scholarly journals Spatially dispersed synapses yield sharply-tuned place cell responses through dendritic spike initiation

2018 ◽  
Vol 596 (17) ◽  
pp. 4173-4205 ◽  
Author(s):  
Reshma Basak ◽  
Rishikesh Narayanan
Keyword(s):  
Place Cell ◽  
Cell Responses ◽  
Dendritic Spike ◽  
Spike Initiation

Multiple Modes of Action Potential Initiation and Propagation in Mitral Cell Primary Dendrite

2002 ◽  
Vol 88 (5) ◽  
pp. 2755-2764 ◽  
Author(s):  
Wei R. Chen ◽  
Gongyu Y. Shen ◽  
Gordon M. Shepherd ◽  
Michael L. Hines ◽  
Jens Midtgaard
Keyword(s):  
Action Potential ◽  
Primary Dendrite ◽  
Back Propagation ◽  
Olfactory Nerve ◽  
Mitral Cell ◽  
Initiation Site ◽  
Initiation And Propagation ◽  
Action Potential Initiation ◽  
Dendritic Spike ◽  
Spike Initiation

The mitral cell primary dendrite plays an important role in transmitting distal olfactory nerve input from olfactory glomerulus to the soma-axon initial segment. To understand how dendritic active properties are involved in this transmission, we have combined dual soma and dendritic patch recordings with computational modeling to analyze action-potential initiation and propagation in the primary dendrite. In response to depolarizing current injection or distal olfactory nerve input, fast Na+ action potentials were recorded along the entire length of the primary dendritic trunk. With weak-to-moderate olfactory nerve input, an action potential was initiated near the soma and then back-propagated into the primary dendrite. As olfactory nerve input increased, the initiation site suddenly shifted to the distal primary dendrite. Multi-compartmental modeling indicated that this abrupt shift of the spike-initiation site reflected an independent thresholding mechanism in the distal dendrite. When strong olfactory nerve excitation was paired with strong inhibition to the mitral cell basal secondary dendrites, a small fast prepotential was recorded at the soma, which indicated that an action potential was initiated in the distal primary dendrite but failed to propagate to the soma. As the inhibition became weaker, a “double-spike” was often observed at the dendritic recording site, corresponding to a single action potential at the soma. Simulation demonstrated that, in the course of forward propagation of the first dendritic spike, the action potential suddenly jumps from the middle of the dendrite to the axonal spike-initiation site, leaving the proximal part of primary dendrite unexcited by this initial dendritic spike. As Na+conductances in the proximal dendrite are not activated, they become available to support the back-propagation of the evoked somatic action potential to produce the second dendritic spike. In summary, the balance of spatially distributed excitatory and inhibitory inputs can dynamically switch the mitral cell firing among four different modes: axo-somatic initiation with back-propagation, dendritic initiation either with no forward propagation, forward propagation alone, or forward propagation followed by back-propagation.

scholarly journals Dendro-dendritic cholinergic excitation controls dendritic spike initiation in retinal ganglion cells

2017 ◽  
Vol 8 (1) ◽  
Author(s):  
A. Brombas ◽  
S. Kalita-de Croft ◽  
E. J. Cooper-Williams ◽  
S. R. Williams
Keyword(s):  
Retinal Ganglion Cells ◽  
Ganglion Cells ◽  
Retinal Ganglion ◽  
Dendritic Spike ◽  
Spike Initiation

scholarly journals Experience-Related Changes in Place Cell Responses to New Sensory Configuration That Does Not Occur in the Natural Environment in the Rat Hippocampus

2017 ◽  
Vol 8 ◽  
Author(s):  
Dan Zou ◽  
Hiroshi Nishimaru ◽  
Jumpei Matsumoto ◽  
Yusaku Takamura ◽  
Taketoshi Ono ◽  
...  
Keyword(s):  
Natural Environment ◽  
Place Cell ◽  
Rat Hippocampus ◽  
Cell Responses

Optical detection of dendritic spike initiation in hippocampal CA1 pyramidal neurons

Neuroscience ◽  
2003 ◽  
Vol 118 (4) ◽  
pp. 899-907 ◽  
Author(s):  
A Kasuga ◽  
R Enoki ◽  
Y Hashimoto ◽  
H Akiyama ◽  
Y Kawamura ◽  
...  
Keyword(s):  
Pyramidal Neurons ◽  
Optical Detection ◽  
Ca1 Pyramidal Neurons ◽  
Hippocampal Ca1 ◽  
Dendritic Spike ◽  
Spike Initiation

scholarly journals Spatially dispersed synapses yield sharply-tuned place cell responses through dendritic spike initiation

2017 ◽  
Author(s):  
Reshma Basak ◽  
Rishikesh Narayanan
Keyword(s):  
Critical Role ◽  
Place Cell ◽  
Place Field ◽  
Apparent Contradiction ◽  
Cell Responses ◽  
Sharp Feature ◽  
Dendritic Spikes ◽  
Feature Selectivity ◽  
Contradictory Evidence ◽  
Strong Candidate

