Behavioral state-dependent lateralization of dorsal dentate gyrus c-Fos expression in mice

Jordan, Jake T.; Shanley, Mary Regis; Pytte, Carolyn L.

doi:10.1042/ns20180206

Cited by 14 publications

(11 citation statements)

References 26 publications

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“…Neurons in the dentate gyrus, two synapses upstream of the CA1, have been implicated in pattern separation processes that may be necessary for contextual behaviour 43 and can do so through differences in millisecond-timescale coactivity 25 . Moreover, there is evidence for a left dominance in the expression of the activity marker cFos in the dentate gyrus during novel object exploration 44 . Importantly, while CA3 neurons in one hemisphere send commissural projections to the contralateral hemisphere 33 , the two hemispheres seem to retain functional differences in their projections to CA1 35 , 42 which we target directly.…”

Section: Discussionmentioning

confidence: 99%

An emergent neural coactivity code for dynamic memory

et al. 2021

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Neural correlates of external variables provide potential internal codes that guide an animal’s behaviour. Notably, first-order features of neural activity, such as single-neuron firing rates, have been implicated in encoding information. However, the extent to which higher-order features, such as multi-neuron coactivity, play primary roles in encoding information or secondary roles in supporting single-neuron codes remains unclear. Here we show that millisecond-timescale coactivity amongst hippocampal CA1 neurons discriminates distinct millisecond-lived behavioural contingencies. This contingency discrimination was unrelated to the tuning of individual neurons but instead an emergent property of their coactivity. Contingency discriminating patterns were reactivated offline after learning and their reinstatement predicted trial-by-trial memory performance. Moreover, optogenetic suppression of inputs from the upstream CA3 region selectively during learning impaired coactivity-based contingency information in CA1 and subsequent dynamic memory retrieval. These findings identify coactivity as a primary feature of neural firing that discriminates distinct behaviourally-relevant variables and supports memory retrieval.

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Section: Discussionmentioning

confidence: 99%

An emergent neural coactivity code for dynamic memory

et al. 2021

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“…In fact, if there is indeed a relationship between embryonic organization of organ laterality and hippocampal laterality (Goto et al, 2010;Kawakami et al, 2008), consistent organ laterality across sexes would indicate that consistent development of hippocampal laterality across sexes is likely. One study found no difference between adult males and female mice in left or right hippocampal c-Fos expression or in degree of lateralization (Jordan et al, 2019). While there is no data to suggest that hippocampal lateralization in males and females may be different, future studies will have to include females to determine whether or not an additional framework is needed (Shansky, 2019).…”

Section: Does Lateralization Differ Across Sexes?mentioning

confidence: 99%

“…These asymmetries were only recently uncovered using advanced methods. Importantly, a recent study showed that failure to consider differences between the left and right rodent hippocampi in cellular quantification experiments can lead to incomplete and inconsistent conclusions (Jordan, Shanley, & Pytte, 2019). Collectively, these findings indicate the importance of understanding the hippocampus as a bilateral structure and of taking into account differences across hemispheres.…”

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confidence: 99%

The rodent hippocampus as a bilateral structure: A review of hemispheric lateralization

Jordan

2019

Hippocampus

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The left and right rodent hippocampi exhibit striking lateralization in some of the very neural substrates considered to be critical for hippocampal cognitive function. Despite this, there is an overwhelming lack of consideration for hemispheric differences in studies of the rodent hippocampus. Asymmetries identified so far suggest that a bilateral model of the hippocampus will be essential for an understanding of this brain region, and perhaps of the brain more widely. Although hypotheses have been proposed to explain how the left and right hippocampi contribute to behavior and cognition, these hypotheses have either been refuted by more recent studies or have been limited in the scope of data they explain. Here, I will first review data on human and rodent hippocampal lateralization. The implications of these data suggest that considering the hippocampus as a bilateral structure with functional lateralization will be critical moving forward in understanding the function and mechanisms of this brain region. In exploring these implications, I will then propose a hypothesis of the hippocampus as a bilateral structure. This discrete‐continuous hypothesis proposes that the left and right hippocampi contribute to spatial memory and navigation in a complementary manner. Specifically, the left hemisphere stores spatial information as discrete, salient locations, and the right hemisphere represents space continuously, contributing to route computation and flexible spatial navigation. Consideration of hippocampal lateralization in designing future studies may provide insight into the function of the hippocampus and resolve debates concerning its function.

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“…In fact, if there is indeed a relationship between embryonic organization of organ laterality and hippocampal laterality (Kawakami et al, 2008;Goto et al, 2010), consistent organ laterality across sexes would indicate that consistent development of hippocampal laterality across sexes is likely. One study found no difference between adult males and female mice in left or right hippocampal c-Fos expression or in degree of lateralization (Jordan et al, 2019). While there is no data to suggest that hippocampal lateralization in males and females may be different, future studies will have to include females to determine whether or not an additional framework is needed (Shansky, 2019).…”

Section: Does Lateralization Differ Across Sexes? a Majority Of Rodenmentioning

confidence: 99%

“…These asymmetries were only recently uncovered using advanced methods. Importantly, a recent study showed that failure to consider differences between the left and right rodent hippocampi in cellular quantification experiments can lead to incomplete and inconsistent conclusions (Jordan et al, 2019). Collectively, these findings indicate the importance of understanding the hippocampus as a bilateral structure and of taking into account differences across hemispheres.…”

Section: Introductionmentioning

confidence: 99%

The rodent hippocampus as a bilateral structure: A review of hemispheric lateralization

Jordan

2017

Preprint

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Lateralization is an organizing principle of nervous systems across taxa. The human hippocampus is known to be lateralized with respect to memory and spatial navigation. In contrast, the rodent hippocampus has been traditionally thought of as a bilaterally symmetric structure, as early studies did not uncover functional differences between the left and right hemispheres. Moreover, it is a common view that the primate hippocampus lacks strong, interhemispheric projections between the bilateral hippocampi, which are present in the rodent brain. Advances in experimental technology have resulted in discoveries of hemispheric asymmetries in the rodent hippocampus, which have led to more sophisticated hypotheses of bilateral hippocampal function. Here, we review studies on hippocampal lateralization with a particular focus on the rodent brain, and suggest that there are more similarities between the human and rodent hippocampus than previously thought. We propose novel hypotheses to uncover the contributions of the left and right hemisphere to hippocampal processing and cognition.All rights reserved. No reuse allowed without permission.(which was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.

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Behavioral state-dependent lateralization of dorsal dentate gyrus c-Fos expression in mice

Cited by 14 publications

References 26 publications

An emergent neural coactivity code for dynamic memory

An emergent neural coactivity code for dynamic memory

The rodent hippocampus as a bilateral structure: A review of hemispheric lateralization

The rodent hippocampus as a bilateral structure: A review of hemispheric lateralization

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