The striking spatial correlates of hippocampal place cells and grid cells have provided unique insights into how the brain constructs internal, cognitive representations of the environment and uses these representations to guide behavior. These spatially selective cells are influenced by both self-motion signals and by external sensory landmarks. Self-motion signals provide the basis for a path integration computation, in which the hippocampal system tracks the animal's location by integrating its movement vector (speed and direction) over time to continuously update a position signal on an internal cognitive map. To prevent accumulation of error, it is crucial that this endogenous spatial representation be anchored by stable, external sensory cues, such as individual landmarks and environmental boundaries. Accurate path integration requires that an internal representation of position be updated in precise agreement with the animal's displacement in the world. What if the relation between position calculated by self-motion cues and position defined by landmark cues is altered, e.g. during development (slow time scale) or due to injury (fast time scale)? Does the animal recalibrate the internal gain between representations of its movement and the updating of the representation of its position in the brain? We hypothesize that this gain must be learned by reference to visual feedback. We constructed an augmented reality system that allows precise, closed-loop control of the visual environment as rats move through physical space and provide evidence that the path integration system can indeed be recalibrated. We propose a collaborative research program to investigate plasticity of the path integration gain at multiple neural levels using combined theoretical, engineering, and experimental approaches. We will combine mathematical analysis, biologically inspired attractor network theory, and principles derived from engineering to develop the first models of how the path integration system dynamically recalibrates itself in response to sensory feedback. We will perform recordings from the hippocampus and medial entorhinal cortex to provide data to constrain and test these models. The combined expertise of the Pl and Co Investigators in electrophysiological recordings of the hippocampal system, engineering, and mathematical neuroscience will propel the theory forward to explain the network dynamics and functional implications of this ethologically critical form of neural plasticity.
Many mental health illnesses are characterized by disordered thought processes and an inability to appropriately react to external information about the world. Spatial navigation is a complex behavior that allows detailed investigation of how internal brain dynamics interact with external sensory input. Understanding this brain circuitry will help to understand how such interactions become disrupted in psychiatric illness and provide insight into potential treatments.