High-field fMRI reveals brain activation patterns underlying saccade execution in the human superior colliculus

Background The superior colliculus (SC) has been shown to play a crucial role in the initiation and coordination of eye- and head-movements. The knowledge about the function of this structure is mainly based on single-unit recordings in animals with relatively few neuroimaging studies investigating eye-movement related brain activity in humans. Methodology/Principal Findings The present study employed high-field (7 Tesla) functional magnetic resonance imaging (fMRI) to investigate SC responses during endogenously cued saccades in humans. In response to centrally presented instructional cues, subjects either performed saccades away from (centrifugal) or towards (centripetal) the center of straight gaze or maintained fixation at the center position. Compared to central fixation, the execution of saccades elicited hemodynamic activity within a network of cortical and subcortical areas that included the SC, lateral geniculate nucleus (LGN), occipital cortex, striatum, and the pulvinar. Conclusions/Significance Activity in the SC was enhanced contralateral to the direction of the saccade (i.e., greater activity in the right as compared to left SC during leftward saccades and vice versa) during both centrifugal and centripetal saccades, thereby demonstrating that the contralateral predominance for saccade execution that has been shown to exist in animals is also present in the human SC. In addition, centrifugal saccades elicited greater activity in the SC than did centripetal saccades, while also being accompanied by an enhanced deactivation within the prefrontal default-mode network. This pattern of brain activity might reflect the reduced processing effort required to move the eyes toward as compared to away from the center of straight gaze, a position that might serve as a spatial baseline in which the retinotopic and craniotopic reference frames are aligned

Active inference and the anatomy of oculomotion

Given that eye movement control can be framed as an inferential process, how are the requisite forces generated to produce anticipated or desired fixation? Starting from a generative model based on simple Newtonian equations of motion, we derive a variational solution to this problem and illustrate the plausibility of its implementation in the oculomotor brainstem. We show, through simulation, that the Bayesian filtering equations that implement ‘planning as inference’ can generate both saccadic and smooth pursuit eye movements. Crucially, the associated message passing maps well onto the known connectivity and neuroanatomy of the brainstem – and the changes in these messages over time are strikingly similar to single unit recordings of neurons in the corresponding nuclei. Furthermore, we show that simulated lesions to axonal pathways reproduce eye movement patterns of neurological patients with damage to these tracts

High-Field fMRI Reveals Brain Activation Patterns Underlying Saccade Execution in the Human Superior Colliculus

BACKGROUND: The superior colliculus (SC) has been shown to play a crucial role in the initiation and coordination of eye- and head-movements. The knowledge about the function of this structure is mainly based on single-unit recordings in animals with relatively few neuroimaging studies investigating eye-movement related brain activity in humans. METHODOLOGY/PRINCIPAL FINDINGS: The present study employed high-field (7 Tesla) functional magnetic resonance imaging (fMRI) to investigate SC responses during endogenously cued saccades in humans. In response to centrally presented instructional cues, subjects either performed saccades away from (centrifugal) or towards (centripetal) the center of straight gaze or maintained fixation at the center position. Compared to central fixation, the execution of saccades elicited hemodynamic activity within a network of cortical and subcortical areas that included the SC, lateral geniculate nucleus (LGN), occipital cortex, striatum, and the pulvinar. CONCLUSIONS/SIGNIFICANCE: Activity in the SC was enhanced contralateral to the direction of the saccade (i.e., greater activity in the right as compared to left SC during leftward saccades and vice versa) during both centrifugal and centripetal saccades, thereby demonstrating that the contralateral predominance for saccade execution that has been shown to exist in animals is also present in the human SC. In addition, centrifugal saccades elicited greater activity in the SC than did centripetal saccades, while also being accompanied by an enhanced deactivation within the prefrontal default-mode network. This pattern of brain activity might reflect the reduced processing effort required to move the eyes toward as compared to away from the center of straight gaze, a position that might serve as a spatial baseline in which the retinotopic and craniotopic reference frames are aligned

