Thesis advisor: Scott D. Slotnick / The overarching aim of this dissertation is to examine the role of human motion processing complex, MT+ during sustained perception and attention. MT+ is comprised of sub-region MT, which processes motion in the contralateral visual field (i.e., left hemisphere MT processes motion in the right visual field and vice versa), and sub-region MST, which processes motion in both the contralateral and ipsilateral visual fields. Whereas previous transcranial magnetic stimulation (TMS) research has provided compelling evidence that region MT+ is necessary for low-level motion processing, Chapter 1 describes an experiment testing whether the sub-region MT is necessary for contralateral low-level motion processing. Chapter 2 describes an experiment that dissociates low-level sensory attentional modulation in MT+ from high-level attentional control processing in the parietal cortex (i.e., during sustained attention). Chapter 3 describes an experiment investigating the role of MT+ during aesthetic processing when viewing visual art. Importantly, this experiment tests whether the aesthetic is tied to not only low-level motion processing in MT+ but also high-level processing in frontal regions. Taken together, the results across the three experiments provide novel evidence for the role of MT+ during low-level motion processing during sustained perception and attention. Moreover, these low-level motion processing effects together with the observed high-level processes in frontal-parietal regions provide neural mechanisms for the cognitive processes of sustained perception and attention. / Thesis (PhD) — Boston College, 2012. / Submitted to: Boston College. Graduate School of Arts and Sciences. / Discipline: Psychology.

Thesis (Ph. D.)--University of California, San Diego, 1997. / Vita. Includes bibliographical references (leaves 103-112).

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Previous research on animate motion perception indicates that animacy detection may be an evolutionarily developed mechanism of the visual system, responsible for adaptive alerting to other organisms in the environment. The present study further examined previously described attention capture by animate motion, and explored whether capture may be modulated by type of animacy (e.g., human motion vs. other animacy). The link between subjective animacy experience and perceptual processing was also examined. Results suggested that attention capture by animacy extends to situations in which animate motion is self-relevant. Animate motion entering the observer’s visual field captured attention relative to motion leaving out of the visual field. Subjective ratings of animacy experience also reliably predict reaction time in perceptual/attention tasks. Implications for theories of social cognition and higher order processing of agency are discussed.

Previous research on animate motion perception indicates that animacy detection may be an evolutionarily developed mechanism of the visual system, responsible for adaptive alerting to other organisms in the environment. The present study further examined previously described attention capture by animate motion, and explored whether capture may be modulated by type of animacy (e.g., human motion vs. other animacy). The link between subjective animacy experience and perceptual processing was also examined. Results suggested that attention capture by animacy extends to situations in which animate motion is self-relevant. Animate motion entering the observer’s visual field captured attention relative to motion leaving out of the visual field. Subjective ratings of animacy experience also reliably predict reaction time in perceptual/attention tasks. Implications for theories of social cognition and higher order processing of agency are discussed.

The visual environment of any animal is a complex amalgamation of sensory information (Lochmann and Deneve, 2011); however, it is adaptive for an animal to only react to salient cues (Zupanc, 2010). For many organisms, the detection of an approaching object, such as an oncoming conspecific or a predator, is particularly important. An approaching object with constant velocity is called looming, and has been widely studied for evoking avoidance behaviours in a number of animal species (Gibson, 1958). The migratory locust, Locusta migratoria, has been used extensively as a model system for visually guided behaviour, due to its robust collision-avoidance behaviours and its tractable nervous system (Schlotterer, 1977). The Lobula Giant Movement Detector (LGMD) and the Descending Contralateral Movement Detector (DCMD) constitute one pathway in the locust visual system that integrates the entire field of view that has been implicated in coordinating these types of behaviours (Santer et al., 2006). Previous studies have found that the LGMD/DCMD pathway responds to many visual stimuli, including complex scenes (Rind and Simmons, 1992), approaching paired objects (Guest and Gray, 2006), objects with compound shapes (Guest and Gray, 2006), and objects that follow compound trajectories (McMillan and Gray, 2012). These findings suggest that this pathway is capable of encoding complex motion such as exists in the locust’s natural environment. In my first objective (Chapter 2), I tested the response of the locust DCMD to increasingly complex motion. Using computer generated disks that followed compound trajectories with different velocities, I demonstrate that the DCMD is capable of encoding the location, trajectory, and velocity of an approaching object through aspects of the response profile over time. The motor systems of invertebrates are often controlled by ensembles of neurons working together (Dubuc et al., 2008; Hedrich et al., 2011; Gonzalez-Bellido et al., 2013). The locust visual system has at least five identified descending neurons, beyond the DCMD, that respond to visual motion (Rowell, 1971; Griss and Rowell, 1986; Gray et al., 2010). Due to the tractability of extracellular recordings of the DCMD, these neurons remain relatively little studied. Furthermore, their responses to stimuli have not been investigated concurrently. With recent advancements in multichannel recordings and spike sorting algorithms, it is now possible to explore the responses of multiple neurons in the locust system together. In my second objective (Chapter 3), I recorded from the connective of the locust using multichannel electrodes while challenging it with a wide array of visual stimuli. Preliminary results of these experiments identified as many as five neuronal units with distinctive firing patterns, some which appear to be novel. Together, these results illustrate that the locust visual system is more complex than previously thought, through both the abilities of a single neuron to encode many aspects of visual motion and the presence of multiple unique, visually-sensitive neurons.

