Active dendrites mediate stratified gamma‐range coincidence detection in hippocampal model neurons

Das, Anindita; Narayanan, Rishikesh

doi:10.1113/jp270688

Cited by 29 publications

(95 citation statements)

References 136 publications

(449 reference statements)

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“…Arguments against temporal coding have raised questions about the ability of neurons to perform millisecond‐or‐submillisecond coincidence detection that is essential for decoding a temporal code, about the relevance of precise timing in the face of noise and variability in neuronal responses to identical stimuli and about the ability of neuronal networks to reliably propagate synchronous firing (London et al, ; Panzeri et al, ; Shadlen & Newsome, ; Shadlen & Newsome, ). Counterarguments have relied on the demonstration of millisecond‐or‐submillisecond coincidence detection in active dendritic structures, on the dependence of synchrony propagation on neuronal intrinsic properties and input structure and on the existence of temporally precise cell assemblies that could mitigate the overall background noise in decoding the precise timing of inputs (Buzsaki, ; Buzsaki et al, ; Das & Narayanan, ; Das & Narayanan, ; Diesmann, Gewaltig, & Aertsen, ; Engel et al, ; Engel & Singer, ; Fries et al, ; Golding & Oertel, ; Hong, Ratte, Prescott, & De Schutter, ; Pastalkova, Itskov, Amarasingham, & Buzsaki, ; Reyes, ; Singer et al, ; Softky, ).…”

Section: Degeneracy At Multiple Scales In the Hippocampusmentioning

confidence: 99%

“…In addition, employing electrophysiological recordings and computational models to assess subthreshold resonance and spike triggered average (STA) of model neurons, it has been shown that hippocampal pyramidal neurons are selective to different input features (including spectral features and temporal coincidence of inputs) depending on the dendritic location of their inputs. This location‐dependent feature encoding is mediated by ion channel expression profiles, and could be achieved through disparate combinations of different ion channel expression profiles (Das & Narayanan, ; Das & Narayanan, ; Das & Narayanan, ; Das et al, ; Narayanan & Johnston, ; Narayanan & Johnston, ; Rathour et al, ; Rathour & Narayanan, ; Rathour & Narayanan, ). Given the well‐established strong relationship between STA and types of coding (Ratte, Hong, De Schutter, & Prescott, ), this location‐dependent scenario argues for location‐dependent forms of coding.…”

Section: Degeneracy At Multiple Scales In the Hippocampusmentioning

confidence: 99%

“…Thus, even from the perspective of encoding strategies within a single neuron, the arguments that pitch rate coding against temporal coding are oversimplifying the complexity of neural encoding and decoding. Instead, there are broad lines of evidence pointing to a hybrid rate/temporal coding system that encompasses degeneracy by achieving encoding goals through disparate combinations of several cellular and network components in a manner that is strongly dependent on several spatiotemporal aspects of neuronal and behavioral state (Das & Narayanan, ; Das & Narayanan, ; Das et al, ; Diesmann et al, ; Lee & Dan, ; Marder, ; Marder & Thirumalai, ; Ratte et al, ).…”

Section: Degeneracy At Multiple Scales In the Hippocampusmentioning

confidence: 99%

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Degeneracy in hippocampal physiology and plasticity

2019

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Degeneracy, defined as the ability of structurally disparate elements to perform analogous function, has largely been assessed from the perspective of maintaining robustness of physiology or plasticity. How does the framework of degeneracy assimilate into an encoding system where the ability to change is an essential ingredient for storing new incoming information? Could degeneracy maintain the balance between the apparently contradictory goals of the need to change for encoding and the need to resist change towards maintaining homeostasis? In this review, we explore these fundamental questions with the mammalian hippocampus as an example encoding system. We systematically catalog lines of evidence, spanning multiple scales of analysis that point to the expression of degeneracy in hippocampal physiology and plasticity. We assess the potential of degeneracy as a framework to achieve the conjoint goals of encoding and homeostasis without cross‐interferences. We postulate that biological complexity, involving interactions among the numerous parameters spanning different scales of analysis, could establish disparate routes towards accomplishing these conjoint goals. These disparate routes then provide several degrees of freedom to the encoding‐homeostasis system in accomplishing its tasks in an input‐ and state‐dependent manner. Finally, the expression of degeneracy spanning multiple scales offers an ideal reconciliation to several outstanding controversies, through the recognition that the seemingly contradictory disparate observations are merely alternate routes that the system might recruit towards accomplishment of its goals.

