Basal Ganglia Activity Timing Underlying Habitual Behavior

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Habits are a part of all animal life. Despite their ubiquity, it remains poorly understood how habits are formed and maintained in the brain. This research project will study how habits are represented in brain activity and how changing that activity can change habits. Science generally lacks an understanding of how fluctuating patterns of brain activity control behaviors like habits because, until recently, tools were not available to manipulate those brain patterns. Using cutting-edge techniques to do so, this work tests a central hypothesis that habits are controlled by the timing of brain activity related to when a habit is initiated and executed. Specifically, prior studies have uncovered a burst of brain activity as a behavior starts that correlates with how habitual the behavior is. This research evaluates how this pattern arises in the brain and whether it controls how habitual a behavior is by using tools to both monitor and manipulate the brain at the sub-second time-scale. Results will provide a rich understanding of how habits arise out of precisely timed bursts of brain activity. As part of this project, the cutting-edge research techniques are taught to undergraduate neuroscience students, which is a vital but lacking ingredient in their education. These techniques, and the brain basis of habits in general, also are taught to grade-schools and the public through outreach activities to convey progress science is making on understanding habits. Underrepresented individuals participate in all aspects of the research and outreach.In the brain, the dorsolateral striatum (DLS) and its dopamine input from the substantia nigra have long been implicated in habits. Neural recording studies have uncovered an activity pattern in these areas that characterizes habits, which involves a spiking burst at the start of behavior and diminished spiking mid-behavior. These dynamics suggest that it is the timing of brain activity that helps dictate whether or not a learned behavior occurs habitually. To test this, rats are exposed to lever-pressing and maze-running tasks that provide a screen of behavioral measures for habits. Activity in the DLS is recorded using electrodes as animals form habits and then modify them. Using optogenetics, in which DLS activity can be manipulated using pulses of light, the strength of the DLS activity is manipulated and consequences on habitual behavior and ongoing DLS dynamics assessed. The first and second objectives are to test if the strength of DLS activity at the start of a behavior is sufficient and necessary for that behavior to be expressed as a habit and for habit-related DLS activity to be maintained over time. The third objective is to test if start-related activity of dopamine input to the DLS is also critical for habits and for the start-related DLS activity that represents habits. Collectively, this work answers a long-standing question of how step-to-step fluctuations in DLS activity guide a behavior towards habitual expression and will merge isolated behavioral and neuroscience approaches to do so.