both eyes. Second-order motion cues thus enable prey motion to be detected, even when perfectly matching the average background luminance and independent of the elementary motion of any parts of the prey. Subsequent to prey detection, processes such as stereopsis could work to determine the distance to the prey. We thus demonstrate how second-order motion mechanisms enable ecologically relevant behavior such as detecting camouflaged targets for other visual functions including stereopsis and target tracking.

Seeing the future: Predictive control in neural models of ocular accommodation.

Ocular accommodation is the process of adjusting the eye's crystalline lens so as to bring the retinal image into sharp focus. The major stimulus to accommodation is therefore retinal defocus, and in essence, the job of accommodative control is to send a signal to the ciliary muscle which will minimize the magnitude of defocus. In this article, we first provide a tutorial introduction to control theory to aid vision scientists without this background. We then present a unified model of accommodative control that explains properties of the accommodative response for a wide range of accommodative stimuli. Following previous work, we conclude that most aspects of accommodation are well explained by dual integral control, with a "fast" or "phasic" integrator enabling response to rapid changes in demand, which hands over control to a "slow" or "tonic" integrator which maintains the response to steady demand. Control is complicated by the sensorimotor latencies within the system, which delay both information about defocus and the accommodation changes made in response, and by the sluggish response of the motor plant. These can be overcome by incorporating a Smith predictor, whereby the system predicts the delayed sensory consequences of its own motor actions. For the first time, we show that critically-damped dual integral control with a Smith predictor accounts for adaptation effects as well as for the gain and phase for sinusoidal oscillations in demand. In addition, we propose a novel proportional-control signal to account for the power spectrum of accommodative microfluctuations during steady fixation, which may be important in hunting for optimal focus, and for the nonlinear resonance observed for low-amplitude, high-frequency input. Complete Matlab/Simulink code implementing the model is provided at https://doi.org/10.25405/data.ncl.14945550.

Reduced surround suppression in monocular motion perception.

Motion discrimination of large stimuli is impaired at high contrast and short durations. This psychophysical result has been linked with the center-surround suppression found in neurons of area MT. Recent physiology results have shown that most frontoparallel MT cells respond more strongly to binocular than to monocular stimulation. Here we measured the surround suppression strength under binocular and monocular viewing. Thirty-nine participants took part in two experiments: (a) where the nonstimulated eye viewed a blank field of the same luminance (n = 8) and (b) where it was occluded with a patch (n = 31). In both experiments, we measured duration thresholds for small (1 deg diameter) and large (7 deg) drifting gratings of 1 cpd with 85% contrast. For each subject, a Motion Suppression Index (MSI) was computed by subtracting the duration thresholds in logarithmic units of the large minus the small stimulus. Results were similar in both experiments. Combining the MSI of both experiments, we found that the strength of suppression for binocular condition (MSIbinocular = 0.249 ± 0.126 log10 (ms)) is 1.79 times higher than under monocular viewing (MSImonocular = 0.139 ± 0.137 log10 (ms)). This increase is too high to be explained by the higher perceived contrast of binocular stimuli and offers a new way of testing whether MT neurons account for surround suppression. Potentially, differences in surround suppression reported in clinical populations may reflect altered binocular processing.

Binocular responsiveness of projection neurons of the praying mantis optic lobe in the frontal visual field.

Praying mantids are the only insects proven to have stereoscopic vision (stereopsis): the ability to perceive depth from the slightly shifted images seen by the two eyes. Recently, the first neurons likely to be involved in mantis stereopsis were described and a speculative neuronal circuit suggested. Here we further investigate classes of neurons in the lobula complex of the praying mantis brain and their tuning to stereoscopically-defined depth. We used sharp electrode recordings with tracer injections to identify visual projection neurons with input in the optic lobe and output in the central brain. In order to measure binocular response fields of the cells the animals watched a vertical bar stimulus in a 3D insect cinema during recordings. We describe the binocular tuning of 19 neurons projecting from the lobula complex and the medulla to central brain areas. The majority of neurons (12/19) were binocular and had receptive fields for both eyes that overlapped in the frontal region. Thus, these neurons could be involved in mantis stereopsis. We also find that neurons preferring different contrast polarity (bright vs dark) tend to be segregated in the mantis lobula complex, reminiscent of the segregation for small targets and widefield motion in mantids and other insects.