Learning the Optimal Control of Coordinated Eye and Head Movements

Various optimality principles have been proposed to explain the characteristics of coordinated eye and head movements during visual orienting behavior. At the same time, researchers have suggested several neural models to underly the generation of saccades, but these do not include online learning as a mechanism of optimization. Here, we suggest an open-loop neural controller with a local adaptation mechanism that minimizes a proposed cost function. Simulations show that the characteristics of coordinated eye and head movements generated by this model match the experimental data in many aspects, including the relationship between amplitude, duration and peak velocity in head-restrained and the relative contribution of eye and head to the total gaze shift in head-free conditions. Our model is a first step towards bringing together an optimality principle and an incremental local learning mechanism into a unified control scheme for coordinated eye and head movements

Implications of interrupted eye–head gaze shifts for resettable integrator reset.

Abstract The neural circuit responsible for saccadic eye movements is generally thought to resemble a closed loop controller. Several models of the saccadic system assume that the feedback signal of such a controller is an efference copy of "eye displacement", a neural estimate of the distance already travelled by the eyes, provided by the so-called "resettable integrator" (RI). The speed, with which the RI is reset, is thought to be fast or instantaneous by some authors and gradual by others. To examine this issue, psychophysicists have taken advantage of the target-distractor paradigm. Subjects engaged in it, are asked to look to only one of two stimuli (the "target") and not to a distractor presented in the diametrically opposite location and they often generate movement sequences in which a gaze shift towards the "distractor" is followed by a second gaze shift to the "target". The fact that the second movement is not systematically erroneous even when very short time intervals (about 5 ms) separate it from the first movement has been used to question the verisimilitude of gradual RI reset. To explore this matter we used a saccade-generating network that relies on a RI coupled to a head controller and a model of the rotational vestibulo-ocular reflex. An analysis of the activation functions of model units provides disproof by counterexample: "targets" can be accurately acquired even when the RI of the saccadic burst generator is not reset at all after the end of the first, interrupted eye-head gaze shift to the distractor and prior to the second, complete eye-head gaze shift to the "target"

Bayesian models of eye movement selection with retinotopic maps

Abstract Among the various possible criteria guiding eye movement selection, we investigate the role of position uncertainty in the peripheral visual field. In particular, we suggest that, in everyday life situations of object tracking, eye movement selection probably includes a principle of reduction of uncertainty. To evaluate this hypothesis, we confront the movement predictions of computational models with human results from a psychophysical task. This task is a freely moving eye version of the Multiple Object Tracking task, where the eye movements may be used to compensate for low peripheral resolution. We design several Bayesian models of eye movement selection with increasing complexity, whose layered structures are inspired by the neurobiology of the brain areas implied this process. Finally, we compare the relative performances of these models with regard to the prediction of the recorded human movements, and show th

