A parsimonious computational model of visual target position encoding in the superior colliculus

International audienceThe superior colliculus (SC) is a brain-stem structure at the crossroad of multiple functional pathways. Several neurophysiological studies suggest that the population of active neurons in the SC encodes the location of a visual target to foveate, pursue or attend to. Although extensive research has been carried out on computational modeling, most of the reported models are often based on complex mechanisms and explain a limited number of experimental results. This suggests that a key aspect may have been overlooked in the design of previous computational models. After a careful study of the literature, we hypothesized that the representation of the whole retinal stimulus (not only its center) might play an important role in the dynamics of SC activity. To test this hypothesis, we designed a model of the SC which is built upon three well accepted principles: the log-polar representation of the visual field onto the SC, the interplay between a center excitation and a surround inhibition and a simple neuronal dynamics, like the one proposed by the dynamic neural field theory. Results show that the retino-topic organization of the collicular activity conveys an implicit computation that deeply impacts the target selection process

Active Neural Field model of goal directed eye-movements

International audienceFor primates (including humans), interacting with objects of interest in the environment often involves their foveation, many of them not being static (e.g. other animals, relative motion due to self-induced movement). Eye movements allow the active and continuous sampling of local information, exploiting the graded precision of visual signals (e.g., due to the types and distributions of photoreceptors). Foveating and tracking targets thus requires adapting to their motion. Indeed, considering the delays involved in the transmission of retinal signals to the eye muscles, a purely reactive schema could not account for the smooth pursuit movements which maintain the target within the central visual field. Internal models have been posited to represent the future position of the target (for instance extrapolating from past observations), in order to compensate for these delays. Yet, adaptation of the sensorimotor and neural activity may be sufficient to synchronize with the movement of the target, converging to encoding its location here-and-now, without explicitly resorting to any frame of reference (Goffart et al., 2017).Committing to a distributed dynamical systems approach, we relied on a computational implementation of neural fields to model an adaptation mechanism sufficient to select, focus and track rapidly moving targets. By coupling the generation of eye-movements with dynamic neural field models and a simple learning rule, we replicated neurophysiological results that demonstrated how the monkey adapts to repeatedly observed moving targets (Bourrelly et al., 2016; Quinton & Goffart, 2018), progressively reducing the number of catch-up saccades and increasing smooth pursuit velocity (yet not going beyond the here-and-now target location). We now focus on eye-movements observed in presence of two simultaneously moving centrifugal targets (Goffart, 2016), for which the reduction to a single trajectory with some predicted dynamics (e.g., target center) is even more inappropriate

Going with the flow? The endogenous/exogenous influences on gaze control in dynamic scenes

This document contains all abstracts of the 16th European Conference on Eye Movements, August 21-25 2011 in Marseille, France. It was a real honour and a great pleasure to welcome more than 500 delegates to Marseille for the 16th edition of the European Conference on Eye Movements. The series of ECEM conferences started in 1981 under the auspices of Rudolf Groner in Bern. This year, we therefore celebrated the 30th Anniversary of ECEM. For this special occasion we had as a special guest Rudolf Groner, and honoured Alan Kennedy and George W. McConkie for their contributions to our field in two special symposia. We had the pleasure of listening to six keynote lectures given respectively by Patrick Cavanagh, Ralf Engbert, Edward L. Keller, Eileen Kowler, Rich Krauzlis and Gordon E. Legge. These exceptional scientific events were nicely complemented by all submissions, which made the ECEM 2011 program a very rich and interdisciplinary endeavor, comprising 19 symposia, 243 talks and 287 poster presentations, and a total of about 550 participants. The conference opened with an address given by Denis Bertin, vice president of the scientific committee of the University of Provence, and representing Jean-Paul Caverni, President of the University of Provence. It closed with Rudolf Groner’s address and the awarding of the best poster contributions by students and postdocs. This year, three posters were awarded; the first prize was offered by SR Research, the second prize was given by the Cognitive Science Society, and the third, the Rudolf Groner Prize, was offered by the ECEM organizing committee. The conference was held on the St Charles campus of the University of Provence, and to mark the return of ECEM in Southern Europe, many events including lunches, coffee breaks, aperitifs and poster sessions took place outside under the trees of our campus. Luckily, the sun was with us for the five days of the conference ! Françoise, Stéphanie, Stéphane, Eric & Lauren

Brain mechanisms for foveating a visual target here-and-now (i.e., where it is and when it is there)

seminar at the Institute of Cognitive Sciences Marc JeannerodIn most goal-directed movements, a spatial congruence is ultimately established between the location of a selected target and the movement endpoint. Using the saccadic orienting response as a model to study the neurobiological basis of this congruence, I will present results of experiments that were performed to understand how and why this sensorimotor association is altered when the medio-posterior cerebellum is functionally impaired, and to test the neural processes that underlie the ability to “intercept” and foveate a target that moves in the peripheral visual field

