Prior expectations can be used to improve perceptual judgments about ambiguous stimuli. However, little is known about if and how these improvements are maintained in dynamic environments in which the quality of appropriate priors changes from one stimulus to the next. Using a sound-localization task, we show that changes in stimulus predictability lead to arousal-mediated adjustments in the magnitude of prior-driven biases that optimize perceptual judgments about each stimulus. These adjustments depend on task-dependent changes in the relevance and reliability of prior expectations, which subjects update using both normative and idiosyncratic principles. The resulting variations in biases across task conditions and individuals are reflected in modulations of pupil diameter, such that larger stimulus-evoked pupil responses correspond to smaller biases. These results suggest a critical role for the arousal system in adjusting the strength of perceptual biases with respect to inferred environmental dynamics to optimize perceptual judgements.
Adaptation is a common principle that recurs throughout the nervous system at all stages of processing. This principle manifests in a variety of phenomena, from spike frequency adaptation, to apparent changes in receptive fields with changes in stimulus statistics, to enhanced responses to unexpected stimuli. The ubiquity of adaptation leads naturally to the question: What purpose do these different types of adaptation serve? A diverse set of theories, often highly overlapping, has been proposed to explain the functional role of adaptive phenomena. In this review, we discuss several of these theoretical frameworks, highlighting relationships among them and clarifying distinctions. We summarize observations of the varied manifestations of adaptation, particularly as they relate to these theoretical frameworks, focusing throughout on the visual system and making connections to other sensory systems.
Animals smelling in the real world use a small number of receptors to sense a vast number of natural molecular mixtures, and proceed to learn arbitrary associations between odors and valences. Here, we propose a new interpretation of how the architecture of olfactory circuits is adapted to meet these immense complementary challenges. First, the diffuse binding of receptors to many molecules compresses a vast odor space into a tiny receptor space, while preserving similarity. Next, lateral interactions "densify" and decorrelate the response, enhancing robustness to noise. Finally, disordered projections from the periphery to the central brain reconfigure the densely packed information into a format suitable for flexible learning of associations and valences. We test our theory empirically using data from Drosophila. Our theory suggests that the neural processing of olfactory information differs from the other senses in its fundamental use of disorder.Animals sense and respond to volatile molecules that carry messages from and about the world. Some kinds of olfactory behaviors require sensing of particular molecules such as pheromones. These molecules and the receptors that bind to them have likely co-evolved over long periods of time to ensure precise and specific binding. However, to be useful as a general purpose tool for interaction with a diverse and changing world, the olfactory system should be prepared to sense and process any volatile molecule. There are a very large number of such monomolecular odorants (perhaps billions [1]), far more than the number of receptor types available to bind these odorants. Humans and mice, for instance, have just ∼ 300 and ∼ 1000 functional olfactory receptor types, respectively. Yet, animals may be able to discriminate between orders of magnitude more odors than the number of receptor types (a high estimate is given in [2], but see [3]).At an abstract level, the early stage of the olfactory system faces the immense challenge of embedding a very high-dimensional input space (the space of odor molecules) into a low-dimensional space of sensors (the response space of olfactory receptors). This embedding must preserve similarity between different odors well enough to permit the judgements of sameness and difference that are crucial for behavior. Furthermore, experiments [4] suggest that this odor representation is reorganized in higher brain regions to be enormously flexible, allowing learning of nearly arbitrary associations between valences and different groups of odors. Here, we propose * co-first author † lead author a new theoretical framework (Fig. 1), and provide empirical evidence, suggesting that the olfactory system powerfully exploits physiological and structural disorder at different stages of processing to meet these two complementary challenges: (i) compression of a vast odor space into a tiny receptor space, and (ii) reorganization of the information to allow flexible learning. To perform effectively within its design constraints, a sensory system must exploit st...
Prior expectations can be used to improve perceptual judgments about ambiguous stimuli. However, little is known about if and how these improvements are maintained in dynamic environments in which the quality of appropriate priors changes from one stimulus to the next. Using a novel sound-localization task, we show that changes in stimulus predictability lead to arousal-mediated adjustments in the magnitude of prior-driven biases that optimize perceptual judgments about each stimulus. These adjustments depend on task-dependent changes in the relevance and reliability of prior expectations, which subjects update using both normative and idiosyncratic principles. The resulting variations in biases across task conditions and individuals are reflected in modulations of pupil diameter, such that larger stimulus-evoked pupil responses correspond to smaller biases. These results suggest a critical role for the arousal system in adjusting the strength of perceptual biases with respect to inferred environmental dynamics to optimize perceptual judgements.
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