Determining the contribution of relative timing of activities across neurons in coding behaviorally distinguishable percepts

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Precise spike timing plays an important role in sensory encoding. Spikes may convey information about the time of events in the external world, as when an animal needs to escape quickly from a predator. Spike timing may carry information about other physical characteristics of an external world; for example, interaural time differences are informative about a location of a sound source. And in general, sensory information can be carried by temporal codes, which means that information is represented in spike trains at time scales that are faster than meaningful fluctuations of the external stimuli. However, these conclusions are based mostly on observed correlations between sensory stimuli and spikes. The question of how the timing of sensory signals relates to behavior remains elusive, mostly because appropriately precise tools have not been available to manipulate the timing of sensory representations. The current project will capitalize on a novel technique of two-photon holographic stimulation, which enables the perturbation of activity in many individual neurons on time scales of ~10 ms, which is relevant for sensory representation and behavioral readout. Application of this technique in three different sensory systems — olfaction, vision, and audition — in combination with novel statistical and theoretical approaches, will address fundamental questions about the role of the temporal structure of neural codes in behavior. Sensory information may be represented by multiple temporal features of the neural code, such as multi- neuronal synchrony, spike timing relative to other spikes, or to global neural dynamics, such as oscillations. However, the presence of the information alone is not enough to prove that these features can be used to evoke behavior. Aim 1 will examine which temporal features of sensory code can be used by animals to guide behavior by measuring which classes of temporal information animals are capable of discriminating. Aim 2 will provide complementary information by measuring the behavioral consequences of perturbing specific temporal aspects of neuronal responses to natural stimuli. Although the use of timing may differ between brain areas, the proposed comparative approach will reveal general principles of sensory coding and establish how neural networks adjust for specific computational demands of sensory information processing.