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Section: Degeneracy At Multiple Scales In the Hippocampusmentioning

confidence: 99%

Section: Degeneracy At Multiple Scales In the Hippocampusmentioning

confidence: 99%

Section: Degeneracy At Multiple Scales In the Hippocampusmentioning

confidence: 99%

See 1 more Smart Citation

Degeneracy in hippocampal physiology and plasticity

2019

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“…16, 2017; relationship between STA and types of coding (Ratte et al, 2013), this location-dependent scenario argues for location-dependent forms of coding. Specifically, the soma and proximal dendrites showing class I STA (integrator) and the distal dendrites manifesting class II STA (coincidence detector) as a consequence of the differential expression of different channels (Das and Narayanan, 2015). Therefore, it seems reasonable to postulate that the proximal and distal regions are respectively geared towards rate and temporal coding, with this location-dependent differential coding strategy extending to cortical and hippocampal neurons Hausser, 2010, 2011;Das and Narayanan, 2015).…”

Section: Degeneracy In Neural Codingmentioning

confidence: 99%

“…Specifically, the soma and proximal dendrites showing class I STA (integrator) and the distal dendrites manifesting class II STA (coincidence detector) as a consequence of the differential expression of different channels (Das and Narayanan, 2015). Therefore, it seems reasonable to postulate that the proximal and distal regions are respectively geared towards rate and temporal coding, with this location-dependent differential coding strategy extending to cortical and hippocampal neurons Hausser, 2010, 2011;Das and Narayanan, 2015). Finally, behaviorally-driven neuromodulatory inputs and activity-dependent plasticity could significantly alter the operating mode and the class of excitability of compartments of a single neuron, and the type of coding employed by a neuron is dependent not just on its operating mode but also the specific characteristics of the input.…”

Section: Degeneracy In Neural Codingmentioning

confidence: 99%

Degeneracy in hippocampal physiology and plasticity

Rathour

Narayanan

2017

Preprint

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Degeneracy, defined as the ability of structurally disparate elements to perform analogous function, has largely been assessed from the perspective of maintaining robustness of physiology or plasticity. How does the framework of degeneracy assimilate into an encoding system where the ability to change is an essential ingredient for storing new incoming information? Could degeneracy maintain the balance between the apparently contradictory goals of the need to change for encoding and the need to resist change towards maintaining homeostasis? In this review, we explore these fundamental questions with the mammalian hippocampus as an example encoding system. We systematically catalog lines of evidence, spanning multiple scales of analysis, that demonstrate the expression of degeneracy in hippocampal physiology and plasticity. We assess the potential of degeneracy as a framework to achieve encoding and homeostasis without cross-interferences, and postulate that multiscale parametric and interactional complexity could establish disparate routes towards accomplishing these conjoint goals. These disparate routes then provide several degrees of freedom to the encodinghomeostasis system in accomplishing its tasks in an input-and state-dependent manner. Finally, the expression of degeneracy spanning multiple scales offers an ideal reconciliation to several outstanding controversies, through the recognition that the seemingly contradictory disparate observations are merely alternate routes that the system might recruit towards accomplishment of its goals. Juxtaposed against the ubiquitous prevalence of degeneracy and its strong links to evolution, it is perhaps apt to add a corollary to Theodosius Dobzhansky's famous quote and state "nothing in physiology makes sense except in the light of degeneracy".peer-reviewed)

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Degeneracy in the nervous system: from neuronal excitability to neural coding

Kamaleddin

2021

BioEssays

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Degeneracy is ubiquitous across biological systems where structurally different elements can yield a similar outcome. Degeneracy is of particular interest in neuroscience too. On the one hand, degeneracy confers robustness to the nervous system and facilitates evolvability: Different elements provide a backup plan for the system in response to any perturbation or disturbance. On the other, a difficulty in the treatment of some neurological disorders such as chronic pain is explained in light of different elements all of which contribute to the pathological behavior of the system. Under these circumstances, targeting a specific element is ineffective because other elements can compensate for this modulation. Understanding degeneracy in the physiological context explains its beneficial role in the robustness of neural circuits. Likewise, understanding degeneracy in the pathological context opens new avenues of discovery to find more effective therapies.

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Active dendrites mediate stratified gamma‐range coincidence detection in hippocampal model neurons

Cited by 29 publications

References 136 publications

Degeneracy in hippocampal physiology and plasticity

Degeneracy in hippocampal physiology and plasticity

Degeneracy in hippocampal physiology and plasticity

Degeneracy in the nervous system: from neuronal excitability to neural coding

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