A thalamo-parietal cortex circuit is critical for place-action coordination

Abstract

The anterior and lateral thalamus (ALT) contains head direction cells that signal the directional orientation of an animal within an environment. ALT has direct and indirect connections with the parietal cortex (PC), an area hypothesized to play a role in coordinating viewer-dependent and viewer-independent spatial reference frames. This coordination between reference frames would allow an individual to translate movements toward a desired location from memory. Thus ALT-PC functional connectivity would be critical for moving toward remembered locations. This hypothesis was tested with a place-action task that requires associating an appropriate action (left or right turn) with a spatial location. There are four arms, each offset by 90 degrees, positioned around a central starting point. A trial begins in the central starting point. After exiting a pseudorandomly selected arm, the rat had to displace the correct object covering one of two (left versus right) feeding stations to receive a reward. For a pair of arms facing opposite directions, the reward was located on the left, and for the other pair, the reward was located on the right. Thus, each reward location had a different combination of allocentric location and egocentric action. Removal of an object was scored as correct or incorrect. Trials in which the rat did not displace any objects were scored as no response trials. After an object was removed, the rat returned to the center starting position and the maze was reset for the next trial. To investigate the role of the ALT-PC network, muscimol inactivation infusions targeted bilateral PC, bilateral ALT, or the ALT-PC network. Muscimol sessions were counterbalanced and compared to saline sessions within the same animal. All inactivations resulted in decreased accuracy. Only bilateral PC inactivations resulted in increased no response trials, increased errors, and longer latency responses on the remaining trials. Thus, the ALT-PC network is critical for linking an action with a spatial location for successful navigation.