ASTEROID stereotest v1.0: lower stereo thresholds using smaller, denser and faster dots.

PURPOSE: In 2019, we described ASTEROID, a new stereotest run on a 3D tablet computer which involves a four-alternative disparity detection task on a dynamic random-dot stereogram. Stereo thresholds measured with ASTEROID were well correlated with, but systematically higher than (by a factor of around 1.5), thresholds measured with previous laboratory stereotests or the Randot Preschool clinical stereotest. We speculated that this might be due to the relatively large, sparse dots used in ASTEROID v0.9. Here, we introduce and test the stereo thresholds and test-repeatability of the new ASTEROID v1.0, which uses precomputed images to allow stereograms made up of much smaller, denser dots. METHODS: Stereo thresholds and test/retest repeatability were tested and compared between the old and new versions of ASTEROID (n = 75) and the Randot Circles (n = 31) stereotest, in healthy young adults. RESULTS: Thresholds on ASTEROID v1.0 are lower (better) than on ASTEROID v0.9 by a factor of 1.4, and do not differ significantly from thresholds on the Randot Circles. Thresholds were roughly log-normally distributed with a mean of 1.54 log10 arcsec (35 arcsec) on ASTEROID v1.0 compared to 1.70 log10 arcsec (50 arcsec) on ASTEROID v0.9. The standard deviation between observers was the same for both versions, 0.32 log10 arcsec, corresponding to a factor of 2 above and below the mean. There was no difference between the versions in their test/retest repeatability, with 95% coefficient of repeatability = 0.46 log10 arcsec (a factor of 2.9 or 1.5 octaves) and a Pearson correlation of 0.8 (comparable to other clinical stereotests). CONCLUSION: The poorer stereo thresholds previously reported with ASTEROID v0.9 appear to have been due to the relatively large, coarse dots and low density used, rather than to some other aspect of the technology. Employing the small dots and high density used in ASTEROID v1.0, thresholds and test/retest repeatability are similar to other clinical stereotests.

Motion-in-depth perception and prey capture in the praying mantis Sphodromantis lineola.

Perceiving motion-in-depth is essential to detecting approaching or receding objects, predators and prey. This can be achieved using several cues, including binocular stereoscopic cues such as changing disparity and interocular velocity differences, and monocular cues such as looming. Although these have been studied in detail in humans, only looming responses have been well characterized in insects and we know nothing about the role of stereoscopic cues and how they might interact with looming cues. We used our 3D insect cinema in a series of experiments to investigate the role of the stereoscopic cues mentioned above, as well as looming, in the perception of motion-in-depth during predatory strikes by the praying mantis Sphodromantis lineola Our results show that motion-in-depth does increase the probability of mantis strikes but only for the classic looming stimulus, an expanding luminance edge. Approach indicated by radial motion of a texture or expansion of a motion-defined edge, or by stereoscopic cues, all failed to elicit increased striking. We conclude that mantises use stereopsis to detect depth but not motion-in-depth, which is detected via looming.

The psychophysics of stereopsis can be explained without invoking independent ON and OFF channels.

Early vision proceeds through distinct ON and OFF channels, which encode luminance increments and decrements respectively. It has been argued that these channels also contribute separately to stereoscopic vision. This is based on the fact that observers perform better on a noisy disparity discrimination task when the stimulus is a random-dot pattern consisting of equal numbers of black and white dots (a "mixed-polarity stimulus," argued to activate both ON and OFF stereo channels), than when it consists of all-white or all-black dots ("same-polarity," argued to activate only one). However, it is not clear how this theory can be reconciled with our current understanding of disparity encoding. Recently, a binocular convolutional neural network was able to replicate the mixed-polarity advantage shown by human observers, even though it was based on linear filters and contained no mechanisms which would respond separately to black or white dots. Here, we show that a subtle feature of the way the stimuli were constructed in all these experiments can explain the results. The interocular correlation between left and right images is actually lower for the same-polarity stimuli than for mixed-polarity stimuli with the same amount of disparity noise applied to the dots. Because our current theories suggest stereopsis is based on a correlation-like computation in primary visual cortex, this postulate can explain why performance was better for the mixed-polarity stimuli. We conclude that there is currently no evidence supporting separate ON and OFF channels in stereopsis.

