Nonlinear dendritic processing determines angular tuning of barrel cortex neurons in vivo

Lavzin, Maria; Rapoport, S. Sh.; Polsky, Alon; Garion, Liora; Schiller, Jackie

doi:10.1038/nature11451

Cited by 263 publications

(301 citation statements)

References 29 publications

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“…Firstly, we predict that hyperpolarization not only broadens somatic tuning (Jia et al, 2010;Lavzin et al, 2012) but it also sharpens dendritic tuning (Fig. 6).…”

Section: Discussionmentioning

confidence: 99%

Dendrites Enable a Robust Mechanism for Neuronal Stimulus Selectivity

et al. 2017

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Hearing, vision, touch -underlying all of these senses is stimulus selectivity, a robust information processing operation in which cortical neurons respond more to some stimuli than to others. Previous models assume that these neurons receive the highest weighted input from an ensemble encoding the preferred stimulus, but dendrites enable other possibilities. Non-linear dendritic processing can produce stimulus selectivity based on the spatial distribution of synapses, even if the total preferred stimulus weight does . CC-BY 4.0 International license peer-reviewed) is the author/funder. It is made available under aThe copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/023200 doi: bioRxiv preprint first posted online Jul. 24, 2015; not exceed that of non-preferred stimuli. Using a multi-subunit non-linear model, we demonstrate that stimulus selectivity can arise from the spatial distribution of synapses.We propose this as a general mechanism for information processing by neurons possessing dendritic trees. Moreover, we show that this implementation of stimulus selectivity increases the neuron's robustness to synaptic and dendritic failure. Importantly, our model can maintain stimulus selectivity for a larger range of synapses or dendrites loss than an equivalent linear model. We then use a layer 2/3 biophysical neuron model to show that our implementation is consistent with two recent experimental observations: (1) one can observe a mixture of selectivities in dendrites, that can differ from the somatic selectivity, and (2) hyperpolarization can broaden somatic tuning without affecting dendritic tuning. Our model predicts that an initially non-selective neuron can become selective when depolarized. In addition to motivating new experiments, the model's increased robustness to synapses and dendrites loss provides a starting point for fault-resistant neuromorphic chip development.

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“…Firstly, we predict that hyperpolarization not only broadens somatic tuning (Jia et al, 2010;Lavzin et al, 2012) but it also sharpens dendritic tuning (Fig. 6).…”

Section: Discussionmentioning

confidence: 99%

Dendrites Enable a Robust Mechanism for Neuronal Stimulus Selectivity

et al. 2017

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“…The analysis of the spike timing dependence of the Ca 2+ transient amplitudes showed a supralinearity when the synaptic stimulus preceded the back-propagating action potential (bAP) and a sublinearity when the order was reversed. Recently, a study combining wholecell recordings in vivo and two-photon imaging in vitro investigated the cellular mechanisms of angular tuning in L4 neurons in the mouse barrel cortex (11). The results indicated that angular tuning of somatic voltage responses involves a complex nonlinear dendritic interplay of thalamo-cortical and cortico-cortical inputs.…”

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confidence: 99%

Linear integration of spine Ca ²⁺ signals in layer 4 cortical neurons in vivo

Jia

Varga

Sakmann

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Sensory information reaches the cortex through synchronously active thalamic axons, which provide a strong drive to layer 4 (L4) cortical neurons. Because of technical limitations, the dendritic signaling processes underlying the rapid and efficient activation of L4 neurons in vivo remained unknown. Here we introduce an approach that allows the direct monitoring of single dendritic spine Ca 2+ signals in L4 spiny stellate cells of the vibrissal mouse cortex in vivo. Our results demonstrate that activation of N-methyl-D-aspartate (NMDA) receptors is required for sensory-evoked action potential (AP) generation in these neurons. By analyzing NMDA receptor-mediated Ca 2+ signaling, we identify whisker stimulationevoked large responses in a subset of dendritic spines. These sensory-stimulation-activated spines, representing predominantly thalamo-cortical input sites, were denser at proximal dendritic regions. The amplitude of sensory-evoked spine Ca 2+ signals was independent of the activity of neighboring spines, without evidence for cooperativity. Furthermore, we found that spine Ca In the mammalian brain, sensory information is transmitted to the neocortex primarily through thalamo-cortical projections. Thus, in the vibrissae-related somatosensory cortex of rodents, tactile information arrives through axons of neurons that are located in the ventro-posterio-medial thalamic nucleus (VPM). It is well established that these axons provide direct input to layer 4 (L4), where they contact the dendrites of three types of excitatory neurons, namely the spiny stellate cells, the pyramids, and the star pyramids (1). In addition, there is recent evidence that axons originating in the VPM provide a direct input also to layer 5 (L5) neurons (2). A particularly interesting cytoarchitectonical feature of L4 of the rodent vibrissal cortex is the organization in distinct structures called "barrels" (3). The dendritic arborization of each spiny stellate cell is confined within the border of a barrel and is typically asymmetric, with cell bodies located at the barrel's periphery and the dendrites facing the center (4, 5). Functionally, most spiny stellate cells and also the other L4 neurons in each barrel respond primarily to a single whisker, referred to as the principal whisker, whereas adjacent, or surround, whiskers provide a much weaker input (6). The fraction of thalamocortical inputs to each L4 neuron is remarkably small (about 10-20%) compared with that of intracortical inputs (7). Nevertheless, thalamocortical inputs are very efficient because of their synchronous activation by sensory stimuli (8, 9).The dendritic processes that are associated with the synaptic activation of L4 neurons were investigated initially in vitro in acute brain slices. For example, a study involving the use of whole-cell recordings in combination with two-photon imaging characterized synaptically evoked N-methyl-D-aspartate (NMDA) receptormediated Ca 2+ influx in dendritic spines (10). The analysis of the spike timing dependence of the Ca 2+ trans...

