Dynamic causal modelling of eye movements during pursuit: Confirming precision-encoding in V1 using MEG

This paper shows that it is possible to estimate the subjective precision (inverse variance) of Bayesian beliefs during oculomotor pursuit. Subjects viewed a sinusoidal target, with or without random fluctuations in its motion. Eye trajectories and magnetoencephalographic (MEG) data were recorded concurrently. The target was periodically occluded, such that its reappearance caused a visual evoked response field (ERF). Dynamic causal modelling (DCM) was used to fit models of eye trajectories and the ERFs. The DCM for pursuit was based on predictive coding and active inference, and predicts subjects' eye movements based on their (subjective) Bayesian beliefs about target (and eye) motion. The precisions of these hierarchical beliefs can be inferred from behavioural (pursuit) data. The DCM for MEG data used an established biophysical model of neuronal activity that includes parameters for the gain of superficial pyramidal cells, which is thought to encode precision at the neuronal level. Previous studies (using DCM of pursuit data) suggest that noisy target motion increases subjective precision at the sensory level: i.e., subjects attend more to the target's sensory attributes. We compared (noisy motion-induced) changes in the synaptic gain based on the modelling of MEG data to changes in subjective precision estimated using the pursuit data. We demonstrate that imprecise target motion increases the gain of superficial pyramidal cells in V1 (across subjects). Furthermore, increases in sensory precision – inferred by our behavioural DCM – correlate with the increase in gain in V1, across subjects. This is a step towards a fully integrated model of brain computations, cortical responses and behaviour that may provide a useful clinical tool in conditions like schizophrenia

Contrast dependency and prior expectations in human speed perception

AbstractThe perceived speed of moving objects has long been known to depend on image contrast. Lowering the contrast of first-order motion stimuli typically decreases perceived speed – the well-known “Thompson effect”. It has been suggested that contrast-dependent biases are the result of optimal inference by the visual system, whereby unreliable sensory information is combined with prior beliefs. The Thompson effect is thought to result from the prior belief that objects move slowly (in Bayesian terminology, a “slow speed prior”). However, there is some evidence that the Thompson effect is attenuated or even reversed at higher speeds. Does the effect of contrast on perceived speed depend on absolute speed and what does this imply for Bayesian models with a slow speed prior? We asked subjects to compare the speeds of simultaneously presented drifting gratings of different contrasts. At low contrasts (3–15%), we found that the Thompson effect was attenuated at high speeds: at 8 and 12deg/s, perceived speed increased less with contrast than at 1 and 4deg/s; however, at higher contrasts (15–95%), the situation was reversed. A semi-parametric Bayesian model was used to extract the subjects’ speed priors and was subsequently improved by combining it with a model of speed tuning. These novel findings regarding the dual, contrast-dependent effect of high speeds help reconcile existing conflicting literature and suggest that physiologically plausible mechanisms of representation of speed in the visual cortex may need to be incorporated into Bayesian models to account for certain subtleties of human speed perception

An experimental and theoretical study of visual motion integration for smooth pursuit : A hierarchical recurrent Bayesian framework

