Online Tracking of the Contents of Conscious Perception Using Real-Time fMRI

Perception is an active process that interprets and structures the stimulus input based on assumptions about its possible causes. We use real-time functional magnetic resonance imaging (rtfMRI) to investigate a particularly powerful demonstration of dynamic object integration in which the same physical stimulus intermittently elicits categorically different conscious object percepts. In this study, we simulated an outline object that is moving behind a narrow slit. With such displays, the physically identical stimulus can elicit categorically different percepts that either correspond closely to the physical stimulus (vertically moving line segments) or represent a hypothesis about the underlying cause of the physical stimulus (a horizontally moving object that is partly occluded). In the latter case, the brain must construct an object from the input sequence. Combining rtfMRI with machine learning techniques we show that it is possible to determine online the momentary state of a subject’s conscious percept from time resolved BOLD-activity. In addition, we found that feedback about the currently decoded percept increased the decoding rates compared to prior fMRI recordings of the same stimulus without feedback presentation. The analysis of the trained classifier revealed a brain network that discriminates contents of conscious perception with antagonistic interactions between early sensory areas that represent physical stimulus properties and higher-tier brain areas. During integrated object percepts, brain activity decreases in early sensory areas and increases in higher-tier areas. We conclude that it is possible to use BOLD responses to reliably track the contents of conscious visual perception with a relatively high temporal resolution. We suggest that our approach can also be used to investigate the neural basis of auditory object formation and discuss the results in the context of predictive coding theory

Activity in area V3A predicts positions of moving objects

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All-optical interrogation of neural circuits during behaviour

This thesis explores the fundamental question of how patterns of neural activity encode information and guide behaviour. To address this, one needs three things: a way to record neural activity so that one can correlate neuronal responses with environmental variables; a flexible and specific way to influence neural activity so that one can modulate the variables that may underlie how information is encoded; a robust behavioural paradigm that allows one to assess how modulation of both environmental and neural variables modify behaviour. Techniques combining all three would be transformative for investigating which features of neural activity, and which neurons, most influence behavioural output. Previous electrical and optogenetic microstimulation studies have told us much about the impact of spatially or genetically defined groups of neurons, however they lack the flexibility to probe the contribution of specific, functionally defined subsets. In this thesis I leverage a combination of existing technologies to approach this goal. I combine two-photon calcium imaging with two-photon optogenetics and digital holography to generate an “all-optical” method for simultaneous reading and writing of neural activity in vivo with high spatio-temporal resolution. Calcium imaging allows for cellular resolution recordings from neural populations. Two-photon optogenetics allows for targeted activation of individual cells. Digital holography, using spatial light modulators (SLMs), allows for simultaneous photostimulation of tens to hundreds of neurons in arbitrary spatial locations. Taken together, I demonstrate that this method allows one to map the functional signature of neurons in superficial mouse barrel cortex and to target photostimulation to functionally-defined subsets of cells. I develop a suite of software that allows for quick, intuitive execution of such experiments and I combine this with a behavioural paradigm testing the effect of targeted perturbations on behaviour. In doing so, I demonstrate that animals are able to reliably detect the targeted activation of tens of neurons, with some sensitive to as few as five cortical cells. I demonstrate that such learning can be specific to targeted cells, and that the lower bound of perception shifts with training. The temporal structure of such perturbations had little impact on behaviour, however different groups of neurons drive behaviour to different extents. In order to probe which characteristics underly such variation, I tested whether the sensory response strength or correlation structure of targeted ensembles influenced their behavioural salience. Whilst these final experiments were inconclusive, they demonstrate their feasibility and provide us with some key actionable improvements that could further strengthen the all-optical approach. This thesis therefore represents a significant step forward towards the goal of combining high resolution readout and perturbation of neural activity with behaviour in order to investigate which features of the neural code are behaviourally relevant

Olfactory learning in Drosophila

Animals are able to form associative memories and benefit from past experience. In classical conditioning an animal is trained to associate an initially neutral stimulus by pairing it with a stimulus that triggers an innate response. The neutral stimulus is commonly referred to as conditioned stimulus (CS) and the reinforcing stimulus as unconditioned stimulus (US). The underlying neuronal mechanisms and structures are an intensely investigated topic. The fruit fly Drosophila melanogaster is a prime model animal to investigate the mechanisms of learning. In this thesis we propose fundamental circuit motifs that explain aspects of aversive olfactory learning as it is observed in the fruit fly. Changing parameters of the learning paradigm affects the behavioral outcome in different ways. The relative timing between CS and US affects the hedonic value of the CS. Reversing the order changes the behavioral response from conditioned avoidance to conditioned approach. We propose a timing-dependent biochemical reaction cascade, which can account for this phenomenon. In addition to form odor-specific memories, flies are able to associate a specific odor intensity. In aversive olfactory conditioning they show less avoidance to lower and higher intensities of the same odor. However the layout of the first two olfactory processing layers does not support this kind of learning due to a nested representation of odor intensity. We propose a basic circuit motif that transforms the nested monotonic intensity representation to a non-monotonic representation that supports intensity specific learning. Flies are able to bridge a stimulus free interval between CS and US to form an association. It is unclear so far where the stimulus trace of the CS is represented in the fly's nervous system. We analyze recordings from the first three layers of olfactory processing with an advanced machine learning approach. We argue that third order neurons are likely to harbor the stimulus trace