Thalamic amplification of cortical connectivity sustains attentional control

Abstract

While interactions between the thalamus and cortex are critical for cognitive function1–3, the exact contribution of the thalamus to these interactions is often unclear. Recent studies have shown diverse connectivity patterns across the thalamus 4,5, but whether this diversity translates to thalamic functions beyond relaying information to or between cortical regions6 is unknown. Here, by investigating prefrontal cortical (PFC) representation of two rules used to guide attention, we find that the mediodorsal thalamus (MD) sustains these representations without relaying categorical information. Specifically, MD input amplifies local PFC connectivity, enabling rule-specific neural sequences to emerge and thereby maintain rule representations. Consistent with this notion, broadly enhancing PFC excitability diminishes rule specificity and behavioral performance, while enhancing MD excitability improves both. Overall, our results define a previously unknown principle in neuroscience; thalamic control of functional cortical connectivity. This function indicates that the thalamus plays much more central roles in cognition than previously thought.

Thalamic Control of Cognition and Social Behavior Via Regulation of Gamma-Aminobutyric Acidergic Signaling and Excitation/Inhibition Balance in the Medial Prefrontal Cortex

“…We predict that high levels of inhibition suppress the activity of functional units of neurons or microcolumns representing distracting information. In concert with the appropriate patterns of excitation, dynamic regulation of these two opposing forces likely support the maintenance of delay-dependent neuronal activity and sustain rule representations in the mPFC as was demonstrated recently (2, 4). Enabling excitatory reverberation to be preferentially sustained within microcolumns representing the correct information could allow the mPFC to optimally process incoming task-related information that can be fed forward to drive the appropriate behavior (Fig 8).…”

“…A prime opportunity to advance our understanding of mPFC function is by focusing on the mechanisms of communication with one of its primary gateways, the mediodorsal thalamus (MD). However, despite recent progress (2–4), our grasp on the nature of the interaction between these two structures remains limited.…”

Thalamic control of functional cortical connectivity

“…In a recent study, we investigated the role of the mediodorsal thalamus (MD) in sustaining distinct categorical representations in the PFC, and ones that are dependent on recurrent lateral interactions between PFC subnetworks [33]. These observations were made in the context of an attentional control task, where mice selected between conflicting visual and auditory targets based on one of two task rules that were randomly presented on a trial-by-trial basis.…”

Abnormal distraction and load‐specific connectivity during working memory in cognitively normal Parkinson's disease

“…We identified ROI from the first‐level voxelwise analyses that showed significant effects of distraction and load for each phase (encoding and retrieval) of the analyses in the combined PD and control groups (Tables S1 and S2). To reduce the dimensionality of the data set and minimize the number of multiple comparisons, seeds were constrained to regions commonly implicated in WM, namely frontal–parietal (Linden et al, ; McNab & Klingberg, ; Murray et al, ), occipital (Galeano Weber et al, ), parahippocampus (Ranganath & Ritchey, ), basal‐ganglia (Cools & D'Esposito, ; McNab & Klingberg, ; Murty et al, ), and thalamus (Hazy et al, ; Schmitt et al, ). Table S3 describes the seeds that were constructed from ROI from the first‐level voxelwise tests.…”