Proximal perimeter encoding in the rat rostral thalamus

Matulewicz, Paweł; Ulrich, Katharina; Mathiasen, M.; Aggleton, John P.; O’Mara, Shane M.

doi:10.1101/417881

Cited by 5 publications

(11 citation statements)

References 35 publications

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“…Accordingly, a picture of a distributed network of interconnected regions with egocentric vector representations is beginning to emerge. Given the presence of EBCs in several midline structures, it is possible that EBCs are also present in the anterior cingulate cortex as well as thalamic structures that innervate midline associative cortex (Weible et al, 2012; Matulewicz et al, 2019). Future investigations should focus on dependencies amongst the regions currently implicated, as the EBC network may possess functional and anatomical connectivity resembling the well-characterized extended head direction cell network (Taube et al, 2007).…”

Section: Discussionmentioning

confidence: 99%

Egocentric boundary vector tuning of the retrosplenial cortex

Alexander

Carstensen

Hinman

et al. 2019

Preprint

121

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31The retrosplenial cortex is reciprocally connected with a majority of structures implicated in 32 spatial cognition and damage to the region itself produces numerous spatial impairments. 33However, in many ways the retrosplenial cortex remains understudied. Here, we sought to 34 characterize spatial correlates of neurons within the region during free exploration in two-35 dimensional environments. We report that a large percentage of retrosplenial cortex neurons 36 have spatial receptive fields that are active when environmental boundaries are positioned at a 37 specific orientation and distance relative to the animal itself. We demonstrate that this vector-38 based location signal is encoded in egocentric coordinates, localized to the dysgranular 39 retrosplenial sub-region, independent of self-motion, and context invariant. Further, we identify a 40 sub-population of neurons with this response property that are synchronized with the 41 hippocampal theta oscillation. Accordingly, the current work identifies a robust egocentric spatial 42 code in retrosplenial cortex that can facilitate spatial coordinate system transformations and 43 support the anchoring, generation, and utilization of allocentric representations. 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 108 From a connectivity standpoint, the retrosplenial cortex (RSC) is an excellent candidate to 109 examine egocentric representations during navigation. Further, theoretical work has posited that 110 RSC forms a computational hub for supporting coordinate transformations (Byrne et al., 2007;111 Clark et al., 2018; Rounds et al., 2018; Bicankski and Burgess, 2018). RSC is composed of two 112 interconnected sub-regions, dysgranular (dRSC) and granular (gRSC), which have slightly 113 different connectivity with cortical and subcortical regions (Shibata et al., 2009). dRSC (in mice 114 agranular RSC) is positioned along the dorsal surface of the brain and possesses biased 115 interconnectivity with association, sensory, and motor processing regions that code in 116

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Section: Discussionmentioning

confidence: 99%

Egocentric boundary vector tuning of the retrosplenial cortex

Alexander

Carstensen

Hinman

et al. 2019

Preprint

121

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“…The grid-like signal found in these regions could, therefore, be thalamic rather than entorhinal in origin. In addition to the head-direction cells in the anterodorsal thalamic nucleus, the anteroventral nucleus possesses theta-modulated head-direction cells (Tsanov et al, 2011), while the anteromedial nucleus contains place cells and perimeter/boundary cells (Jankowski et al, 2015;Matulewicz et al, 2019). Bonnavie et al (2013) demonstrated that when the hippocampus was inactivated with muscimol, entorhinal grid cells lost their periodicity resulting in head direction cells.…”

Section: Discussionmentioning

confidence: 99%

“…In rodents, for instance, anterior thalamic lesions severely impair spatial learning, echoing the effects of hippocampal damage (Morris et al, 1982;Sutherland and Rodriguez, 1989;Moran and Dalrymple-Alford, 2003), with disconnection studies confirming the interdependence of the hippocampal formation and anterior thalamus (Warburton et al, 2000(Warburton et al, , 2001Henry et al, 2004). Moreover, neuronal recordings within the ATN show the presence of place, head direction and border cells (Taube, 1995;Jankowski et al, 2015;Matulewicz et al, 2019), suggesting the ATN is also a spatial processing node. Outstanding questions include whether any hippocampal formation spatial functions are dependent on the ATN and, if so, why.…”

