Thalamus and claustrum control parallel layer 1 circuits in retrosplenial cortex

Abstract

The granular retrosplenial cortex (RSG) is critical for both spatial navigation and fear conditioning, but the neural codes enabling these seemingly disparate functions remain unknown. Here, using optogenetic circuit mapping, we reveal a double dissociation that allows parallel circuits in superficial RSG to process navigation- versus fear-related inputs. The anterior thalamus, a source of head direction information, strongly recruits small, low rheobase (LR) pyramidal cells in RSG layer 3. Neighboring regular-spiking (RS) cells are instead preferentially controlled by claustral and anterior cingulate inputs, sources of higher-order and fear-related information. Precise sublaminar axonal and dendritic arborization within RSG layer 1 enable this parallel processing. Synaptic dynamics and computational modeling suggest LR neurons are optimally-tuned conjunctive encoders of direction and distance inputs from the thalamus and dorsal subiculum, respectively. RS cells are better positioned to support contextual fear memories. Thus, parallel input streams to computationally-distinct principal neurons help facilitate diverse RSG functions.

Regional and cell type-specific afferent and efferent projections of the mouse claustrum

“…Our single neuron tracing data are much better than the bulk tracing technique to identify the laminar distribution of their cortical targets without contamination. Different laminar distributions between claustrocortical projections and thalamocortical projections influence different cell types in the cortex (Brennan et al, 2021). It may be underly the mechanisms that neuron responses differ in cortical areas, layers and cell types after optical activating the CLA neurons (McBride et al, 2022)…”

Multisensory coding of angular head velocity in the retrosplenial cortex

“…Yet again, despite reports of head direction cells (Jankowski et al, 2015;Tsanov et al, 2011), AHV-tuned neurons have not been reported in these thalamic structures. Interestingly, recent modeling data suggest that synaptic dynamics of anterior thalamic inputs to the RSP may transform the head direction input to angular speed signal (Brennan et al, 2021). Alternatively, the laterodorsal thalamus, which receives direct afferents from the medial vestibular nucleus (Shiroyama et al, 1999) could be a source of AHV information.…”

Influence of claustrum on cortex varies by area, layer, and cell type

“…Another study also recorded in PFC but used different, prolonged CLA optogenetic stimulation patterns and found that a majority of frontal neurons increased in firing rate, rather than decreased (Fodoulian et al, 2020). In addition, a recent slice physiology study found that stimulation of CLA axons drove robust excitatory post-synaptic potentials in RSP pyramidal neurons (Brennan et al, 2021). Thus, the nature of CLA's influence on cortex remains unresolved.…”