A thalamocortical circuit for updating action-outcome associations

Abstract

The ability to flexibly use knowledge is one cardinal feature of goal-directed behaviors. We recently showed that thalamocortical and corticothalamic pathways connecting the medial prefrontal cortex and the mediodorsal thalamus (MD) contribute to adaptive decision-making (Alcaraz et al., 2018). In this study, we examined the impact of disconnecting the MD from its other main cortical target, the orbitofrontal cortex (OFC) in a task assessing outcome devaluation after initial instrumental training and after reversal of action-outcome contingencies. Crossed MD and OFC lesions did not impair instrumental performance. Using the same approach, we found however that disconnecting the OFC from its other main thalamic afferent, the submedius nucleus, produced a specific impairment in adaptive responding following action-outcome reversal. Altogether, this suggests that multiple thalamocortical circuits may act synergistically to achieve behaviorally relevant functions.

Keywords: adaptive decision-making; disconnection; mediodorsal thalamus; neuroscience; orbitofrontal cortex; rat; reversal; submedius thalamic nucleus.

Figure 1.. Unilateral cortical and thalamic lesions.

Photomicrographs of thionin-stained coronal sections showing representative OFC (A), MD (B) and Sub (C) lesions. A dotted line highlights thalamic lesions. The extent of each lesion for the included rats is shown on the right (D–F) with the largest lesion shown in gray and the smallest in black (from top to bottom: OFC, MD and Sub). Numbers indicate approximate location relative to bregma (in mm).

Figure 2.. Experimental paradigm to assess flexible goal-directed responding.

The design is adapted from Parkes et al. (2018) and consists in providing a choice test following outcome devaluation after an initial instrumental training phase (green), but also after reversal of action-outcome contingencies (orange).

Figure 3.. Disconnecting the OFC and the MD.

Mean rate of lever presses (± sem) during instrumental conditioning (A) or during action-outcome contingency reversal (D). Lever presses (% Baseline,+ sem) during the initial choice test (B) or following contingency reversal (E). Consumption tests following the initial choice test (C) and the post-reversal test (F).

Figure 4.. Disconnecting the OFC and the Sub.

Mean rate of lever presses (± sem) during instrumental conditioning (A) or during action-outcome contingency reversal (D). Lever presses (% Baseline,+ sem) during the choice test that followed outcome devaluation immediately after initial instrumental conditioning (B) or contingency reversal (E). Consumption tests following the initial choice test (C) or the post-reversal one (F).