Midline thalamic neurons are differentially engaged during hippocampus network oscillations

Ariel Lara-Vásquez,Marcelo Stockle,Pablo Fuentealba,Nelson Espinosa,Ernesto Durán

doi:10.1038/srep29807

Ariel Lara-Vásquez, Marcelo Stockle + Show 3 more

Open Access

https://doi.org/10.1038/srep29807

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Journal: Scientific Reports	Publication Date: Jul 1, 2016
Citations: 27	License type: CC BY 4.0

Affiliation: Pontificia Universidad Católica de Chile

Abstract

The midline thalamus is reciprocally connected with the medial temporal lobe, where neural circuitry essential for spatial navigation and memory formation resides. Yet, little information is available on the dynamic relationship between activity patterns in the midline thalamus and medial temporal lobe. Here, we report on the functional heterogeneity of anatomically-identified thalamic neurons and the differential modulation of their activity with respect to dorsal hippocampal rhythms in the anesthetized mouse. Midline thalamic neurons expressing the calcium-binding protein calretinin, irrespective of their selective co-expression of calbindin, discharged at overall low levels, did not increase their activity during hippocampal theta oscillations, and their firing rates were inhibited during hippocampal sharp wave-ripples. Conversely, thalamic neurons lacking calretinin discharged at higher rates, increased their activity during hippocampal theta waves, but remained unaffected during sharp wave-ripples. Our results indicate that the midline thalamic system comprises at least two different classes of thalamic projection neuron, which can be partly defined by their differential engagement by hippocampal pathways during specific network oscillations that accompany distinct behavioral contexts. Thus, different midline thalamic neuronal populations might be selectively recruited to support distinct stages of memory processing, consistent with the thalamus being pivotal in the dialogue of cortical circuits.

Highlights

We report on the functional heterogeneity of anatomically-identified thalamic neurons and the differential modulation of their activity with respect to dorsal hippocampal rhythms in the anesthetized mouse
By recording and labeling individual neurons in anesthetized mice, we show here evidence for functionally distinct neuronal populations in the midline thalamus
Our data show that rather than anatomical location, a major defining feature in the physiological properties of midline thalamic neurons is the expression of CR, a calcium-binding protein

Summary

Introduction

We report on the functional heterogeneity of anatomically-identified thalamic neurons and the differential modulation of their activity with respect to dorsal hippocampal rhythms in the anesthetized mouse. Midline thalamic neurons expressing the calcium-binding protein calretinin, irrespective of their selective co-expression of calbindin, discharged at overall low levels, did not increase their activity during hippocampal theta oscillations, and their firing rates were inhibited during hippocampal sharp wave-ripples. The reuniens nucleus is implicated in system consolidation of memory[18,19] and strategy shifting[20], and recent experiments have demonstrated that is contains head-direction cells[21] Such cognitive and executive functions are implemented by the coordinated action of the frontal and medial temporal lobes[22,23]; suggesting that the midline thalamus is probably important to sustain cortical interactions underlying memory processing[5,24,25]. The hippocampus is directly targeted by ventral midline thalamic nuclei, by the reuniens and rhomboidal nuclei[26,27,28], whereas most of the midline thalamus receives reciprocal afferents from the hippocampus via the subiculum[29,30,31,32]

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