Divergence in Population Coding for Space between Dorsal and Ventral CA1

Chockanathan, Udaysankar; Padmanabhan, Krishnan

doi:10.1523/eneuro.0211-21.2021

Cited by 14 publications

(16 citation statements)

References 101 publications

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“…Mice were head-fixed and placed on a non-motorized run-wheel. An image of a 1.9m virtual one-dimensional track was projected onto a curved screen in front of the mouse (Figure 1a, b), such that the movement of the wheel caused a corresponding change in the virtual track position (Chockanathan and Padmanabhan, 2021; Gauthier and Tank, 2018). When the mouse reached the end of the track, a sweetened milk reward was provided and the mouse was returned to the start of the track.…”

Section: Resultsmentioning

confidence: 99%

“…As with metrics like firing rate, mean changes in pairwise correlations and functional connectivity represent the complex architecture of networks as a single value, which can often obscure critical aspects of network topology necessary to understand function. Inspired by studies from functional magnetic resonance imaging (fMRI) (Bullmore and Sporns, 2009; Chockanathan et al, 2019; Farahani et al, 2019) and previous work using graph theoretical approaches to study functional interactions across neuronal populations in CA1 (Chockanathan and Padmanabhan, 2021), we built on our correlation result by studying the topology of the functional connectivity we observed in our recordings. To do this, we constructed network graphs of the populations (Newman, 2003), in which nodes denoted neurons and edges denoted a pairwise correlation greater than 0.01 (Figure 4d).…”

Section: Resultsmentioning

confidence: 99%

“…When this was done for all the units in a given animal, a matrix of binned activity was generated. A single column of this matrix thus represented the activity of all the neurons of the population within a 10ms window, which we refer to as a pattern (Chockanathan and Padmanabhan, 2021; de Ruyter van Steveninck et al, 1997; Schneidman et al, 2006). In a population of 10 units, there would thus be 2 10 = 1024 possible binary patterns.…”

Section: Methodsmentioning

confidence: 99%

“…Mice were not used for any previous experiments or procedures. Virtual reality setup A one-dimensional virtual track was generated using the Virtual Reality MATLAB (VirMEn) toolbox based on previously published designs (Chockanathan and Padmanabhan, 2021;Gauthier and Tank, 2018;Meshulam et al, 2017). The virtual track was projected onto a curved board, which occupied 180 o of the visual field of the mouse.…”

Section: Micementioning

confidence: 99%

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Differential disruptions in population coding along the dorsal-ventral axis of CA1 in the APP/PS1 mouse model of Aβ pathology

Chockanathan

Padmanabhan

2022

Preprint

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Alzheimer's Disease (AD) is a progressive neurodegenerative disorder characterized by a range of behavioral alterations including memory loss as well as cognitive and psychiatric symptoms. While there is growing evidence that cellular and molecular pathologies, such as the accumulation of amyloid beta plaques may contribute to AD, it remains unclear how this histopathology can give rise to such disparate behavioral deficits. One hypothesis for these diverse behavioral presentations is that amyloid beta plaques; accumulation has differential effects on neuronal circuits across brain regions, depending on the diverse neurophysiological properties and connections within and between the neurons in these different areas. To test this, we recorded from large neuronal populations in the dorsal and ventral CA1 regions of the hippocampus, areas that are known to be structurally and functionally diverse, in both APP/PS1 animals, a mouse model of Amyloid pathology, and age-matched C57BL/6 controls. Although we found similar levels of Amyloid pathology in the two subregions, populations of neurons in dorsal and ventral CA1 in APP/PS1 mice showed distinct signatures of disrupted neuronal activity as animals navigated a virtual reality environment. In dorsal CA1, pairwise correlations and entropy, a measure of the diversity of activity patterns, were decreased in the APP/PS1 mice. However, in ventral CA1, the opposite findings were observed; pair-wise correlations and entropy was increased in APP/PS1 mice relative to C57BL/6 controls. When we attempted to connect the microscopic features of population activity (the correlations) with the macroscopic features of the population code (the entropy) using a pairwise Ising model, we found that the models' performance decreased in predicting dorsal CA1 activity but increased in predicting vCA1 activity in APP/PS1 mice, as compared to the C57BL/6 animals. Taken together, these findings suggest that amyloid beta pathology exerts distinct effects across different hippocampal regions. Our results suggest that the diverse behavioral deficits associated with AD and the cellular pathology that arises from amyloid accumulation may be mechanistically linked by studying the dynamics of neural activity within these diverse hippocampal circuits.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Micementioning

