Functional properties of corticothalamic circuits targeting paraventricular thalamic neurons

Guillermo Aquino-Miranda; Dounya Jalloul; Xu O Zhang; Sa Li; Gilbert J Kirouac; Michael Beierlein; Fabricio H Do Monte

doi:10.1016/j.neuron.2024.10.010

Functional properties of corticothalamic circuits targeting paraventricular thalamic neurons

Neuron. 2024 Nov 2:S0896-6273(24)00731-1. doi: 10.1016/j.neuron.2024.10.010. Online ahead of print.

Authors

Guillermo Aquino-Miranda¹, Dounya Jalloul², Xu O Zhang², Sa Li³, Gilbert J Kirouac³, Michael Beierlein², Fabricio H Do Monte⁴

Affiliations

¹ Department of Neurobiology and Anatomy, McGovern Medical School, The University of Texas Health Science Center at Houston, 6431 Fannin Street, Houston, TX 77030, USA.
² Department of Neurobiology and Anatomy, McGovern Medical School, The University of Texas Health Science Center at Houston, 6431 Fannin Street, Houston, TX 77030, USA; MD Anderson Cancer Center UTHealth Houston Graduate School of Biomedical Sciences, 6767 Bertner Ave, Houston, TX 77030, USA.
³ Rady Faculty of Health Sciences, University of Manitoba, 780 Bannatyne Avenue, Winnipeg, MB R3E 0W2, Canada.
⁴ Department of Neurobiology and Anatomy, McGovern Medical School, The University of Texas Health Science Center at Houston, 6431 Fannin Street, Houston, TX 77030, USA; MD Anderson Cancer Center UTHealth Houston Graduate School of Biomedical Sciences, 6767 Bertner Ave, Houston, TX 77030, USA. Electronic address: fabricio.h.domonte@uth.tmc.edu.

PMID: 39504962
DOI: 10.1016/j.neuron.2024.10.010

Abstract

Corticothalamic projections to sensorimotor thalamic nuclei show modest firing rates and serve to modulate the activity of thalamic relay neurons. By contrast, here we find that high-order corticothalamic projections from the prelimbic (PL) cortex to the anterior paraventricular thalamic nucleus (aPVT) maintain high-frequency activity and evoke strong synaptic excitation of aPVT neurons in rats. In a significant fraction of aPVT cells, such high-frequency excitation of PL-aPVT projections leads to a rapid decay of action potential amplitudes, followed by a depolarization block (DB) that strongly limits aPVT maximum firing rates, thereby regulating both defensive and appetitive behaviors in a frequency-dependent manner. Strong inhibitory inputs from the anteroventral portion of the thalamic reticular nucleus (avTRN) inhibit the firing rate of aPVT neurons during periods of high-spike fidelity but restore it during prominent DB, suggesting that avTRN activity can modulate the effects of PL inputs on aPVT firing rates to ultimately control motivated behaviors.

Keywords: active avoidance; defensive behavior; depolarization block; feedforward inhibition; food seeking; midline thalamus; prelimbic prefrontal cortex; short-term synaptic plasticity; thalamic reticular nucleus.