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L'imagerie par résonance magnétique fonctionnelle (IRMf) permet d'examiner l'organisation fonctionnelle du cerveau humain de manière non-invasive et chez les sujets sains. L'implémentation de cette technique chez des primates non-humains représente un progrès important dans les neurosciences des systèmes. D'une part, l'IRMf singe permet la réduction et le raffinement des protocoles invasifs impliquant des primates non humains, en révélant les régions d'intérêts dans lesquelles les approches focales invasives, électrophysiologiques ou anatomiques, devraient être menées. D'un autre côté, les connaissances acquises avec ces approches invasives peuvent être transposées plus aisément à l'homme, une fois que les homologies et différences interspécifiques ont été identifiées au travers de protocoles d'IRMf menées en parallèle chez les primates humains et non- humains. La 1ère partie de cette thèse présente les approches conventionnelles d'étude des fonctions cérébrales. Nous montrons que des études invasives chez l'animal demeurent nécessaires pour comprendre les mécanismes neuronaux qui sous-tendent nos fonctions cognitives, malgré le progrès des techniques d'investigation chez l'homme. Suit une revue sur l'évolution des techniques d'IRMf singe et certaines de ses réalisations majeures comme pont dressé entre les études non-invasives menées chez l'homme et les études invasives réalisées chez l'animal, notamment en ce qui concerne notre compréhension des mécanismes neuronaux permettant la saisie manuelle d'objets sous contrôle visuel. Purement méthodologique, la fin de cette 1ère partie décrit l'animalerie et la plate-forme d'IRM à Toulouse et expose les jalons de l'implémentation de l'IRMf chez le singe macaque vigile. La 2ème partie de la thèse présente les 4 études que nous avons menées en IRMf singe. La 1ère étude modélise la réponse hémodynamique chez le singe, un outil indispensable à l'analyses de données d'IRMf, acquises dans les études suivantes. La 2ème étude traite de l'organisation visuotopique du cortex visuel dorsal des primates, et y décrit un nouvel assemblage d'aires visuotopiques chez 2 animaux, grâce à l'usage de nouvelles techniques de stimulation visuelle et d'analyse de champ récepteurs. Ces résultats apportent un point de vue neuf sur l'organisation fonctionnelle de la voie visuelle dorsale et ouvrent de nombreuses perspectives pour les comparaisons entre espèces. La 3ème étude cartographie le réseau d'aires corticales impliqué dans le traitement du flux optique chez les primates non humains et le compare à celui décrit récemment chez l'homme. Grâce à la réplication d'une étude réalisée chez l'homme, nous avons confirmé chez 3 macaques l'implication de zones précédemment identifiées par des enregistrements électrophysiologiques. Nos résultats révèlent de nouvelles zones corticales impliquées dans le traitement du flux optique, dessinant l'image d'un réseau cortical partageant de nombreuses similitudes, mais ayant également des différences frappantes, avec celui documenté dans le cerveau humain. En résumé, l'ambition de cette thèse est double : (1) fournir des recommandations pour la mise en place de techniques IRMf chez le singe, tirées de notre propre expérience et (2) exposer les résultats d'un ensemble d'études que nous avons menées avec cette approche, traitant de l'organisation visuotopique du cortex visuel dorsal et de son implication dans le traitement du mouvement visuel. En plus d'apporter une perspective nouvelle sur l'organisation fonctionnelle du cortex visuel chez les primates non humains, ces études illustrent la contribution de l'IRMf singe comme pont entre études électrophysiologiques chez les primates non humains et études d'imagerie fonctionnelle chez l'homme. / Functional magnetic resonance imaging (fMRI) allows addressing the functional organization of the human brain with minimal invasiveness and in healthy individuals. The implementation of that technique in non-human primates represents an important achievement in systems neuroscience. On the one hand, monkey fMRI contributes to the reduction and refinement of invasive approaches in non-human primates, by revealing the regions of interest in which focal electrophysiological and/or anatomical investigations should be carried out. On the other hand, the knowledge acquired with such invasive approaches can be more safely transposed to humans, once inter-species homologies and differences have been identified through the use of similar fMRI protocols in human and non-human primates. The first part of this thesis reviews the most common approaches that have been used to study brain functions, either in humans or in non-human primates. It is shown that despite progresses in the human approaches, invasive studies in monkeys remain necessary for understanding the neuronal mechanisms underlying cognitive functions. Then follows a description of the evolution of the monkey fMRI techniques and some of its achievements in bridging the gap between non-invasive human studies and invasive animal studies, notably for deciphering the neural mechanisms supporting visually-guided grasping. The end of this first part is purely methodological. It undertakes the description of the monkey facilities and the MR platform in Toulouse, and details the necessary milestones for conducting fMRI research in macaque monkeys. The second part of the thesis presents the 4 studies we have conducted with monkey fMRI. The first study is a preparatory experiment for characterizing the monkey hemodynamic response function, which is a prerequisite for proper analysis of subsequent monkey fMRI data. The second study addresses the visuotopic organization of the primate dorsal visual cortex with a novel technique of wide-field (80°) phase-encoded visual stimulation, coupled with a state of the art surface-based analysis of population receptive fields. The results obtained in 2 animals uncover a new cluster of visuotopic areas in the posterior parietal cortex of the macaque monkey, bringing a fresh view to the functional organization of this piece of cortex and opening a promising avenue for inter-species comparisons. The third study unveils the cortical network involved in optic flow processing in non-human primates and it compares this network to that recently described in humans. To that end, we replicated in macaque monkeys an experiment previously conducted in human subjects with optic flow stimuli that are either consistent or inconsistent with egomotion. Besides confirming the involvement of areas previously identified through electrophysiological recordings, our results reveal new cortical areas involved in the processing of optic flow, drawing the picture of a network sharing many similarities, but also striking differences, with that documented in the human brain. In summary, the ambition of this thesis is two-fold: (1) providing guidelines for setting-up monkey fMRI techniques, drawn from our own experience and (2) exposing a set of studies we have conducted with this approach, dealing with the visuotopic organization of the dorsal visual cortex and its involvement in the processing of visual motion. Besides bringing a fresh view to the functional organization of the dorsal visual pathway in non-human primates, these studies illustrate how monkey fMRI bridges the gap between electrophysiological studies in non-human primates and functional imaging studies in humans.

