Evidence for two distinct thalamocortical circuits in retrosplenial cortex

Lomi, Eleonora; Mathiasen, M.; Cheng, Han Yin; Zhang, Ningyu; Aggleton, John P.; Mitchell, Anna S.; Jeffery, Kate J.

doi:10.1016/j.nlm.2021.107525

Cited by 21 publications

(24 citation statements)

References 115 publications

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“…It would also be informative to learn whether many or only some neural projections from the ATN support this example of non-spatial paired-associate learning. Neuroanatomical evidence suggests a different pattern of neural connections with limbic and cortical memory structures among the three ATN nuclei, that is, the anterodorsal nuclei, anteroventral nuclei and the anteromedial nuclei (Bubb et al, 2017;Lomi et al, 2021;Nelson, 2021). In addition, these ATN component nuclei have different molecular and electrophysiological characteristics that may underpin different behavioural functions (Jankowski et al, 2013;Roy et al, 2021Roy et al, , 2022Safari et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

Anterior thalamic nuclei: A critical substrate for non‐spatial paired‐associate memory in rats

Hamilton

Dalrymple‐Alford

2022

Eur J of Neuroscience

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Injury or dysfunction in the anterior thalamic nuclei (ATN) may be the key contributory factor in many instances of diencephalic amnesia. Experimental ATN lesions impair spatial memory and temporal discriminations, but there is only limited support for a more general role in non-spatial memory. To extend evidence on the effects of ATN lesions, we examined the acquisition of biconditional associations between odour and object pairings presented in a runway, either with or without a temporal gap between these items. Intact adult male rats acquired both the no-trace and 10-s trace versions of this non-spatial task.Intact rats trained in the trace version showed elevated Zif268 activation in the dorsal CA1 of the hippocampus, suggesting that the temporal component recruited additional neural processing. ATN lesions completely blocked acquisition on both versions of this association-memory task. This deficit was not due to poor inhibition to non-rewarded cues or impaired sensory processing, because rats with ATN lesions were unimpaired in the acquisition of simple odour discriminations and simple object discriminations using similar task demands in the same apparatus. This evidence challenges the view that impairments in arbitrary paired-associate learning after ATN lesions require the use of multimodal spatial stimuli. It suggests that diencephalic amnesia associated with the ATN stems from degraded attention to stimulus-stimulus associations and their representation across a distributed memory system.

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Section: Discussionmentioning

confidence: 99%

Anterior thalamic nuclei: A critical substrate for non‐spatial paired‐associate memory in rats

Hamilton

Dalrymple‐Alford

2022

Eur J of Neuroscience

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“…The former explanation (direct spread) appears unlikely given the wide spacing of the retrosplenial injections in this and the previous study (Horikawa et al, 1988). To test for the second explanation (direct cingulum body uptake) we examined both the injection sites and the topography of retrogradely labelled cells within the anterior thalamic nuclei to see if they matched previous descriptions for that part of the retrosplenial cortex (Bubb et al, 2020;Lomi et al, 2021;Perry et al, 2021;Shibata, 1993;Sripanidkulchai & Wyss, 1986) or whether the labelled cells were distributed broadly across the nuclei, that is, more consistent with cingulum uptake. By these measures we did not find evidence of direct cingulum bundle uptake.…”

Section: Discussionmentioning

confidence: 66%

“…This method will give higher double-cell counts if there is a bias towards zones of label overlap. In contrast, the present study counted cells across each entire nucleus, a method likely to reduce the proportions of double-labelled cells given the topographic origins of many of the cortical projections from within the target nuclei (Lomi et al, 2021;Shibata, 1993;Sripanidkulchai & Wyss, 1986). Even though the counting methods in the present study tended to be conservative (as indicated by parallel confocal analyses), when cell counts are made across the entire nucleus (Condé et al, 1990;Horikawa et al, 1988;Varela et al, 2014) the proportions of double-labelled cells were more comparable to those in the present study.…”

Section: Discussionmentioning

confidence: 96%

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Collateral rostral thalamic projections to prelimbic, infralimbic, anterior cingulate and retrosplenial cortices in the rat brain

Yanakieva

Mathiasen

Amin

et al. 2022

Eur J of Neuroscience

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As the functional properties of a cortical area partly reflect its thalamic inputs, the present study compared collateral projections arising from various rostral thalamic nuclei that terminate across prefrontal (including anterior cingulate) and retrosplenial areas in the rat brain. Two retrograde tracers, fast blue and cholera toxin B, were injected in pairs to different combinations of cortical areas. The research focused on the individual anterior thalamic nuclei, including the interanteromedial nucleus, nucleus reuniens and the laterodorsal nucleus. Of the principal anterior thalamic nuclei, only the anteromedial nucleus contained neurons reaching both the anterior cingulate cortex and adjacent cortical areas (prefrontal or retrosplenial), though the numbers were modest. For these same cortical pairings (medial prefrontal/anterior cingulate and anterior cingulate/retrosplenial), the interanteromedial nucleus and nucleus reuniens contained slightly higher proportions of bifurcating neurons (up to 11% of labelled cells). A contrasting picture was seen for collaterals reaching different areas within retrosplenial cortex. Here, the anterodorsal nucleus, typically provided the greatest proportion of bifurcating neurons (up to 15% of labelled cells). While individual neurons that terminate in different retrosplenial areas were also found in the other thalamic nuclei, they were infrequent. Consequently, these thalamo‐cortical projections predominantly arise from separate populations of neurons with discrete cortical termination zones, consistent with the transmission of segregated information and influence. Overall, two contrasting medial‐lateral patterns of collateral projections emerged, with more midline nuclei, for example, nucleus reuniens and the interoanteromedial nucleus innervating prefrontal areas, while more dorsal and lateral anterior thalamic collaterals innervated retrosplenial cortex.

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“…While this is possible, it could also be the case that distinct AV subpopulations and their circuits have differential functional roles. This functional heterogeneity may map onto the well-known subdivisions within AV thalamus, specifically the anteroventral dorsomedial (AVDM) and anteroventral ventrolateral (AVVL) parts ( 29 , 30 ), or the anterior–posterior axis as has been shown for other thalamic nuclei ( 31 ). Additional work is needed to reveal potential functional heterogeneity (i.e., the presence of thalamic subnetworks) within AV thalamus ( 32 ).…”

Section: Discussionmentioning

confidence: 89%

Anterior thalamic circuits crucial for working memory

Roy

Zhang

Aida

et al. 2022

Proc. Natl. Acad. Sci. U.S.A.

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Significance Anterior thalamus exhibits significant functional changes with increasing age. While it has been associated with cognitive functions, the specific circuitry relevant for working memory remains unknown. The significance of this study is threefold: First, the anteroventral subdivision of anterior thalamic nuclei is necessary for working memory maintenance; second, aged mice showed a decrease in the excitability of anteroventral thalamic neurons, which correlated with a working memory impairment; and third, activating anteroventral thalamic neurons in aged mice was sufficient to improve their working memory.

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Evidence for two distinct thalamocortical circuits in retrosplenial cortex

Cited by 21 publications

References 115 publications

Anterior thalamic nuclei: A critical substrate for non‐spatial paired‐associate memory in rats

Anterior thalamic nuclei: A critical substrate for non‐spatial paired‐associate memory in rats

Collateral rostral thalamic projections to prelimbic, infralimbic, anterior cingulate and retrosplenial cortices in the rat brain

Anterior thalamic circuits crucial for working memory

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