A Probabilistic Framework for Region-Specific Remodeling of Dendrites in Three-Dimensional Neuronal Reconstructions

2005 ◽  
Vol 17 (1) ◽  
pp. 75-96 ◽  
Author(s):  
Rishikesh Narayanan ◽  
Anusha Narayan ◽  
Sumantra Chattarji
Keyword(s):  
Morphological Changes ◽  
Three Dimensional ◽  
Dendritic Tree ◽  
Pyramidal Cells ◽  
Dendritic Arborization ◽  
Biological Data ◽  
Hippocampal Ca3 ◽  
Ca3 Pyramidal Cells ◽  
Dendritic Atrophy ◽  
Neuron Function

Dendritic arborization is an important determinant of single-neuron function as well as the circuitry among neurons. Dendritic trees undergo remodeling during development, aging, and many pathological conditions, with many of the morphological changes being confined to certain regions of the dendritic tree. In order to analyze the functional consequences of such region-specific dendritic remodeling, it is essential to develop techniques that can systematically manipulate three-dimensional reconstructions of neurons. Hence, in this study, we develop an algorithm that uses statistics from precise morphometric analyses to systematically remodel neuronal reconstructions. We use the distribution function of the ratio of two normal distributed random variables to specify the probabilities of remodeling along various regions of the dendritic arborization. We then use these probabilities to drive an iterative algorithm for manipulating the dendritic tree in a region-specific manner. As a test, we apply this framework to a well-characterized example of dendritic remodeling: stress-induced dendritic atrophy in hippocampal CA3 pyramidal cells. We show that our pruning algorithm is capable of eliciting atrophy that matches biological data from rodent models of chronic stress.

scholarly journals Computational Analysis of the Impact of Chronic Stress on Intrinsic and Synaptic Excitability in the Hippocampus

2010 ◽  
Vol 103 (6) ◽  
pp. 3070-3083 ◽  
Author(s):  
Rishikesh Narayanan ◽  
Sumantra Chattarji
Keyword(s):  
Chronic Stress ◽  
Pyramidal Neurons ◽  
Three Dimensional ◽  
Input Resistance ◽  
Synaptic Potentiation ◽  
Synaptic Inputs ◽  
Hippocampal Ca3 ◽  
Ca3 Pyramidal Neurons ◽  
Dendritic Atrophy ◽  
The Impact

Dendritic atrophy and impaired long-term synaptic potentiation (LTP) are hallmarks of chronic stress-induced plasticity in the hippocampus. It has been hypothesized that these disparate structural and physiological correlates of stress lead to hippocampal dysfunction by reducing postsynaptic dendritic surface, thereby adversely affecting the availability of synaptic inputs and suppressing LTP. Here we examine the validity of this framework using biophysical models of hippocampal CA3 pyramidal neurons. To statistically match with the experimentally observed region specificity of stress-induced atrophy, we use an algorithm to systematically prune three-dimensional reconstructions of CA3 pyramidal neurons. Using this algorithm, we build a biophysically realistic computational model to analyze the effects of stress on intrinsic and synaptic excitability. We find that stress-induced atrophy of CA3 dendrites leads to an increase in input resistance, which depends exponentially on the percentage of neuronal atrophy. This increase translates directly into higher spiking frequencies in response to both somatic current injections and synaptic inputs at various locations along the dendritic arbor. Remarkably, we also find that the dendritic regions that manifest atrophy-induced synaptic hyperexcitability are governed by the region specificity of the underlying dendritic atrophy. Coupled with experimentally observed modulation of N-methyl-d-aspartate receptor currents, such hyperexcitability could tilt the balance of plasticity mechanisms in favor of synaptic potentiation over depression. Thus paradoxically, our results suggest that stress may impair hippocampal learning and memory, not by directly inhibiting LTP, but because of stress-induced facilitation of intrinsic and synaptic excitability and the consequent imbalance in bidirectional synaptic plasticity.

scholarly journals Dendritic branch-constrained NMDA spikes drive synaptic plasticity in hippocampal CA3 pyramidal cells