Neurons in Striate Cortex Signal Disparity in Half-Matched Random-Dot Stereograms.

UNLABELLED: Human stereopsis can operate in dense "cyclopean" images containing no monocular objects. This is believed to depend on the computation of binocular correlation by neurons in primary visual cortex (V1). The observation that humans perceive depth in half-matched random-dot stereograms, although these stimuli have no net correlation, has led to the proposition that human depth perception in these stimuli depends on a distinct "matching" computation possibly performed in extrastriate cortex. However, recording from disparity-selective neurons in V1 of fixating monkeys, we found that they are in fact able to signal disparity in half-matched stimuli. We present a simple model that explains these results. This reinstates the view that disparity-selective neurons in V1 provide the initial substrate for perception in dense cyclopean stimuli, and strongly suggests that separate correlation and matching computations are not necessary to explain existing data on mixed correlation stereograms. SIGNIFICANCE STATEMENT: The initial step in stereoscopic 3D vision is generally thought to be a correlation-based computation that takes place in striate cortex. Recent research has argued that there must be an additional matching computation involved in extracting stereoscopic depth in random-dot stereograms. This is based on the observation that humans can perceive depth in stimuli with a mean binocular correlation of zero (where a correlation-based mechanism should not signal depth). We show that correlation-based cells in striate cortex do in fact signal depth here because they convert fluctuations in the correlation level into a mean change in the firing rate. Our results reinstate the view that these cells provide a sufficient substrate for the perception of stereoscopic depth.

The optomotor response of the praying mantis is driven predominantly by the central visual field.

The optomotor response has been widely used to investigate insect sensitivity to contrast and motion. Several studies have revealed the sensitivity of this response to frequency and contrast, but we know less about the spatial integration underlying this response. Specifically, few studies have investigated how the horizontal angular extent of stimuli influences the optomotor response. We presented mantises with moving gratings of varying horizontal extents at three different contrasts in the central or peripheral regions of their visual fields. We assessed the relative effectivity of different regions to elicit the optomotor response and modelled the dependency of the response on the angular extent subtended by stimuli at these different regions. Our results show that the optomotor response is governed by stimuli in the central visual field and not in the periphery. The model also shows that in the central region, the probability of response increases linearly with increase in horizontal extent up to a saturation point. Furthermore, the dependency of the optomotor response on the angular extent of the stimulus is modulated by contrast. We discuss the implications of our results for different modes of stimulus presentation and for models of the underlying mechanisms of motion detection in the mantis.

Stereopsis in animals: evolution, function and mechanisms.

Stereopsis is the computation of depth information from views acquired simultaneously from different points in space. For many years, stereopsis was thought to be confined to primates and other mammals with front-facing eyes. However, stereopsis has now been demonstrated in many other animals, including lateral-eyed prey mammals, birds, amphibians and invertebrates. The diversity of animals known to have stereo vision allows us to begin to investigate ideas about its evolution and the underlying selective pressures in different animals. It also further prompts the question of whether all animals have evolved essentially the same algorithms to implement stereopsis. If so, this must be the best way to do stereo vision, and should be implemented by engineers in machine stereopsis. Conversely, if animals have evolved a range of stereo algorithms in response to different pressures, that could inspire novel forms of machine stereopsis appropriate for distinct environments, tasks or constraints. As a first step towards addressing these ideas, we here review our current knowledge of stereo vision in animals, with a view towards outlining common principles about the evolution, function and mechanisms of stereo vision across the animal kingdom. We conclude by outlining avenues for future work, including research into possible new mechanisms of stereo vision, with implications for machine vision and the role of stereopsis in the evolution of camouflage.

A Single Mechanism Can Account for Human Perception of Depth in Mixed Correlation Random Dot Stereograms.

