CAREER: Characterizing mechanisms of navigation and memory using direct human brain recording and stimulation

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The goal of this project is to explain how the human brain supports spatial navigation and memory. To examine this issue, we will directly record brain activity from subjects performing spatial navigation and memory tasks. We will measure how the brain supports different aspects of spatial memory by having people perform several different types of navigation paradigms using virtual reality on a laptop computer. Our participants are neurosurgical patients who have electrodes surgically implanted as part of treatment for their epilepsy. These patients volunteer to participate in our experiments, thus providing rare direct human brain data on the neural basis of behavior. We will analyze the patterns of brain activity to understand how spatial and memory information is represented across the brain, including both local neural signals in individual regions as well as interactions between brain structures. Further, in addition to recording brain activity, we will also apply targeted (and safe) patterns of electrical stimulation to brains during certain parts of these tasks, allowing us to test how behavior varies when selected brain regions are stimulated. The findings from our research will help us to understand fundamental types of brain signals that support spatial navigation and to compare how these signals differ across brain structures. This project also has a substantial educational component with the development of educational and outreach programs to advance neuroscience education and research at both the K-12 and University levels. We will deploy new curricula on the neuroscience of navigation and memory at New York City schools. To support this outreach, we will develop novel and engaging augmented reality spatial navigation protocols, enabling the students to study spatial memory in their everyday life.This project aims to characterize the distinct neural mechanisms underlying spatial navigation and memory in the human brain, with emphasis on the medial temporal lobe (MTL). We approach this goal with four key elements: direct brain recordings from neurosurgical patients, custom-designed spatial memory tasks using virtual reality, novel computational methods for analyzing local and distributed neural signals related to spatial behavior, and direct brain stimulation for testing the causality of these signals. The subjects in our study are neurosurgical patients who will perform customized spatial memory tasks that are designed to distinguish neural signals corresponding to spatial and non-spatial memory at different scales. Our data analyses will identify patterns of brain activity underlying specific memory processes in the MTL as well as various brain regions using both single-neuron spiking and network oscillations. All experimental designs are grounded in our preliminary data, in which we show that the nature of neural responses to spatial vs. non-spatial memory tasks varies fundamentally across hemisphere, with the right MTL supporting navigation and left MTL supporting memory. Furthermore, to identify how information propagates across this network, we will characterize the functional role of a new phenomenon we recently identified, cortical traveling waves, in which oscillations propagate across the brain to coordinate inter-region communication. Finally, we will use electrical stimulation to causally validate our findings. By combining data across these methods, we will obtain a comprehensive view of how spatial memories are represented in various brain areas and distinguish the large-scale brain networks where information propagates to support spatial memory and navigation. The results of these experiments have the potential for evaluating the key theoretical question of whether a single electrophysiological process in the medial temporal lobe supports both spatial and episodic memory or, alternatively, whether separate neural processes and sub-regions in the MTL support distinct aspects of multi-scale navigation and memory behaviors. THis approach involving direct human brain recordings and stimulation is qualified to address this question because the data we will acquire overcomes limitations of both animal electrophysiology and noninvasive neuroimaging.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.