Critique de la cérébralisation de notions relevant des sciences physiques et mathématiques

International audienceDuring the last decades, confusions were made in the domain of cognitive neuroscience, between the concepts, the measurements (and their numerical transformations) and the physiological processes that generate the measured phenomenon. The limitations of measurements and their associated theoretical notions led some authors to propose nativist and evolutionist options, such as a coding of space, time and number in the brain. For example, in the neurosciences of movement, the activity of neurons would encode kinematic parameters: when they emit action potentials, neurons would "speak" a language imbued with notions of classical mechanics. Yet, the movement of a body segment is the mere ultimate measured product, the outcome of multiple processes taking place in parallel in the brain and converging on the groups of neurons responsible for muscle contractions. In my presentation, I will present a different viewpoint and expose my criticisms about the so-called "neural code for number".Au cours des dernières décennies, des confusions ont été faites dans le domaine des neurosciences cognitives, entre les concepts, les mesures (et leurs transformations numériques) et les processus physiologiques qui engendrent le phénomène mesuré. Les limites des mesures et leurs notions théoriques associées ont conduit certains auteurs à proposer des options nativistes et évolutionnistes, comme celle d'un codage de l'espace, du temps et du nombre dans le cerveau. Par exemple, dans les neurosciences du mouvement, l'activité des neurones coderait des paramètres cinématiques : lorsqu'ils émettent des potentiels d'action, les neurones « parleraient » une langue imprégnée de notions de mécanique classique. Pourtant, le mouvement d'un segment du corps n'est que le produit ultime mesuré, le résultat de multiples processus qui se déploient en parallèle dans le cerveau et qui convergent vers les groupes de neurones responsables des contractions musculaires. Dans ma présentation, je présenterai un point de vue différent et exposerai mes critiques sur le soi-disant "code neuronal pour le nombre"

Critique de la cérébralisation des nombres et des notions de mécanique classique

National audienceSelon certaines études contemporaines, l’activité cérébrale véhiculerait des signaux internes correspondant à des notions cinématiques ou aux nombres d’éléments dans le champ visuel. Dans sa présentation, l’auteur exposera une analyse critique des preuves qu’elles avancen

La cinématique est-elle en-corporée dans le cerveau?

International audienceComment la poursuite et la capture ici et maintenant d’un objet en mouvement sont-elles possibles ? Faut-il croire que le fonctionnement du système nerveux mette en place des cadres généraux, tels l’espace et le temps, et des principes pareils à ceux que la cinématique Newtonienne utilise pour décrire le mouvement d’un corps ? Vers la fin du 19ème siècle, Herbert Spencer défendait que les formes a priori de l’intelligence, comme celle d’espace, étaient un héritage de l’évolution, inscrit dans la neurophysiologie. Pour lui, "les rapports d'espace ont été les mêmes, non-seulement pour tous les hommes, tous les primates et tous les ordres de mammifères dont nous descendons, mais aussi pour tous les ordres d'êtres moins élevés". Ils seraient "exprimés dans des structures nerveuses définies, congénitalement constituées pour agir d'une manière déterminée, et incapables d'agir d'une manière différente". Cette adaptation phylogénétique, complétée d’ajustements ontogénétiques, consisterait alors, par une sorte de mimétisme, en une internalisation des "lois" supposées régir les phénomènes du monde physique. Pour Konrad Lorenz, elle aurait "donné à notre pensée une structure innée qui correspond dans une large mesure à la réalité du monde extérieur", où "nos formes d’intuition et nos catégories s’ajustent à ce qui existe réellement de la même manière que notre pied s’ajuste au sol ou les nageoires du poisson à l’eau". Plus proche de nous, Alain Berthoz défend aussi l’idée d’une "internalisation des lois de la physique newtonienne", que "le cerveau dispose de modèles internes des lois de Newton". Malheureusement, cette doctrine ne précise pas de quelle manière ni sous quelle forme ces “lois” y sont inscrites. Elle ne nous explique pas non plus comment réconcilier la diversité des systèmes nerveux observée dans le monde vivant avec la paucité et la simplicité des lois du mouvement, ou encore, comment la dynamique de l’activité cérébrale, spatialement et temporellement distribuée, flexible et changeante, est assimilable au mouvement d’un corps rigide. Est-il seulement possible de trouver dans l’organisation et le fonctionnement cérébral des éléments qui témoigneraient d’une internalisation des “lois” physiques? Car il se peut bien que cette idée ne soit ni testable ni réfutable. L’adaptation, phylogénétique et ontogénétique, peut simplement résulter du fait que la physiologie des organismes vivants est fonctionnellement plastique, suffisamment labile pour que l’apprentissage et l’exercice répété permettent un ajustement progressif de leur répertoire comportemental aux contraintes environnementales. Car à défaut de cette malléabilité, les animaux concernés auraient plus de difficultés à survivre. Au cours des cinq dernières décennies, des notions cinématiques ont pourtant été utilisées pour expliquer la neurophysiologie sous-jacente à la production des mouvements dirigés vers un objet. La question de leur adéquation à un milieu radicalement différent du monde physique ne fût pas posée. Nous verrons comment, par l’étude des mouvements oculaires d’orientation du regard, poursuivant une cible visuelle en mouvement, la neurophysiologie nous explique que si les globes oculaires se conforment aux lois physiques du mouvement, les processus neuronaux qui produisent leurs mouvements de rotation suivent en fait des principes dictés par les propriétés intrinsèques au cerveau

