Adaptive Rewiring of a Sensory Network through Spike-Timing-Dependent Plasticity

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Behavior in all animals, including humans, depends on detecting external sensory stimuli and responding appropriately. There are a variety of mechanisms by which sensory systems maximize the detection of stimuli that are important to the animal. However, the sensory environment is constantly changing. How can animals reliably detect behaviorally relevant sensory stimuli while also retaining the flexibility to adapt to changes in the sensory environment? One possible mechanism is synaptic plasticity in which the strengths of the synaptic connections between neurons are adjusted based on past experience. The central hypothesis of this project is that the intrinsic dynamics of neural networks induce synaptic plasticity that results in increased sensitivity to frequently encountered stimuli. Synaptic plasticity is found throughout the brain, but it is generally challenging to study directly in a living animal. The researchers capitalize on the unique experimental advantages of electric fish, in which it is possible to manipulate precisely and monitor the electrical activity of sensory neurons in an awake, behaving animal. In the context of social communication behavior, the researchers study how plasticity alters responses to sensory input, whether natural patterns of sensory input can induce this plasticity, and how this plasticity impacts the behavioral detection of stimuli. This research has broad implications by elucidating how sensory systems adjust to changing external conditions. In addition, electric fish are excellent tools for public outreach in neuroscience and behavior. As exotic animals, they attract a wide audience. The project includes ongoing outreach and education activities to teach K-12 students in the St. Louis region about hypothesis-driven science and the importance of brain plasticity in sensory perception and behavior.Temporal codes have been implicated in sensory processing, cognition, and motor control. Recent studies reveal several mechanisms by which central sensory pathways decode temporal patterns. However, the sensory environment can change. A fundamental problem in sensory neuroscience is understanding how central circuits can robustly detect behaviorally relevant stimuli while retaining the flexibility to adapt to changes in the sensory environment. Spike-timing-dependent plasticity (STDP), in which synaptic strength is adjusted as a function of the relative timing of pre- and postsynaptic spiking, is found in several brain regions across a wide diversity of species. However, its role in the processing of behaviorally relevant stimuli remains controversial, largely because it is inherently difficult to link changes in synaptic strength at the cellular level to effects on behavior. The central hypothesis of this project is that STDP provides a mechanism for modifying network connectivity to adapt information processing to a changing sensory environment. The researchers address this hypothesis by using an integrative approach that capitalizes on the unique experimental advantages of electric fish, in which temporal patterns of spiking are themselves the behaviorally relevant stimulus. Using a combination of neurophysiology, imaging, and behavior, the researchers are determining how STDP alters responses to sensory input in awake and behaving animals, how natural patterns of sensory input can elicit STDP, and how these changes impact behavioral stimulus detection. The project includes outreach and education efforts that target K-12 students in the St. Louis region to teach them about brain plasticity and how the scientific method can be used to address questions about how brains control behavior. As part of the outreach, researchers lead hands-on activities that include experiments with freely behaving fish, psychophysical experiments on participants, and multimedia demonstrations to illustrate brain plasticity and its role in modifying behavior.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.