In order to extract retinal disparity from a visual scene, the brain must match corresponding points in the left and right retinae. This computationally demanding task is known as the stereo correspondence problem. The initial stage of the solution to the correspondence problem is generally thought to consist of a correlation-based computation. However, recent work by Doi et al suggests that human observers can see depth in a class of stimuli where the mean binocular correlation is 0 (half-matched random dot stereograms). Half-matched random dot stereograms are made up of an equal number of correlated and anticorrelated dots, and the binocular energy model-a well-known model of V1 binocular complex cells-fails to signal disparity here. This has led to the proposition that a second, match-based computation must be extracting disparity in these stimuli. Here we show that a straightforward modification to the binocular energy model-adding a point output nonlinearity-is by itself sufficient to produce cells that are disparity-tuned to half-matched random dot stereograms. We then show that a simple decision model using this single mechanism can reproduce psychometric functions generated by human observers, including reduced performance to large disparities and rapidly updating dot patterns. The model makes predictions about how performance should change with dot size in half-matched stereograms and temporal alternation in correlation, which we test in human observers. We conclude that a single correlation-based computation, based directly on already-known properties of V1 neurons, can account for the literature on mixed correlation random dot stereograms.

Unravelling the illusion of flicker fusion.

For over 150 years, researchers have investigated the anti-predator function of animal patterns. However, this work has mainly focused on when prey remain still, and has only recently started to incorporate motion into the study of defensive coloration. As motion breaks camouflage, a new challenge is to understand how prey avoid predators while moving around their environment, and if a moving prey can ever be camouflaged. We propose that there is a solution to this, in that a 'flicker fusion effect' can change the appearance of the prey in the eyes of their predators to reduce the chances of initial detection. This effect occurs when a high contrast pattern blurs at speed, changing the appearance of the prey, which may help them better match their background. Despite being widely discussed in the literature, the flicker fusion effect is poorly described, there is no clear theoretical framework for testing how it might reduce predation, and the terminology describing it is, at best, rather confusing. Our review addresses these three key issues to enable researchers to formulate precise predictions about when the flicker fusion effect occurs, and to test how it can reduce predation.

Blindness to background: an inbuilt bias for visual objects.

Sixty-eight 2- to 12-year-olds and 30 adults were shown colorful displays on a touchscreen monitor and trained to point to the location of a named color. Participants located targets near-perfectly when presented with four abutting colored patches. When presented with three colored patches on a colored background, toddlers failed to locate targets in the background. Eye tracking demonstrated that the effect was partially mediated by a tendency not to fixate the background. However, the effect was abolished when the targets were named as nouns, whilst the change to nouns had little impact on eye movement patterns. Our results imply a powerful, inbuilt tendency to attend to objects, which may slow the development of color concepts and acquisition of color words. A video abstract of this article can be viewed at: https://youtu.be/TKO1BPeAiOI. [Correction added on 27 January 2017, after first online publication: The video abstract link was added.].

Overestimation of stereo thresholds by the TNO stereotest is not due to global stereopsis.

PURPOSE: It has been repeatedly shown that the TNO stereotest overestimates stereo threshold compared to other clinical stereotests. In the current study, we test whether this overestimation can be attributed to a distinction between 'global' (or 'cyclopean') and 'local' (feature or contour-based) stereopsis. METHODS: We compared stereo thresholds of a global (TNO) and a local clinical stereotest (Randot Circles). In addition, a global and a local psychophysical stereotest were added to the design. One hundred and forty-nine children between 4 and 16 years old were included in the study. RESULTS: Stereo threshold estimates with TNO were a factor of two higher than with any of the other stereotests. No significant differences were found between the other tests. Bland-Altman analyses also indicated low agreement between TNO and the other stereotests, especially for higher stereo threshold estimates. Simulations indicated that the TNO test protocol and test disparities can account for part of this effect. DISCUSSION: The results indicate that the global - local distinction is an unlikely explanation for the overestimated thresholds of TNO. Test protocol and disparities are one contributing factor. Potential additional factors include the nature of the task (TNO requires depth discrimination rather than detection) and the use of anaglyph red/green 3D glasses rather than polarizing filters, which may reduce binocular fusion.