Are kinematic parameters encoded within the brain activity while a gaze movement is being achieved toward a visual target?

International audienceTwo types of eye movement are made while one tracks a target moving in the visual field. The first type is an abrupt step-like movement (called saccade) that rapidly rotates the eyes toward the target location and brings its image within the central visual field. The second type is a slower movement (called pursuit) whose velocity approximates that of the target. From the retinal excitation to the contraction of extraocular muscle fibers, distinct and parallel visuomotor channels are involved in generating these two movements. Most of the time, the eyes do not rotate as fast as the target; the target image slips on the retina and catch-up saccades punctuate the oculomotor tracking. The performance during which gaze moves continuously and as fast as the target is not spontaneous but requires training. During the last six decades, numerous studies investigated the neuronal processes driving the changes in the orientation of the eyes in response to a moving target. High-resolution recording techniques yielded time series of numerical values from which magnitudes such as eye movement amplitude, duration and velocity were calculated. Some models proposed the existence in the brain of processes that would reduce the difference between internal signals encoding gaze and target directions (for guiding the saccade) and the difference between signals encoding the eye rotation speed and the target speed (for accelerating the slow pursuit component). Lastly, during the pursuit maintenance, a process would sustain the eye velocity while the target image is more or less stabilized in the central visual field. This cybernetic formalism guided electrophysiologists who studied the correlations between the activity of neurons and various kinematic parameters of the eyes and target (position, distance, amplitude, velocity and even acceleration). A one-to-one correspondence was often assumed between notions belonging to the physical world and the inner functioning of the brain.However, contrary to the receptacle (space) within which the object is moving, the brain medium is not empty, neutral, homogeneous, isotropic or uniform. The neurophysiology unravels clusters of various kinds of cells between which multiple channels transmit the retinal signals with unequal conduction speeds. Before converging onto the motor nerves and exciting the appropriate muscle fibers, the visuomotor transmission consists of flows of activity that are distributed across several neuronal regions. Within these neuronal networks, the neural image of a small target spot does not look compact and rigid but dynamic and expanded, spatially and temporally. Yet, despite this tremendous complexity, animals exhibit the ability to capture an object, at the location where it is and at the time when it is there. During my communication, I shall report examples illustrating attempts to “cerebralize” kinematic parameters and explain their limitations. Instead of embedding within the cerebral medium, notions that are classically used to describe the motion of a rigid body in the external world, an alternative option remains possible. A saccade can be viewed as the outcome of a process that restores an equilibrium between visuomotor channels exerting mutually opposing tendencies whereas the slow eye movement as a sustained imbalance

Neurophysiologie de l'orientation visuelle du regard : Approches expérimentale, historique et épistémologique

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Review of "Neural encoding of instantaneous kinematics of eye-head gaze shifts in monkey superior Colliculus" by Dr John van Opstal

