Long-Term Value Memory in the Primate Posterior Thalamus for Fast Automatic Action

• Published in: Current biology Vol. 30; no. 15; pp. 2901 - 2911.e3
• Main Authors: Kim, Hyoung F., Griggs, Whitney S., Hikosaka, Okihide
• Format: Journal Article
• Language: English
• Published: England Elsevier Inc 03.08.2020
• Subjects: habit; long-term memory; monkey; object value; subcortical visual pathway; superior colliculus; suprageniculate nucleus; tail of the caudate nucleus; thalamus; visual object; monkey; habit; superior colliculus; subcortical visual pathway; tail of the caudate nucleus; object value; suprageniculate nucleus; visual object; long-term memory; thalamus
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2020.05.047

The thalamus is known to process information from various brain regions and relay it to other brain regions, serving an essential role in sensory perception and motor execution. The thalamus also receives inputs from basal ganglia nuclei (BG) involved in value-based decision making, suggesting a role in the value process. We found that neurons in a particular area of the rhesus macaque posterior thalamus encoded the historical value memory of visual objects. Many of these value-coding neurons were located in the suprageniculate nucleus (SGN). This thalamic area directly received anatomical input from the superior colliculus (SC), and the neurons showed visual responses with contralateral preferences. Notably, the value discrimination activity of these thalamic neurons increased during learning, with the learned values stably retained even more than 200 days after learning. Our data indicate that single neurons in the posterior thalamus not only processed simple visual information but also represented historical values. Furthermore, our data suggest an SC-posterior thalamus-BG-SC subcortical loop circuit that encodes the historical value, enabling a quick automatic gaze by bypassing the visual cortex. •Complex visual objects activate the posterior thalamus, including the SGN•Posterior thalamus receives subcortical visual inputs and projects to the striatum•Posterior thalamic neurons retain reward values of learned objects•The posterior thalamus guides fast habitual actions by bypassing the visual cortex Kim et al. find a subcortical loop circuit that generates habitual actions quickly. The posterior thalamus in the loop circuit stably retains reward value memories, even more than 200 days after learning. Historical values can be processed through this short subcortical circuit by bypassing the visual cortex, thus guiding fast automatic actions.