Cerebellar control of eye movements: from cerebellar cortex to cerebellar nuclei

Arguably visual information is the most important source of sensory information for us human beings, allowing us to perceive the world. Almost a quarter of our brain is devoted to visual processing. To achieve a precise projection of objects of interest onto the retinal fovea, the region offering the highest spatial resolution and other advantages for the analysis of visual objects, two major types of eye movements, saccades and smooth pursuit are deployed. Saccades shift the image of an object of interest into the fovea. In case the object should be moving, smooth pursuit eye movements (SPEM) try to keep the image of the object within the confines of the fovea in order to ensure sufficient time for its analysis. It has been known that the oculomotor vermis (OMV) of the cerebellar cortex is dedicated to the control of both saccades and SPEM. However, it has remained unclear if the same oculomotor vermal neurons contribute to controlling these two different types of movements, a scenario that does not look very likely considering their dramatically different kinematics. To address this question, we recorded the activity of OMV Purkinje cells (PCs), the only type of output neuron of cerebellar cortex, in monkeys, and the most suitable animal model for studies of the cerebellar control of eye movements made by humans. During recordings the monkeys were performing saccades and smooth pursuit eye movement (SPEM). Subjecting the recorded saccade and SPEM related PC simple spike responses to a multiple regression analysis, we found that, for saccades, the neural firing pattern is mainly determined by eye position. In contrast, in the case of SPEM, eye velocity plays the most important role in defining the firing pattern. These results indicate that the cerebellar computations for saccades and SPEM are different, even at the level of individual PCs. Both saccades and SPEM can be adaptively changed by the experience of insufficiencies, compromising the precision of saccades or the minimization of object image slip in the case of SPEM. As both forms of adaptation rely on the cerebellar oculomotor vermis (OMV), most probably deploying a shared neuronal machinery, one might expect that the adaptation of one type of eye movement should affect the kinematics of the other. In order to test this expectation, we subjected 2 monkeys to a standard saccadic adaption paradigm with SPEM test trials at the end and, alternatively, the same 2 monkeys plus a 3rd one to a random saccadic adaptation paradigm with interleaved trials of SPEM. In contrast to our expectation we observed at best marginal transfer which, moreover was little consistent across experiments and subjects. The lack of consistent transfer of saccadic adaptation decisively constrains models of the implementation of oculomotor learning in the OMV, suggesting an extensive separation of saccade and SPEM-related synapses on P-cell dendritic trees. The OMV projects ipsilaterally to the caudal fastigial nuclei (cFN) (Yamada & Noda, 1987), which is also called the fastigial oculomotor region. Not surprisingly, in view of the established role of the OMV in the control of saccades and SPEM, also the cFN is known to contribute to both. Microsaccades are small saccades produced during fixation, whose amplitudes are <1 degree. The concept of a microsaccade-saccade continuum is supported by the fact that studies on the underpinnings of microsaccades have shown that those oculomotor structures explored contribute to saccades of all sizes. The OMV is one of these structures for which a microsaccade-macrosaccade continuum has been established. As shown in this second work package, this continuum is maintained at the level of the cFN, the recipient of saccade-related signals from the OMV. Furthermore, we demonstrate that the pre-microsaccadic baseline firing rate of cFN neurons has properties suitable to ensure precise fixation. In summary, our results demonstrate the participation of the cerebellum in the control of saccades and SPEM at the level of cerebellar cortex as well as at the level of the caudal fastigial nucleus. It establishes that, contrary to the still dominating view of a separation of the cerebellar machinery for saccades and SPEM, these two forms of goal-directed eye movements rely on largely overlapping, if not identical circuitry. Irrespective of this overlap, learning based adjustments maintain a stunning degree of independence. This is established by our behavioral work. It suggests that this specificity may be a consequence of delimiting distinct dendritic territories of OMV Purkinje cells for the two types of eye movements. Finally, this work supports the notion of a general micro- macrosaccade continuum by establishing that also cFN neurons care for both, micro- and macrosaccades

The computational neurology of active vision

In this thesis, we appeal to recent developments in theoretical neurobiology – namely, active inference – to understand the active visual system and its disorders. Chapter 1 reviews the neurobiology of active vision. This introduces some of the key conceptual themes around attention and inference that recur through subsequent chapters. Chapter 2 provides a technical overview of active inference, and its interpretation in terms of message passing between populations of neurons. Chapter 3 applies the material in Chapter 2 to provide a computational characterisation of the oculomotor system. This deals with two key challenges in active vision: deciding where to look, and working out how to look there. The homology between this message passing and the brain networks solving these inference problems provide a basis for in silico lesion experiments, and an account of the aberrant neural computations that give rise to clinical oculomotor signs (including internuclear ophthalmoplegia). Chapter 4 picks up on the role of uncertainty resolution in deciding where to look, and examines the role of beliefs about the quality (or precision) of data in perceptual inference. We illustrate how abnormal prior beliefs influence inferences about uncertainty and give rise to neuromodulatory changes and visual hallucinatory phenomena (of the sort associated with synucleinopathies). We then demonstrate how synthetic pharmacological perturbations that alter these neuromodulatory systems give rise to the oculomotor changes associated with drugs acting upon these systems. Chapter 5 develops a model of visual neglect, using an oculomotor version of a line cancellation task. We then test a prediction of this model using magnetoencephalography and dynamic causal modelling. Chapter 6 concludes by situating the work in this thesis in the context of computational neurology. This illustrates how the variational principles used here to characterise the active visual system may be generalised to other sensorimotor systems and their disorders