Neuroscience ◽  
2021 ◽  
Author(s):  
Federico Brandalise ◽  
Stefano Carta ◽  
Roberta Leone ◽  
Fritjof Helmchen ◽  
Anthony Holtmaat ◽  
...  
Keyword(s):  
Synaptic Plasticity ◽  
Pyramidal Cells ◽  
Dendritic Branch ◽  
Hippocampal Ca3 ◽  
Ca3 Pyramidal Cells

scholarly journals Separable actions of acetylcholine and noradrenaline on neuronal ensemble formation in hippocampal CA3 circuits

2021 ◽  
Vol 17 (10) ◽  
pp. e1009435
Author(s):  
Luke Y. Prince ◽  
Travis Bacon ◽  
Rachel Humphries ◽  
Krasimira Tsaneva-Atanasova ◽  
Claudia Clopath ◽  
...  
Keyword(s):  
Granule Cells ◽  
Mossy Fiber ◽  
Pyramidal Cells ◽  
Recurrent Network ◽  
Memory Storage ◽  
Neuronal Ensembles ◽  
Hippocampal Ca3 ◽  
Ca3 Pyramidal Cells ◽  
Episodic Memories ◽  
Mossy Fiber Pathway

In the hippocampus, episodic memories are thought to be encoded by the formation of ensembles of synaptically coupled CA3 pyramidal cells driven by sparse but powerful mossy fiber inputs from dentate gyrus granule cells. The neuromodulators acetylcholine and noradrenaline are separately proposed as saliency signals that dictate memory encoding but it is not known if they represent distinct signals with separate mechanisms. Here, we show experimentally that acetylcholine, and to a lesser extent noradrenaline, suppress feed-forward inhibition and enhance Excitatory–Inhibitory ratio in the mossy fiber pathway but CA3 recurrent network properties are only altered by acetylcholine. We explore the implications of these findings on CA3 ensemble formation using a hierarchy of models. In reconstructions of CA3 pyramidal cells, mossy fiber pathway disinhibition facilitates postsynaptic dendritic depolarization known to be required for synaptic plasticity at CA3-CA3 recurrent synapses. We further show in a spiking neural network model of CA3 how acetylcholine-specific network alterations can drive rapid overlapping ensemble formation. Thus, through these distinct sets of mechanisms, acetylcholine and noradrenaline facilitate the formation of neuronal ensembles in CA3 that encode salient episodic memories in the hippocampus but acetylcholine selectively enhances the density of memory storage.

The dendritic origins of penicillin-induced epileptogenesis in CA3 hippocampal pyramidal cells

1986 ◽  
Vol 56 (6) ◽  
pp. 1718-1738 ◽  
Author(s):  
J. W. Swann ◽  
R. J. Brady ◽  
R. J. Friedman ◽  
E. J. Smith
Keyword(s):  
Cell Body ◽  
Average Distance ◽  
Hippocampal Slices ◽  
Current Source ◽  
Field Potential ◽  
Pyramidal Cells ◽  
Large Current ◽  
Hippocampal Ca3 ◽  
Ca3 Pyramidal Cells ◽  
Negative Field