The literature offers evidence for a critical role of spatially-clustered iso-feature synapses in eliciting dendritic spikes essential for sharp feature selectivity, with apparently contradictory evidence demonstrating spatial dispersion of iso-feature synapses. Here, we reconcile this apparent contradiction by demonstrating that the generation of dendritic spikes, the emergence of an excitatory ramp in somatic voltage responses and sharp tuning of place-cell responses are all attainable even when iso-feature synapses are randomly dispersed across the dendritic arbor. We found this tuning sharpness to be critically reliant on dendritic sodium and transient potassium channels and on N-methyl-D-aspartate receptors. Importantly, we demonstrate that synaptic potentiation targeted to afferents from one specific place field is sufficient to effectuate place-field selectivity even when intrinsically disparate neurons received randomly dispersed afferents from multiple place-field locations. These conclusions proffer dispersed localization of iso-feature synapses as a strong candidate for achieving sharp feature selectivity in neurons across sensory-perceptual systems.

scholarly journals Robust emergence of sharply tuned place cell responses in hippocampal neurons with structural and biophysical heterogeneities

2019 ◽  
Author(s):  
Reshma Basak ◽  
Rishikesh Narayanan
Keyword(s):  
Hippocampal Neurons ◽  
Degrees Of Freedom ◽  
Pyramidal Neurons ◽  
Place Field ◽  
Synaptic Localization ◽  
Sharp Feature ◽  
Channel Expression ◽  
Dendritic Spike ◽  
Spike Initiation ◽  
The Impact

ABSTRACTHippocampal pyramidal neurons sustain propagation of fast electrical signals and are electrotonically non-compact structures exhibiting cell-to-cell variability in their complex dendritic arborization. In this study, we demonstrate that sharp place-field tuning and several somato-dendritic functional maps concomitantly emerge despite the presence of geometrical heterogeneities in these neurons. We establish this employing an unbiased stochastic search strategy involving thousands of models that spanned several morphologies and distinct profiles of dispersed synaptic localization and channel expression. Mechanistically, employing virtual knockout models, we explored the impact of bidirectional modulation in dendritic spike prevalence on place-field tuning sharpness. Consistent with prior literature, we found that across all morphologies, virtual knockout of either dendritic fast sodium channels or N-methyl-D-aspartate receptors led to a reduction in dendritic spike prevalence, whereas A-type potassium channel knockouts resulted in a nonspecific increase in dendritic spike prevalence. However, place-field tuning sharpness was critically impaired in all three sets of virtual knockout models, demonstrating that sharpness in feature tuning is maintained by an intricate balance between mechanisms that promote and those that prevent dendritic spike initiation. From the functional standpoint of the emergence of sharp feature tuning and intrinsic functional maps, within this framework, geometric variability was compensated by a combination of synaptic democracy, the ability of randomly dispersed synapses to yield sharp tuning through dendritic spike initiation, and ion-channel degeneracy. Our results suggest electrotonically non-compact neurons to be endowed with several degrees of freedom, encompassing channel expression, synaptic localization and morphological micro-structure, in achieving sharp feature encoding and excitability homeostasis.

Hyperpolarization-Activated Current Ih Disconnects Somatic and Dendritic Spike Initiation Zones in Layer V Pyramidal Neurons

2003 ◽  
Vol 90 (4) ◽  
pp. 2428-2437 ◽  
Author(s):  
Thomas Berger ◽  
Walter Senn ◽  
Hans-R. Lüscher
Keyword(s):  
Somatosensory Cortex ◽  
Action Potentials ◽  
Pyramidal Cells ◽  
Apical Dendrite ◽  
Distal Dendrite ◽  
Dendritic Spike ◽  
Hyperpolarization Activated Current ◽  
Layer V ◽  
Spike Initiation ◽  
Calcium Action Potentials

Layer V pyramidal cells of the somatosensory cortex operate with two spike initiation zones. Subthreshold depolarizations are strongly attenuated along the apical dendrite linking the somatic and distal dendritic spike initiation zones. Sodium action potentials, on the other hand, are actively back-propagating from the axon hillock into the apical tuft. There they can interact with local excitatory input leading to the generation of calcium action potentials. We investigated if and how back-propagating sodium action potentials alone, without concomitant excitatory dendritic input, can initiate calcium action potentials in the distal dendrite. In acute slices of the rat somatosensory cortex, layer V pyramidal cells were studied under current-clamp with simultaneous recordings from the soma and the apical dendrite. A train of four somatic action potentials had to reach high frequencies to induce calcium action potentials in the dendrite (“critical frequency,” CF ∼100 Hz). Depolarization in the dendrite reduced the CF, while hyperpolarization increased it. The CF depended on the presence of the hyperpolarization-activated current Ih: blockade with 20 μM 4-( N-ethyl- N-phenylamino)-1,2-dimethyl-6-(methylamino) pyridinium chloride (ZD7288) reduced the CF to 68% of control. If the neurons were stimulated with noisy current injections, leading to in-vivo-like irregular spiking, no calcium action potentials were induced in the dendrite. However, after Ih channel blockade, calcium action potentials were frequently seen. These data suggest that Ih prevents initiation of the dendritic calcium action potential by proximal input alone. Dendritic calcium action potentials may therefore represent a unique signature for coincident somatic and dendritic activation.

Hippocampal place cell responses to distal and proximal cue manipulations in dopamine D2 receptor-knockout mice

2014 ◽  
Vol 1567 ◽  
pp. 13-27 ◽  
Author(s):  
Chien Le Nguyen ◽  
Anh Hai Tran ◽  
Jumpei Matsumoto ◽  
Etsuro Hori ◽  
Teruko Uwano ◽  
...  
Keyword(s):  
Knockout Mice ◽  
Dopamine D2 Receptor ◽  
D2 Receptor ◽  
Place Cell ◽  
Cell Responses ◽  
Dopamine D2 ◽  
Hippocampal Place Cell
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