Auditory-based navigation: attentional shifts rapidly modulate hippocampal codes

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Project Summary/Abstract The hippocampus, a brain structure implicated in spatial memory and navigation, show changes in the course of aging, mental illnesses, neurological disorders, and neurodegenerative diseases. Hippocampal dysfunctions give rise to diverse clinical symptoms, many of which are tied to impairments in attention and navigation. In healthy subjects, spatial attention and navigation are tightly linked, because mapping the environment requires attention to one’s surroundings. Furthermore, while navigating, humans and other animals switch attention between two complementary coordinate systems: a world-centered reference frame for monitoring absolute position, and an egocentric reference frame for monitoring relative position with respect to obstacles, conspecifics, and targets. Little is known about neural dynamics that underlie the rapid shifts in attention that accompany switches between these reference frames—primarily because reliable indicators of spatial attention are lacking in standard animal models. The proposed research bridges this gap by exploiting the bat, a mammal that actively controls its echolocation signals to attend to objects while navigating—similar to many blind humans who use echoes from self-produced sounds (tongue clicks and cane tapping) to localize objects and navigate indoors and outdoors. Both bats and human blind echolocators attend to objects using their sonar, generating an ‘acoustic flashlight’—which provides a direct metric of their moment-to-moment spatial attention. The proposed experiments will track overt spatial attentional shifts while wirelessly recording hippocampal neurons to study attentional effects on neural activity. The hypothesis to be tested is that overt spatial attention rapidly modulates hippocampal spatial codes, by sharpening spatial representation and by switching hippocampal coding between world-centered and egocentric coordinate frames. To do so, animals will navigate under two conditions: (1) a stationary and predictable environment where animals direct attention to fixed objects, and where attentional demands are relatively low; and (2) an unpredictable environment with moving conspecifics and targets, where attentional demands are high and animals shift attention rapidly to inspect dynamic objects. These predictable and unpredictable conditions will be studied in two different experimental setups: a three-dimensional multimedia test room where animals navigate slowly, and a 200- meter, one-dimensional tunnel where animals travel at high speeds. Because echolocation provides a powerful explicit indicator of overt spatial attention, this research will yield transformative insights into attention-driven hippocampal dynamics during naturalistic behavior. The findings will offer new insights into neurological deficits in spatial navigation and memory, yield technological advances in the design of lightweight, miniaturized assistive medical devices used to monitor patient health, and will shed new light on the neural basis of auditory attention and auditory-based navigation in blind humans.