Experiments were performed in order to identify the sites of epileptiform burst generation in rat hippocampal CA3 pyramidal cells. A subsequent slow field potential was studied, which is associated with afterdischarge generation. Laminar field potential and current source-density (CSD) methods were employed in hippocampal slices exposed to penicillin. Simultaneous intracellular and extracellular field recordings from the CA3 pyramidal cell body layer showed that whenever an epileptiform burst was recorded extracellularly, individual CA3 neurons underwent an intense depolarization shift. In extracellular records a slow negative field potential invariably followed epileptiform burst generation. In approximately 10% of slices, synchronous afterdischarges rode on the envelope of this negative field potential. Intracellularly a depolarizing afterpotential followed the depolarization shift and was coincident with the extracellular slow negative field potential. A one-dimensional CSD analysis performed perpendicular to the CA3 cell body layer showed that during epileptiform burst generation large current sinks occur simultaneously in the central portions of both the apical and basilar dendrites. The average distance of the peak amplitude for these sinks from the center of the cell body layer was 175 +/- 46.8 microns and 158 +/- 25.0 microns, respectively. A large current source was recorded in the cell body layer. Smaller current sources were observed in the distal portions of the dendritic layers. During the postburst slow field potential a current sink was recorded at the edge of the cell body layer in stratum oriens--a region referred to as the infrapyramidal zone. Simultaneous with the current sink recorded there, smaller sinks were often observed in the dendritic layers that appeared to be "tails" or prolongations of the currents underlying burst generation. Two-dimensional analyses of these field potentials were performed on planes parallel and perpendicular to the exposed surface of the slice. Isopotential contours showed that the direction of extracellular current is mainly orthogonal to the CA3 laminae. Correction of CSD estimates made perpendicular to the cell body layer for current flowing in the other direction did not alter the location of computed current sources and sinks. In order to show that the dendritic currents associated with epileptiform burst generation were active sinks, tetrodotoxin (TTX) was applied locally to the dendrites where the current sinks were recorded.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Distinct dendritic Ca2+ spike forms produce opposing input-output transformations in rat CA3 pyramidal cells

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Ádám Magó ◽  
Noémi Kis ◽  
Balázs Lükő ◽  
Judit K Makara
Keyword(s):  
Dendritic Structure ◽  
Dendritic Tree ◽  
Pyramidal Cells ◽  
Afferent Input ◽  
Male Rats ◽  
Input Output ◽  
Single Action ◽  
Two Photon ◽  
Ca3 Pyramidal Cells ◽  
Output Transformation

Proper integration of different inputs targeting the dendritic tree of CA3 pyramidal cells (CA3PCs) is critical for associative learning and recall. Dendritic Ca2+ spikes have been proposed to perform associative computations in other PC types by detecting conjunctive activation of different afferent input pathways, initiating afterdepolarization (ADP), and triggering burst firing. Implementation of such operations fundamentally depends on the actual biophysical properties of dendritic Ca2+ spikes; yet little is known about these properties in dendrites of CA3PCs. Using dendritic patch-clamp recordings and two-photon Ca2+ imaging in acute slices from male rats, we report that, unlike CA1PCs, distal apical trunk dendrites of CA3PCs exhibit distinct forms of dendritic Ca2+ spikes. Besides ADP-type global Ca2+ spikes, a majority of dendrites expresses a novel, fast Ca2+ spike type that is initiated locally without bAPs, can recruit additional Na+ currents, and is compartmentalized to the activated dendritic subtree. Occurrence of the different Ca2+ spike types correlates with dendritic structure, indicating morpho-functional heterogeneity among CA3PCs. Importantly, ADPs and dendritically initiated spikes produce opposing somatic output: bursts versus strictly single-action potentials, respectively. The uncovered variability of dendritic Ca2+ spikes may underlie heterogeneous input-output transformation and bursting properties of CA3PCs, and might specifically contribute to key associative and non-associative computations performed by the CA3 network.

Animal Models: Abnormal Calcium Current in Hippocampal CA3 Pyramidal Cells of the Spontaneously Epileptic Rat (SER)

1992 ◽  
Vol 46 (2) ◽  
pp. 526-528
Author(s):  
Masashi Sasa ◽  
Kumatoshi Ishihara ◽  
Toshihiko Momiyama ◽  
Xie Renming ◽  
Naoyuki Todo ◽  
...  
Keyword(s):  
Animal Models ◽  
Calcium Current ◽  
Pyramidal Cells ◽  
Hippocampal Ca3 ◽  
Ca3 Pyramidal Cells

Variation in electrophysiology and morphology of hippocampal CA3 pyramidal cells

1990 ◽  
Vol 514 (1) ◽  
pp. 77-83 ◽  
Author(s):  
David K. Bilkey ◽  
Philip A. Schwartzkroin
Keyword(s):  
Pyramidal Cells ◽  
Hippocampal Ca3 ◽  
Ca3 Pyramidal Cells
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