Abstract
It is proposed that mediodorsal thalamus contributes to cognition via interactions with prefrontal cortex. However, there is relatively little evidence detailing the interactions between mediodorsal thalamus and prefrontal cortex linked to cognition in primates. This study investigated these interactions during learning, memory, and decision-making tasks in rhesus monkeys using a disconnection lesion approach. Preoperatively, monkeys learned object-in-place scene discriminations embedded within colorful visual backgrounds. Unilateral neurotoxic lesions to magnocellular mediodorsal thalamus (MDmc) impaired the ability to learn new object-in-place scene discriminations. In contrast, unilateral ablations to ventrolateral and orbital prefrontal cortex (PFv+o) left learning intact. A second unilateral MDmc or PFv+o lesion in the contralateral hemisphere to the first operation, causing functional MDmc–PFv+o disconnection across hemispheres, further impaired learning object-in-place scene discriminations, although object discrimination learning remained intact. Adaptive decision-making after reward satiety devaluation was also reduced. These data highlight the functional importance of interactions between MDmc and PFv+o during learning object-in-place scene discriminations and adaptive decision-making but not object discrimination learning. Moreover, learning deficits observed after unilateral removal of MDmc but not PFv+o provide direct behavioral evidence of the MDmc role influencing more widespread regions of the frontal lobes in cognition.
Highlights
It is a widely held view that direct cortico-cortical connections convey perceptual, motor, and cognitive information, whereas it is customary to think of the thalamus as a structure relaying sensorimotor information (Sherman and Guillery 2002)
All monkeys spent an average of 16.1 min in the devaluation test sessions. This current study assessed cognitive abilities, including learning new object-in-place scene discriminations, learning object discriminations, and adaptive decision-making in monkeys who received either unilateral MDmc neurotoxic lesions or unilateral PFv+o ablation lesions and after either combined contralateral or ipsilateral hemisphere disconnection of MDmc and PFv+o
These experiments produced several important findings and provide the first causal evidence in primates to support the hypothesis that interactions between the MDmc and PFv+o are critical for learning object-in-place scene discriminations and adaptive decision-making
Summary
It is a widely held view that direct cortico-cortical connections convey perceptual, motor, and cognitive information, whereas it is customary to think of the thalamus as a structure relaying sensorimotor information (Sherman and Guillery 2002). Mounting evidence shows that some thalamic nuclei (e.g., mediodorsal thalamus via cortico-thalamo-cortical links) may modulate information transfer across cortical areas and, via these interconnections may influence cognition and behavior in their own right (Jones 2007; Sherman and Guillery 2011; Wurtz et al 2011; Mitchell et al 2014). The mediodorsal thalamus in primates and rodents has several distinct subdivisions, each with its own unique anatomical links with other brain regions (Mitchell and Chakraborty 2013). The anatomy pertaining to the magnocellular subdivision of the mediodorsal thalamus (MDmc) involves reciprocal and crossed interconnections with lateral and medial orbital prefrontal cortex (Preuss and Goldman-Rakic 1987; Ray and Price 1993). The neuronal signals flowing to and from MDmc suggest that it plays a critical role in cognition
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