It is unknown how thalamic head direction neurons extract meaningful information from multiple conflicting sensory information sources when animals run under conditions of sensory mismatch. In the present study, rats were placed on a treadmill on a stage that moved in a figure-8-shaped pathway. The anterodorsal and laterodorsal neurons were recorded under two conditions: (1) control sessions, in which both the stage and the treadmill moved forward, or (2) backward (mismatch) sessions, in which the stage was moved backward while the rats ran forward on the treadmill. Of the 222 thalamic neurons recorded, 55 showed differential responses to the directions to window (south) and door (north) sides, along which the animals were translocated in the long axis of the trajectory. Of these 55 direction-related neurons, 15 showed heading direction-dependent responses regardless of movement direction (forward or backward movements). Thirteen neurons displayed heading and movement direction-dependent responses, and, of these 13, activity of 6 neurons increased during forward movement to the window or door side, while activity of the remaining 7 neurons increased during backward movement to the window or door side. Eighteen neurons showed movement direction-related responses regardless of heading direction. Furthermore, activity of some direction-related neurons increased only in a specific trajectory. These results suggested that the activity of these neurons reflects complex combinations of facing direction (landmarks), movement direction (optic flow/vestibular information), motor/proprioceptive information, and the trajectory of the movement.
The retrosplenial cortex (RSC) has been implicated in wayfinding using different sensory cues. However, the neural mechanisms of how the RSC constructs spatial representations to code an appropriate route under different sensory cues are unknown. In this study, rat RSC neurons were recorded while rats ran on a treadmill affixed to a motion stage that was displaced along a figure-8-shaped track. The activity of some RSC neurons increased during specific directional displacements, while the activity of other neurons correlated with the running speed on the treadmill regardless of the displacement directions. Elimination of visual cues by turning off the room lights and/or locomotor cues by turning off the treadmill decreased the activity of both groups of neurons. The ensemble activity of the former group of neurons discriminated displacements along the common central path of different routes in the track, even when visual or locomotor cues were eliminated where different spatial representations must be created based on different sensory cues. The present results provide neurophysiological evidence of an RSC involvement in wayfinding under different spatial representations with different sensory cues.
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