Cette thèse se compose de deux parties, concernant deux études expérimentales sur les mouvements oculaires de poursuite lente d'un stimulus visuel en mouvement (barre inclinée). La première étude aborde l'intégration dynamique de signaux locaux de mouvement visuel provenant de la rétine, tandis que la seconde porte sur l'influence de signaux extra-rétiniens sur l'intégration du mouvement. Un cadre théorique plus général est également proposé, sur la base d'un modèle bayésien récurrent et hiérarchique pour la poursuite lente. Pour la première étude, l'intégration dynamique de mouvement a été analysée en variant le contraste et la vitesse de la barre inclinée. Les résultats montrent que des vitesses plus élevées et des valeurs plus basses de contraste produisent un plus fort biais dans la direction initiale de poursuite et que successivement la dynamique d'intégration de mouvement est plus lente pour les contrastes faibles. Une version en boucle ouverte d'un modèle bayésien est proposée, où un réseau bayésien récurrent est connecté en cascade avec un modèle du système oculomoteur pour générer des réponses de poursuite lente. Les réponses du modèle reproduisent qualitativement les différentes dynamiques observées dans les réponses de poursuite à la barre inclinée en fonction des vitesses et des contrastes différents. La deuxième étude a enquêté sur les interactions dynamiques entre les signaux rétiniens et extra-rétiniens dans l'intégration dynamique de mouvement pour la poursuite lente par le moyen d'une suppression transitoire de la cible à différents moments de la poursuite, et notamment au cours de la phase de boucle ouverte et pendant l'état d'équilibre.This thesis addresses two studies by studying smooth pursuit eye movements for a translating tilted bar stimulus. First, the dynamic integration of local visual motion signals originating from retina and second, the influence of extra-retinal signals on motion integration. It also proposes a more generalized, hierarchical recurrent bayesian framework for smooth pursuit. The first study involved investigating dynamic motion integration for varying contrasts and speeds using a tilted bar stimuli. Results show that higher speeds and lower contrasts result in higher initial direction bias and subsequent dynamics of motion integration is slower for lower contrasts. It proposes an open-loop version of a recurrent bayesian model where a recurrent bayesian network is cascaded with an oculomotor plant to generate smooth pursuit responses. The model responses qualitatively account for the different dynamics observed in smooth pursuit responses to tilted bar stimulus at different speeds and contrasts. The second study investigated the dynamic interactions between retinal and extra-retinal signals in dynamic motion integration for smooth pursuit by transiently blanking the target at different moments during open-loop and steady-state phases of pursuit. The results suggest that weights to retinal and extra-retinal signals are dynamic in nature and extra-retinal signals dominate retinal signals on target reappearance after a blank introduced during open-loop of pursuit when compared to a blank introduced during steady-state of pursuit. The previous version of the model is updated to a closed-loop version and extended to a hierarchical recurrent bayesian model

Express detection of visual objects by primate superior colliculus neurons

Abstract Primate superior colliculus (SC) neurons exhibit visual feature tuning properties and are implicated in a subcortical network hypothesized to mediate fast threat and/or conspecific detection. However, the mechanisms through which SC neurons contribute to peripheral object detection, for supporting rapid orienting responses, remain unclear. Here we explored whether, and how quickly, SC neurons detect real-life object stimuli. We presented experimentally-controlled gray-scale images of seven different object categories, and their corresponding luminance- and spectral-matched image controls, within the extrafoveal response fields of SC neurons. We found that all of our functionally-identified SC neuron types preferentially detected real-life objects even in their very first stimulus-evoked visual bursts. Intriguingly, even visually-responsive motor-related neurons exhibited such robust early object detection. We further identified spatial frequency information in visual images as an important, but not exhaustive, source for the earliest (within 100 ms) but not for the late (after 100 ms) component of object detection by SC neurons. Our results demonstrate rapid and robust detection of extrafoveal visual objects by the SC. Besides supporting recent evidence that even SC saccade-related motor bursts can preferentially represent visual objects, these results reveal a plausible mechanism through which rapid orienting responses to extrafoveal visual objects can be mediated

Stimulus Invariant Attentional Responses In The Human Temporal Cortex

The role of parietal and frontal cortices in the control of visual attention in humans and macaques is well-known. Recent studies in macaques identified a temporal cortical region involved in the control of visual attention independent of the type of visual stimulation. This temporal cortical region is part of a network including the superior colliculus (SC) in the control of visual attention. In humans, a homolog of this attention-related temporal cortical region has not been identified until now. We set out to locate such an attention-related region in the human temporal cortex using visual stimuli that identified the respective region in macaques, i.e., motion (MS) and dynamic white-noise stimuli (WNS). In 6 participants (median age: 29 std: 8.6, 2 female), we acquired functional MRI at 9.4T (voxel size 1.5mm isotropic, TR = 1s, TE=21ms) while the participants performed a covert attention task with MS and WNS. The MS was a circular patch of dots with motion direction 30° above horizontal, while the WNS was a dynamic white-noise patch. Two stimuli were presented symmetrically with 4.5° eccentricity relative to a central fixation and 3.5° above horizontal. The covert attention task had three experimental conditions: Attend Left (AL), Attend Right (AR) and Ignore (IG). In AL, the subjects attend to the stimulus in the left visual field and press a button when the attended stimulus changed direction (MS) or a second-order orientation appeared (WNS). In AR, subjects reported on the stimulus in the right visual field. In IG, the subjects ignored the peripheral stimuli and report dimming of the central fixation spot with a button press. We find a consistent, lateralized activation in MT, MST, FST and PH across motion and non-motion stimuli when contrasting AR vs AL conditions. Posterior-dorsal sub-regions of the TPOJ and medio-dorsal parahippocampal regions also show attentional activation across tasks without lateralization. These findings add to the growing evidence supporting the involvement of sub-regions of the temporal cortex in visual attentional processing. Further analyses will address the interplay between attention-related regions of temporal cortex and subcortical structures

