A Critical Role for the Anterior Thalamus in Directing Attention to Task-Relevant Stimuli

The prefrontal cortex mediates adaption to changing environmental contingencies. The anterior thalamic nuclei, which are closely interconnected with the prefrontal cortex, are important for rodent spatial memory, but their potential role in executive function has received scant attention. The current study examined whether the anterior thalamic nuclei are involved in attentional processes akin to those of prefrontal regions. Remarkably, the results repeatedly revealed attentional properties opposite to those of the prefrontal cortex. Two separate cohorts of rats with anterior thalamic lesions were tested on an attentional set-shifting paradigm that measures not only the ability of stimuli dimensions that reliably predict reinforcement to gain attention (intradimensional shift), but also their ability to shift attention to another stimulus dimension when contingencies change (extradimensional shift). In stark contrast to the effects of prefrontal damage, anterior thalamic lesions impaired intradimensional shifts but facilitated extradimensional shifts. Anterior thalamic lesion animals were slower to acquire discriminations based on the currently relevant stimulus dimension but acquired discriminations involving previously irrelevant stimulus dimensions more rapidly than controls. Subsequent tests revealed that the critical determinant of whether anterior thalamic lesions facilitate extradimensional shifts is the degree to which the stimulus dimension has been established as an unreliable predictor of reinforcement over preceding trials. This pattern of performance reveals that the anterior thalamic nuclei are vital for attending to those stimuli that are the best predictors of reward. In their absence, unreliable predictors of reward usurp attentional control.