Extending the conclusions of Smalianchuk et al. (2018) to gaze shifts made with the unrestrained head, the author concludes that the “SC population activity encodes the instantaneous kinematics of the desired gaze shift through its firing rates” based on a “tight correlation” between the velocity profile and the spike density profile of individual neurons (L728-729, L734, L746-748, L752). He contends that “the finding that single-trial and single-unit firing dynamics at a central neural stage correlate well with the instantaneous motor output of a highly complex and nonlinear synergistic system (comprising the multiple-degrees of freedom oculomotor, head-motor, and vestibular systems; see Fig. 1B) is quite remarkable” (L769-771).In spite of careful readings of his manuscripts, this reviewer remains unconvinced. In each of her/his reviews, she/he exposed several concerns that prevented her/him from admitting the author’s conclusion. The author and this reviewer agree on several points. However, regarding the correlation between the spike density and the saccade velocity, this reviewer suspects that it is actually an artefact for the following reasons.1) From looking at the figures (Fig. 3C: activity of neuron Sa1007, Fig. 4B, Fig. 10B and Fig. S1: activity of neuron Sa3006, Fig. S15: activity of neuron Sa0107), the reader is led to the impression that all saccade-related neurons in the SC cease emitting action potentials shortly before the gaze shift ends. However, this inference may result from the author’s choice of example neurons. Indeed, all saccade-related neurons in the SC do not exhibit an abrupt cessation of activity shortly before saccade end. In the head-unrestrained monkey, Choi and Guitton (2009) documented several neurons that continue to fire after the end of the gaze shift (see the middle row of their Figure 6C). In the head-restrained monkey, numerous studies documented neural discharges that persist after saccade end (Anderson et al. (1998); Goossens and van Opstal (2000); Keller et al. (2000), Munoz and Wurtz (1995), Munoz et al. (1996); Rodgers et al. (2006); Sparks and Mays (1980); Waitzman et al. (1991)). The author did not document how many neurons exhibited this persistent activity after gaze saccade end. It is also unclear whether his analysis was only restricted to the so-called “clipped” saccade-related cells.2) If the time course of the instantaneous spike density and the time course of “gaze-track” velocity look remarkably similar for the neuron (Sa0107) illustrated in Fig. 10 A-B, it is also because the spikes that preceded the saccade-related burst were removed. The graph at the bottom of Fig. 10A shows that twenty milliseconds before gaze onset, the firing rate rises from 0 to 200 spikes per second. However, examination of Fig. 4A (same neuron) reveals that such an enhancement (from zero to 200 spikes/s) is rare. It seems that the author removed the spikes that were emitted before the onset of an analysis interval (elapsed from 20 ms before gaze saccade onset to 20 ms before gaze saccade end). However, numerous studies (see references listed above) reported collicular saccade-related neurons that emit spikes sometimes within a long prelude before saccade onset.Thus, by selecting only the spikes emitted from 20 ms before saccade onset to 20 ms before saccade end, the spike density exhibits a rising phase like the acceleration part of the velocity profile, and a decline like the deceleration part of the velocity profile. The correlation between the instantaneous firing rate and the gaze velocity may be the consequence of selecting a portion of the neuron’s activity.The author may wish to explain to the readers that the premotor neurons are sensitive to the spikes that collicular neurons emit during a specific time interval, that this interval starts 20 ms before saccade onset and terminates 20 ms before saccade end. He may wish to add that the onset and the end of this interval is determined by the pause of firing from a specific group of inhibitory neurons located in the nucleus raphe interpositus: the so-called omnipause neurons. If so, then the author should warn the readers that this scenario remains controversial. Indeed, if this hypothesis were true, then experimentally increasing the pause duration should lead to hypermetric saccades. Empirical studies actually show the lesion of these neurons does not lead to dysmetric saccades (Kaneko 1996; Soetedjo et al. 2000). The author may also explain why these results are not convincing.3) Moreover, plotting the number of trials (or responses) as a function of the correlation coefficient between spike density and gaze velocity (Fig. 10) does not teach us anything about the proportion of neurons that were concerned. Fig. 10C shows that for one neuron (Sa0107), the correlation coefficient ranged from 0.8 to 1.0 in approximately 330 trials out of a total number of 664 trials. Fig. 10D shows that for 20 best-recorded cells, the correlation coefficient ranged from 0.8 to 1.0 in approximately 1022 trials out of 3981 trials. Thus, 32% (330/1021) of the correlation coefficients that ranged from 0.8 to 1.0 are only due to neuron Sa0107. How many neurons account for the remaining 691 correlations? Three neurons like Sa0107 would be sufficient to account for the 1021 trials. In other words, the claim of a “tight correlation” between the velocity profile and the spike density profile of individual neurons” (L728-729, L734, L746-748, L752) is a hasty conclusion if it concerns a small percentage of neurons. Three neurons out of 20 best recorded cells or three neurons out of 43 cells correspond to a small percentage of cells (15% and 7 %, respectively).For these reasons and for other reasons exposed in her/his previous reviews (see also reservations expressed by Goffart et al. 2018 about the encoding of velocity by central neurons), this reviewer thinks that the author’s conclusions are not yet sufficiently founded.However, for the sake of pedagogy to the uninformed readers and for the sake also of reminding the tremendous knowledge acquired by previous neurophysiological studies in the awake and trained monkey, this reviewer supports the publication of the author’s work as long as the readers are warned about its limitations and shortcomings