Section: Introductionmentioning

confidence: 92%

“…Units were sorted using conventional cluster-cutting techniques (Tint, Axona Ltd.). Standard statistical testing was performed using an open-source custom-written suite in Python (NeuroChaT;Islam et al, 2019); additional custom codes in R, and Axona. Units were classified based on the spatiotemporal features of their activity in the open field during pellet-chasing, as described below.…”

Section: Statistical Analysis and Unit Classificationmentioning

confidence: 99%

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Anterior thalamic function is required for spatial coding in the subiculum and is necessary for spatial memory

Frost

Martin

Cafalchio

et al. 2020

Preprint

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Hippocampal function relies on the anterior thalamic nuclei, yet the reasons remain poorly understood. While anterior thalamic lesions disrupt parahippocampal spatial signalling, their impact on the subiculum is unknown, despite the importance of this area for hippocampal networks. We recorded subiculum cells in rats with either permanent (N-methyl-D-aspartic acid) or reversible (muscimol) anterior thalamic lesions. The diverse spatial signals normally found in the subiculum, including place cells, disappeared following permanent thalamic lesions and showed marked disruption during transient lesions. Meanwhile, permanent anterior thalamic lesions had no discernible impact on CA1 place fields. Thalamic lesions reduced spatial alternation performance (permanently or reversibly) to chance levels, while leaving a non-spatial recognition memory task unaffected. These findings, which help to explain why anterior thalamic damage is so deleterious for spatial memory, cast a new spotlight on the importance of subiculum function, and reveal its dependence on anterior thalamic signalling.

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“…(The one possible exception concerns the appreciation that the anterodorsal thalamic nucleus contains headdirection cells; 2007). Unexpectedly, there are cells in all of these regions that code for aspects of three-dimensional space, including positional information, boundary or perimeter information, as well as head directional and object information (Jankowski et al, 2014;2015;2017;Jankowski and O'Mara, 2015;Matulewicz et al, 2019). Moreover, it is now clear that lesions of the rostral and anterior thalamic nuclei can result in deficits in the performance of spatial and non-spatial tasks that appear comparable to those resulting from lesions within the entorhinal-hippocampal axis.…”

Section: Introductionmentioning

confidence: 99%

Space and Memory (far) beyond the Hippocampus: Many Subcortical Structures also Support Cognitive Mapping and Mnemonic Processing

O’Mara¹,

Aggleton²

2019

Preprint

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Memory research remains focused on just a few brain structures – in particular, the hippocampal formation (the hippocampus and entorhinal cortex). Three key discoveries promote this continued focus: the striking demonstrations of enduring anterograde amnesia after bilateral hippocampal damage; the realisation that synapses in the hippocampal formation are plastic e.g., when responding to short bursts of patterned stimulation (‘long-term potentiation’ or LTP); and the discovery of a panoply of spatially-tuned cells, principally surveyed in the hippocampal formation (place cells coding for position; head-direction cells, providing compass-like information; and grid cells, providing a metric for 3D space). Recent anatomical, behavioural, and electrophysiological work extends this picture to a growing network of subcortical brain structures (including the anterior thalamic nuclei, rostral midline thalamic nuclei, and the claustrum). There are, for example, spatially-tuned cells in all of these regions, including cells with properties similar to place cells of the hippocampus proper. These findings add new perspectives to what had been originally been proposed - but often overlooked - half a century ago: that damage to an extended network of structures connected to the hippocampal formation results in diencephalic amnesia. We suggest these new findings extend spatial signalling in the brain far beyond the hippocampal formation, with profound implications for theories of the neural bases of spatial and mnemonic functions.

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Proximal perimeter encoding in the rat rostral thalamus

Cited by 5 publications

References 35 publications

Egocentric boundary vector tuning of the retrosplenial cortex

Egocentric boundary vector tuning of the retrosplenial cortex

Anterior thalamic function is required for spatial coding in the subiculum and is necessary for spatial memory

Space and Memory (far) beyond the Hippocampus: Many Subcortical Structures also Support Cognitive Mapping and Mnemonic Processing

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