Modélisation bayésienne et robotique

This document describes my research around Bayesian modeling and robotics. My work started with the modeling of biological processes before evolving towards robotics. In both cases, I was interested in both perception and action. I first proposed a model of human perception of planar surfaces with optic flow which fuses in a single framework two concurrent hypotheses of the literature. I also proposed and compared several models of eye movement selection in a Multiple Object Tracking task. I was able to show that the model with explicit uncertainty was the closest to the subjects eye movements.In robotics, I worked on the state estimation of several robots with classical filtering techniques but also including fusion of multiple sources of information of various nature and characteristics. I also discuss the Iterative Closest Point algorithm for which we proposed a more rigorous method for evaluating the different variants. The last piece of work I present deals with online three-dimensional path planning and execution of a tracked robot with significant climbing capabilities.I conclude this document with perspectives on what I call situated robotics, that is robots not taken in isolation but embedded in a sensorized environment shared with humans.Ce document décrit mes travaux de recherche autour de la modélisation bayésienne et de la robotique. Mon travail a commencé par la modélisation de processus biologiques avant, dans un deuxième temps, d'évoluer vers la robotique. Dans les deux cas, je me suis intéressé à la fois à la perception et à l'action. J'ai donc proposé un modèle de la perception humaine de plans par le flux optique qui réunit deux hypothèses de la littérature dans un cadre unique. J'ai aussi proposé et comparé différents modèle de la sélection de mouvement oculaire dans une tâche de suivi multi-cibles, et montré que le modèle prenant en compte explicitement l'incertitude proposait des mouvements plus proches de ceux des sujets.Du côté robotique, j'ai travaillé sur l'estimation d'état de plusieurs robots avec des techniques classiques de filtrage mais en incluant la fusion de plusieurs sources d'informations de nature et caractéristiques différentes. Je discute aussi de l'algorithme d'Iterative Closest Point pour proposer une méthode plus rigoureuse d'évaluation des différentes variantes. Le dernier travail que je présente concerne la planification en ligne et l'exécution de chemin pour un robot à chenille avec des capacités de franchissement importantes.Je conclus ce document par des perspectives de travail sur ce que j'appelle la robotique située, c'est-à-dire des robots non plus isolés mais plongés dans un environnement équipé de capteurs et partagé avec des humains

The visuo-oculomotor system as a biological model of decision making

Animals, wild or civilized, are permanently in interaction with their environment through a perception-action loop. Their brains are experts in transforming the continuous flow of perceived information into action – continuously deciding the next action and seamlessly executing it. The present work addresses the mechanisms forming the stream from perception to action, which embody the interaction between signals driven by the environment and signals driven by the goals and expectations of the animal. In the case of the visuo-oculomotor system, which we take as a biological model, those signals converge in the intermediate layers of the Superior Colliculus (SCi), which serves as an interface spatially representing the possible eye movements. Interestingly, action execution can start while the selection is not completed, allowing us to infer the signals present in the SCi from the eye movements. In Chapter 2, using a computational model, we addressed the spatial interactions possibly occurring upstream the SCi and discuss their effects on behaviour. In Chapter 3, we inferred the presence of a spatiotopic signal in the SCi and refute current models of the visuo-oculomotor system. In Chapter 4, we introduced a new way to infer activity of the SCi, and we used it to distinguish the effects of goal-driven and expectation-related signals on the SC map. In Chapter 5, modelling separately the superficial and the intermediate layers of the SC based on recent neurophysiological recordings, we explored how neural properties and connectivity affect signal interactions. Finally, we discussed how we could implement the theories developed in this thesis, how our view of the visuo-oculomotor system could be refined, and whether this system could become a general model of decision making