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“…synaptic integration | 2-layer model | active dendrites | NMDA spike | dendritic spike O n the path to understanding the diverse information processing functions of the brain, it is essential to develop simplified models of individual neurons. The classical view that a neuron collects excitatory and inhibitory influences from across its dendritic arbor and passively funnels them to a single spikegenerating zone near the soma has been challenged by the finding that dendrites generate local spikes (1)(2)(3)(4)(5)(6)(7)(8)(9)(10)(11)(12)(13)(14)(15) and can support a variety of compartmentalized computations (16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28). We previously showed that the input-output (i/o) behavior of a dendritic subtree, whose branches emanate from a main trunk or soma, can be described by a two-layer model (2LM), where the first layer consists of multiple independent dendritic "subunits" with stereotyped nonlinear i/o functions.…”

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confidence: 99%

Mechanisms underlying subunit independence in pyramidal neuron dendrites

Behabadi¹,

Mel

2013

Proc. Natl. Acad. Sci. U.S.A.

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Pyramidal neuron (PN) dendrites compartmentalize voltage signals and can generate local spikes, which has led to the proposal that their dendrites act as independent computational subunits within a multilayered processing scheme. However, when a PN is strongly activated, back-propagating action potentials (bAPs) sweeping outward from the soma synchronize dendritic membrane potentials many times per second. How PN dendrites maintain the independence of their voltage-dependent computations, despite these repeated voltage resets, remains unknown. Using a detailed compartmental model of a layer 5 PN, and an improved method for quantifying subunit independence that incorporates a more accurate model of dendritic integration, we first established that the output of each dendrite can be almost perfectly predicted by the intensity and spatial configuration of its own synaptic inputs, and is nearly invariant to the rate of bAP-mediated "cross-talk" from other dendrites over a 100-fold range. Then, through an analysis of conductance, voltage, and current waveforms within the model cell, we identify three biophysical mechanisms that together help make independent dendritic computation possible in a firing neuron, suggesting that a major subtype of neocortical neuron has been optimized for layered, compartmentalized processing under in-vivo-like spiking conditions.O n the path to understanding the diverse information processing functions of the brain, it is essential to develop simplified models of individual neurons. The classical view that a neuron collects excitatory and inhibitory influences from across its dendritic arbor and passively funnels them to a single spikegenerating zone near the soma has been challenged by the finding that dendrites generate local spikes (1-15) and can support a variety of compartmentalized computations (16-28). We previously showed that the input-output (i/o) behavior of a dendritic subtree, whose branches emanate from a main trunk or soma, can be described by a two-layer model (2LM), where the first layer consists of multiple independent dendritic "subunits" with stereotyped nonlinear i/o functions. In the second layer, corresponding to the soma, the dendritic outputs are summed and fed through the cell's somatic firing rate-current (f-I) curve (8,21,22,29) (Fig. 1A). The core assumption of the 2LM is that each dendrite's output depends only on its synaptic inputs, and is independent of the activity of other dendrites or the cell as a whole. The 2LM was previously tested in both experimental and modeling studies, outperforming passive dendrite (one-layer) models in predicting pyramidal neuron (PN) responses both to brief inputs leading to subthreshold somatic responses (8,29) and to high-frequency stimulation that produced output trains lasting hundreds of milliseconds (21,22). Notwithstanding the improved description of PN responses provided by two-layer models, a substantial fraction of the response variance remained unexplained by 2LM predictions in those previous studies (21, 22), leav...

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Nonlinear dendritic processing determines angular tuning of barrel cortex neurons in vivo

Cited by 263 publications

References 29 publications

Dendrites Enable a Robust Mechanism for Neuronal Stimulus Selectivity

Dendrites Enable a Robust Mechanism for Neuronal Stimulus Selectivity

Linear integration of spine Ca ²⁺ signals in layer 4 cortical neurons in vivo

Mechanisms underlying subunit independence in pyramidal neuron dendrites

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Nonlinear dendritic processing determines angular tuning of barrel cortex neurons in vivo

Cited by 263 publications

References 29 publications

Dendrites Enable a Robust Mechanism for Neuronal Stimulus Selectivity

Dendrites Enable a Robust Mechanism for Neuronal Stimulus Selectivity

Linear integration of spine Ca 2+ signals in layer 4 cortical neurons in vivo

Mechanisms underlying subunit independence in pyramidal neuron dendrites

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Linear integration of spine Ca ²⁺ signals in layer 4 cortical neurons in vivo