Robust information routing by dorsal subiculum neurons

Kitanishi, Takuma; Umaba, Ryoko; Mizuseki, Kenji

doi:10.1126/sciadv.abf1913

Cited by 60 publications

(81 citation statements)

References 90 publications

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“…axis versus boundary vector cells) to LR cells interacts with thalamic head direction inputs. Very recent work on understanding the tuning properties of subicular cells in a projection-specific manner will help to narrow the functional range of possible dorsal subicular inputs to LR cells ( Kitanishi et al, 2021 ). We anticipate that one key impact of dorsal subicular inputs to LR cells will be to impose a spatial filter on the angular speed and directional predictions stated above.…”

Section: Discussionmentioning

confidence: 99%

Thalamus and claustrum control parallel layer 1 circuits in retrosplenial cortex

Brennan

Jedrasiak‐Cape

Kailasa

et al. 2021

eLife

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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.

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Section: Discussionmentioning

confidence: 99%

Thalamus and claustrum control parallel layer 1 circuits in retrosplenial cortex

Brennan

Jedrasiak‐Cape

Kailasa

et al. 2021

eLife

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“…ICA results that were significantly correlated with behavior, on average weighted the dSub contribution higher than any other brain region and dSub was one of the only individual brain regions that was significantly correlated with behavioral performance, despite pTau densities that were lower than 6 of the 7 other brain regions. Sub is one of the major outputs of CA1 and entorhinal cortex, and passes information to cortical areas, including RSC (Kitanishi et al, 2021). Previous research has shown that Sub can be partitioned into two regions, distal Sub and proximal Sub, which have been shown to be structurally and functionally different.…”

Section: Discussionmentioning

confidence: 99%

“…Interestingly, Sub neurons have been shown to represent spatial information, such as place, speed, and trajectory, as accurately, or even more so, than CA1. An important role of Sub may be to create noise-resistant, high-firing rate, accurate representations for multiple types of navigational information (Kitanishi et al, 2021). Thus, Tau accumulation in Sub may be a critical driver of early hippocampal-parietal network dysfunction leading to the emergence of impaired spatial navigation in AD.…”

Section: Discussionmentioning

confidence: 99%

Tau Pathology Profile Across a Parietal-Hippocampal Brain Network Is Associated With Spatial Reorientation Learning and Memory Performance in the 3xTg-AD Mouse

Stimmell

Moseley

et al. 2021

Front. Aging

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In early Alzheimer's disease (AD) spatial navigation is one of the first impairments to emerge; however, the precise cause of this impairment is unclear. Previously, we showed that, in a mouse model of tau and amyloid beta (Aβ) aggregation, getting lost represents, at least in part, a failure to use distal cues to get oriented in space and that impaired parietal-hippocampal network level plasticity during sleep may underlie this spatial disorientation. However, the relationship between tau and amyloid beta aggregation in this brain network and impaired spatial orientation has not been assessed. Therefore, we used several approaches, including canonical correlation analysis and independent components analysis tools, to examine the relationship between pathology profile across the parietal-hippocampal brain network and spatial reorientation learning and memory performance. We found that consistent with the exclusive impairment in 3xTg-AD 6-month female mice, only 6-month female mice had an ICA identified pattern of tau pathology across the parietal-hippocampal network that were positively correlated with behavior. Specifically, a higher density of pTau positive cells predicted worse spatial learning and memory. Surprisingly, despite a lack of impairment relative to controls, 3-month female, as well as 6- and 12- month male mice all had patterns of tau pathology across the parietal-hippocampal brain network that are predictive of spatial learning and memory performance. However, the direction of the effect was opposite, a negative correlation, meaning that a higher density of pTau positive cells predicted better performance. Finally, there were not significant group or region differences in M78 density at any of the ages examined and ICA analyses were not able to identify any patterns of 6E10 staining across brain regions that were significant predictors of behavioral performance. Thus, the pattern of pTau staining across the parietal-hippocampal network is a strong predictor of spatial learning and memory performance, even for mice with low levels of tau accumulation and intact spatial re-orientation learning and memory. This suggests that AD may cause spatial disorientation as a result of early tau accumulation in the parietal-hippocampal network.

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“…Both the CLA and ACC are heavily implicated in a range of non-spatial behaviors often described as being “cognitive” or “mnemonic” in function (Botvinick, 2007; Brown and Braver, 2005; Carter et al, 1998; Devinsky et al, 1995; Kim et al, 2016; Mohanty et al, 2007; Smith et al, 2012; Smythies et al, 2012; Stevens et al, 2011), but there is also evidence that these regions exhibit some degree of spatial information processing (Guterstam et al, 2015; Jankowski and O’Mara, 2015; Sutherland et al, 1988; Whishaw et al, 2001). Indeed, 7-15% of cells in the claustrum were found to encode place or boundary-related information (Jankowski and O’Mara, 2015), though this percentage is relatively low compared to the 60% of anterior thalamic (Taube, 1998) and 61% of dorsal subicular (Kitanishi et al, 2021) neurons that are known to clearly encode elemental direction, place, and other spatial features. Regardless, retrosplenial RS neurons may be receiving direct spatial inputs from the CLA and ACC in addition to the cognitive and mnemonic information relayed by these two regions.…”

Section: Discussionmentioning

confidence: 99%

Thalamus and claustrum control parallel layer 1 circuits in retrosplenial cortex

Brennan

Jedrasiak‐Cape

Kailasa

et al. 2020

Preprint

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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.

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Robust information routing by dorsal subiculum neurons

Cited by 60 publications

References 90 publications

Thalamus and claustrum control parallel layer 1 circuits in retrosplenial cortex

Thalamus and claustrum control parallel layer 1 circuits in retrosplenial cortex

Tau Pathology Profile Across a Parietal-Hippocampal Brain Network Is Associated With Spatial Reorientation Learning and Memory Performance in the 3xTg-AD Mouse

Thalamus and claustrum control parallel layer 1 circuits in retrosplenial cortex

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