Thalamus and claustrum control parallel layer 1 circuits in retrosplenial cortex.

Ellen Kw Brennan,Omar J Ahmed,Izabela Jedrasiak-Cape,Shyam Kumar Sudhakar,Sharena P Rice,Sameer Kailasa

doi:10.7554/elife.62207

Ellen Kw Brennan, Omar J Ahmed + Show 4 more

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https://doi.org/10.7554/elife.62207

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Journal: eLife	Publication Date: Jun 25, 2021
Citations: 33	License type: CC BY 4.0

Affiliation: University of Michigan–Ann Arbor

Abstract

The granular retrosplenial cortex (RSG) is critical for both spatial and non-spatial behaviors, but the underlying neural codes remain poorly understood. Here, we use optogenetic circuit mapping in mice to reveal a double dissociation that allows parallel circuits in superficial RSG to process disparate inputs. The anterior thalamus and dorsal subiculum, sources of spatial information, strongly and selectively recruit small low-rheobase (LR) pyramidal cells in RSG. In contrast, neighboring regular-spiking (RS) cells are preferentially controlled by claustral and anterior cingulate inputs, sources of mostly non-spatial information. Precise sublaminar axonal and dendritic arborization within RSG layer 1, in particular, permits this parallel processing. Observed thalamocortical synaptic dynamics enable computational models of LR neurons to compute the speed of head rotation, despite receiving head direction inputs that do not explicitly encode speed. Thus, parallel input streams identify a distinct principal neuronal subtype ideally positioned to support spatial orientation computations in the RSG.

Highlights

Activity in the granular retrosplenial cortex (RSG) is correlated with a wide variety of behaviors, including spatial navigation, learning, memory, fear conditioning, imagination, and planning for the future (Alexander et al, 2020; Alexander and Nitz, 2017; Chang et al, 2020; Chrastil, 2018; Hinman et al, 2018; Mao et al, 2018; Miller et al, 2021; Miller et al, 2019)
From resting membrane potentials of approximately À65 mV, LR neurons were strongly driven past spike threshold by these thalamic inputs while RS neurons exhibited far smaller excitatory postsynaptic potential (EPSP) (Figure 1F)
Using the same channelrhodopsin-assisted circuit mapping (CRACM) approach to examine anterior cingulate cortex (ACC) inputs to RSG (Figure 4A), we found that corticocortical inputs from the anterior cingulate target L1b/c and, to a lesser extent, layer 5 (L5) (Figure 4B), partially resembling the laminar pattern seen with CLA arbors (Figure 3B) and overlapping precisely with RS, but not LR, dendrites (Figure 3C&D)

Summary

Introduction

Activity in the granular retrosplenial cortex (RSG) is correlated with a wide variety of behaviors, including spatial navigation, learning, memory, fear conditioning, imagination, and planning for the future (Alexander et al, 2020; Alexander and Nitz, 2017; Chang et al, 2020; Chrastil, 2018; Hinman et al, 2018; Mao et al, 2018; Miller et al, 2021; Miller et al, 2019). The RSG is among the most densely connected regions of the brain, integrating inputs from a bevy of cortical and subcortical sources and serving as part of the default mode network (Greicius et al, 2009; Kaboodvand et al, 2018; Liu et al, 2019; Whitesell et al, 2021) While these anatomical connections are well-documented (Van Groen and Wyss, 2003; van Groen and Wyss, 1990; Whitesell et al, 2021; Wyss and Van Groen, 1992), few studies have examined their functional nature (Nitzan et al, 2020; Yamawaki et al, 2019b; Yamawaki et al, 2019a; Yamawaki et al, 2016a), and cell-type specificity has yet to be sufficiently explored. Thalamic relay cells (Clascaet al., 2012) are grouped into three distinct classes: core, intralaminar, and paralaminar/ventral midline (matrix) nuclei (Hanbery and Jasper, 1953; Herkenham, 1986; Jones, 2001; Jones, 1998; Morison and Dempsey, 1941; Rubio-Garrido et al, 2009)

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