confidence: 99%

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Differential disruptions in population coding along the dorsal-ventral axis of CA1 in the APP/PS1 mouse model of Aβ pathology

Chockanathan

Padmanabhan

2022

Preprint

Self Cite

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“…In contrast to a prior report on FSR neurons in ventral CA1 that project to the basolateral amygdala (Jimenez et al, 2020), we did not observe recruitment of FSR neurons into training context-associated ensembles in CA1 during recent recall. This differential contribution of dorsal and ventral hippocampal FSR neurons to context-associated ensembles may reflect output connectivity (basolateral amygdala vs. other downstream circuits) and distinct roles of dorsal and ventral hippocampus in encoding spatial and non-spatial information (Chockanathan & Padmanabhan, 2021;Fanselow & Dong, 2010;Strange et al, 2014). It is thought that the DG -CA3 -CA1 -ACC network undergoes changes in synaptic weights following learning that likely result in inter-regional ensembles.…”

Section: Discussionmentioning

confidence: 99%

A dentate gyrus-CA3 inhibitory circuit promotes evolution of hippocampal-cortical ensembles during memory consolidation

Twarkowski

Steininger

Kim

et al. 2022

eLife

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Memories encoded in the dentate gyrus (DG) - CA3 circuit of the hippocampus are routed from CA1 to anterior cingulate cortex (ACC) for consolidation. Although CA1 parvalbumin inhibitory neurons (PV INs) orchestrate hippocampal-cortical communication, we know less about CA3 PV INs or DG - CA3 principal neuron - IN circuit mechanisms that contribute to evolution of hippocampal-cortical ensembles during memory consolidation. Using viral genetics to selectively mimic and boost an endogenous learning-dependent circuit mechanism, DG cell recruitment of CA3 PV INs and feed-forward inhibition (FFI) in CA3, in combination with longitudinal in vivo calcium imaging, we demonstrate that FFI facilitates formation and maintenance of context-associated neuronal ensembles in CA1. Increasing FFI in DG - CA3 promoted context specificity of neuronal ensembles in ACC over time and enhanced long-term contextual fear memory. In vivo LFP recordings in mice with increased FFI in DG - CA3 identified enhanced CA1 sharp-wave ripple - ACC spindle coupling as a potential network mechanism facilitating memory consolidation. Our findings illuminate how FFI in DG - CA3 dictates evolution of ensemble properties in CA1 and ACC during memory consolidation and suggest a teacher-like function for hippocampal CA1 in stabilization and re-organization of cortical representations.

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Astrocytes contribute to the functional differentiation of the hippocampal longitudinal axis during reward and aversion processing in the adult male rat

Rezagholizadeh,

Shojaei,

Hosseinmardi

et al. 2024

Neuroscience

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Divergence in Population Coding for Space between Dorsal and Ventral CA1

Abstract: Visual Abstract

Cited by 14 publications

References 101 publications

Differential disruptions in population coding along the dorsal-ventral axis of CA1 in the APP/PS1 mouse model of Aβ pathology

Differential disruptions in population coding along the dorsal-ventral axis of CA1 in the APP/PS1 mouse model of Aβ pathology

A dentate gyrus-CA3 inhibitory circuit promotes evolution of hippocampal-cortical ensembles during memory consolidation

Astrocytes contribute to the functional differentiation of the hippocampal longitudinal axis during reward and aversion processing in the adult male rat

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