Spatial Coding in the Subiculum Requires Anterior Thalamic Inputs

Frost, Bethany E.; Cafalchio, Matheus; Martin, Sean; Islam, Nurul; Aggleton, John P.; O’Mara, Shane M.

doi:10.2139/ssrn.3545958

Cited by 3 publications

(6 citation statements)

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“…The excluded rat had a satisfactory lesion in one hemisphere only (47.9 % total, 75% left, 20% right). NeuN count throughout the ATN of intact rats was similar to that reported by Frost et al (2020); ATN lesion rats showed substantially fewer neuronal cells (Figure 2 d ). Overall, there was relatively little damage to the mediodorsal thalamus (MD) and reuniens/rhomboid (Re/Rh) nuclei.…”

Section: Resultssupporting

confidence: 85%

“…The excluded rat had a satisfactory lesion in one hemisphere only (48% total, 75% left, and 20% right). Figure 2d shows that the NeuN counts for ATN neurons in the ATN-lesion rats (M = 3388, SD = 2024) were all well below the values found in the sham-lesion rats (M = 15339, SD = 1065; this count was similar to that reported by Frost et al 2020). Eight of the 17 lesion rats (4 in the Trace group and 4 in the No-Trace group) had no damage to either the mediodorsal thalamus (MD) or reuniens/rhomboid (Re/Rh) nuclei and there was relatively little damage to these structures in the remaining 9 rats with lesions.…”

Section: Lesion Verificationsupporting

confidence: 79%

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

Hamilton

Dalrymple‐Alford

2021

Preprint

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The anterior thalamic nuclei (ATN), a central node in a complex memory system, process spatial and temporal memory. Here, we show that ATN lesions do not affect acquisition of a simple odour discrimination or a simple object discrimination in a runway apparatus. The same procedures were used to test learning of an arbitrary association between non-spatial object-odour pairings (A+X or B+Y were rewarded; but not A+Y or B+X). If ATN lesions recapitulate hippocampal function, specifically CA1 function, then they should disrupt acquisition only when an explicit delay (i.e., a 10-second trace) is inserted between the odour and object. Acquisition was completely abolished by ATN lesions, irrespective of the presence of the temporal trace, and despite extensive training (50x12-trial sessions). Faster acquisition with the 10-second trace was found in the sham-lesion rats. During recall, 5 days after criterion, sham rats but not ATN-lesion rats showed elevated Zif268 expression in hippocampal CA1 for the trace compared to no-trace condition; both sham and lesion rats tested in the trace condition showed increased IEG expression in the superficial layers of the prefrontal cortex and retrosplenial cortex. ATN lesions markedly reduced Zif268 expression in the prefrontal cortex and retrosplenial cortex. This is the first evidence that ATN lesions impair non-spatial paired-associate tasks. The findings suggest that the ATN influence memory beyond time and space, and constitute a critical neural structure for learning arbitrary associations even in the task version that is not disrupted by hippocampal lesions.

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Section: Resultssupporting

confidence: 85%

Section: Lesion Verificationsupporting

confidence: 79%

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

Hamilton

Dalrymple‐Alford

2021

Preprint

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“…The axis-tuned neurons previously reported from a minor sub-population of the present dataset (Olson et al, 2017) may be an extreme form of this sort of analogous representation. This may reflect association of inputs from different sub-populations of anterior thalamic neurons having opposite tuning by head orientation ((Taube, 1995; Goodridge & Taube, 1997; Peyrache et al, 2017; Viejo & Peyrache, 2019; Frost et al, 2020). Future work on environments where functionally similar spaces are not parallel may help tease apart whether the structural or functional aspects of the locations drive such responses in SUB neurons.…”

Section: Discussionmentioning

confidence: 99%

“…Recent work has shown the importance of anterior thalamic inputs into SUB in guiding choice behavior at intersections. Temporary and permanent anterior thalamic lesions led to marked behavioral deficits and degraded spatial firing in SUB while CA1 place fields remain intact (Frost et al, 2020). Further research is needed into investigating the importance of these inputs for SUB function.…”

Section: Discussionmentioning

confidence: 99%

“…The dorsal subiculum is situated within a distributed system of brain regions forming a ‘cognitive map’ that encodes an organism’s spatial relationship to its environment (Andersen et al, 1973; Hjorth-Simonsen, 1973; Amaral & Witter, 1989; Amaral et al, 1991; Witter, 2006). The few studies that have examined the impact of damage selective to subiculum (SUB) support a role for this structure in the two most prominent tests for spatial navigation, the Morris water tank and T-maze spatial alternation tasks (Morris et al, 1990; Galani et al, 1998; Frost et al, 2020). Despite this, relatively few studies have addressed the form or forms by which subiculum neurons represent spatial and orientational relationships to the environment.…”

Section: Introductionmentioning

confidence: 99%

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Complementary Maps for Location and Environmental Structure in CA1 and Subiculum

Chang

et al. 2021

Preprint

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The dorsal subiculum lies among a network of interconnected brain regions that collectively map multiple spatial and orientational relationships between an organism and the boundaries and pathways composing its environment. A unique role of the subiculum in spatial information processing has yet to be defined despite reports of small neuron subpopulations that encode relationships to specific boundaries, axes of travel, or locations. We examined the activity patterns among populations of subiculum neurons during performance of a spatial working memory task performed within a complex network of interconnected pathways. Compared to neurons in hippocampal sub-region CA1, a major source of its afferents, subiculum neurons were far more likely to exhibit multiple firing fields at locations that were analogous with respect to path structure and function. Subiculum neuron populations were also found to exhibit a greater dynamic range in scale of spatial representation and for persistent patterns of spiking activity to be aligned to transitions between maze segments. Together, the findings indicate that the subiculum plays a unique role in spatial mapping, one that complements the location-specific firing of CA1 neurons with the encoding of emergent and recurring structural features of a complex path network.

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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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Spatial Coding in the Subiculum Requires Anterior Thalamic Inputs

Cited by 3 publications

References 0 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

Complementary Maps for Location and Environmental Structure in CA1 and Subiculum

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

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