Spatial attention deficits are causally linked to an area in macaque temporal cortex

Spatial neglect is a common clinical syndrome involving disruption of the brain’s attention-related circuitry, including the dorsocaudal temporal cortex. In macaques, the attention deficits associated with neglect can be readily modeled, but the absence of evidence for temporal cortex involvement has suggested a fundamental difference from humans. To map the neurological expression of neglect-like attention deficits in macaques, we measured attention-related fMRI activity across the cerebral cortex during experimental induction of neglect through reversible inactivation of the superior colliculus and frontal eye fields. During inactivation, monkeys exhibited hallmark attentional deficits of neglect in tasks using either motion or non-motion stimuli. The behavioral deficits were accompanied by marked reductions in fMRI attentional modulation that were strongest in a small region on the floor of the superior temporal sulcus; smaller reductions were also found in frontal eye fields and dorsal parietal cortex. Notably, direct inactivation of the mid-superior temporal sulcus (STS) cortical region identified by fMRI caused similar neglect-like spatial attention deficits. These results identify a putative macaque homolog to temporal cortex structures known to play a central role in human neglect

Effects of spatial cues on color-change detection in humans

Studies of covert spatial attention have largely used motion, orientation, and contrast stimuli as these features are fundamental components of vision. The feature dimension of color is also fundamental to visual perception, particularly for catarrhine primates, and yet very little is known about the effects of spatial attention on color perception. Here we present results using novel dynamic color stimuli in both discrimination and color-change detection tasks. We find that our stimuli yield comparable discrimination thresholds to those obtained with static stimuli. Further, we find that an informative spatial cue improves performance and speeds response time in a color-change detection task compared with an uncued condition, similar to what has been demonstrated for motion, orientation, and contrast stimuli. Our results demonstrate the use of dynamic color stimuli for an established psychophysical task and show that color stimuli are well suited to the study of spatial attention

Sensory tuning in neuronal movement commands

Successful interaction with our environment requires constant sampling of new sensory information by our brain. In vision, sampling is achieved by means of orienting eye movements, which entail both receiving visual input as well as generating movement commands. Indeed, oculomotor structures like the midbrain superior colliculus (SC) contribute to both processes. Conventionally, however, SC visuo-motor integration is believed to occur in a sequential manner: “vision” first takes place, and “action” follows. Thus, if the same saccade is made towards two different image features, the SC motor bursts should be completely the same; it should not matter, from a motor perspective, whether the saccade target is a car or a face. Here, by recording from SC neurons while monkeys generated saccades towards peripheral stimuli of varying visual features, we found intriguing evidence to the contrary. SC movement commands exhibit robust sensory tuning that is not explained by systematic changes in saccade properties; for a given saccade, the SC motor burst could be strong or weak simply as a function of the image features at the saccade target location. This sensory tuning of SC neural movement commands can afford higher brain areas with information about the upcoming foveated visual stimulus, which can aid in establishing perceptual stability in the face of saccade-induced retinal image shifts. To explore this possibility, we measured human peri-saccadic perceptual thresholds when saccades were made to different image features. As expected, participants exhibited elevated thresholds around saccades. Critically, however, the thresholds varied significantly with the saccade targets’ image features. These results provide a novel insight on the functional role of SC motor bursts, and they suggest that corollary discharge of SC neural movement commands can extend beyond simple spatial location updating to relaying information about the visual properties of saccade targets