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Nous avons expliqué comment le système visuel intègre les informations de mouvement en manipulant la distribution de vitesse locale à l'aide d'une classe bien contrôlée de stimuli de texture aléatoires à large bande appelée Motion Clouds (TM), avec des spectres de fréquence spatio-temporels naturalistes continus. Nos résultats montrent que le gain et la précision des poursuites se détériorent à mesure que la variabilité de la fréquence de stimulation augmente. Dans l'expérience de discrimination de vitesse perceptuelle, nous avons constaté que les MC ayant une largeur de bande légèrement supérieure à la vitesse étaient perçus comme se déplaçant plus rapidement. Cependant, au-delà d'une bande passante critique, la perception d'une vitesse constante a été perdue. Dans une troisième expérience de discrimination, nous avons constaté que pour les contrôleurs multimédias à large bande passante, les participants ne pouvaient plus discriminer la direction du mouvement. Ces résultats suggèrent que lorsqu’on augmente la bande passante de petites à grandes vitesses, l’observateur expérimente différents régimes de perception. Nous avons finalement réalisé une expérience d’échelle de différence de vraisemblance maximale avec nos stimuli MC afin d’étudier ces différents régimes de perception possibles. Nous avons identifié trois régimes dans la plage des valeurs de différence de vitesse testées qui correspondraient à la cohérence de mouvement, à la transparence de mouvement et à l'incohérence complète. / It is still not fully understood how the visual system integrates motion information across different spatial and temporal frequencies, in order to build a coherent percept of the global motion under complex, noisy naturalistic conditions. We addressed this question by manipulating local speed distribution (i.e. speed bandwidth Bv) using a well-controlled class of broadband random-texture stimuli called Motion Clouds (MCs), with continuous naturalistic spatiotemporal frequency spectra (Sanz-Leon et al., 2012,; Simoncini et al., 2012).Our results show that pursuit gain and precision deteriorate as stimulus speed variability increases. In the perceptual speed discrimination experiment, we found that MCs with moderately larger speed bandwidth were perceived as moving faster. However, beyond a critical bandwidth (Bv > 0.5 °/s), the perception of a coherent speed was lost. In a third direction discrimination experiment, we found that for large bandwidth MCs participants could no longer discriminate motion direction. These results suggest that when increasing speed bandwidth from a small to a large range, the observer experiences different perceptual regimes. We finally ran a Maximum Likelihood Difference Scaling (Knoblauch & Maloney, 2008) experiment with our MC stimuli to investigate these different possible perceptual regimes. We identified three regimes across the range of tested values of velocity difference, that would correspond to motion coherency (and speed integration), motion transparency and complete incoherency.