Amplification and linearization of distal synaptic input to cortical pyramidal cells

1994 ◽  
Vol 72 (6) ◽  
pp. 2743-2753 ◽  
Author(s):  
O. Bernander ◽  
C. Koch ◽  
R. J. Douglas
Keyword(s):  
Pyramidal Cell ◽  
Synaptic Input ◽  
Striate Cortex ◽  
Dendritic Tree ◽  
Pyramidal Cells ◽  
Synaptic Efficacy ◽  
Induced Voltage ◽  
Apical Tuft ◽  
Voltage Dependent ◽  
The Relationship

1. Computer simulations were used to study the effect of voltage-dependent calcium and potassium conductances in the apical dendritic tree of a pyramidal cell on the synaptic efficacy of apical synaptic input. The apical tuft in layers 1 and 2 is the target of feedback projections from other cortical areas. 2. The current, Isoma, flowing into the soma in response to synaptic input was used to assess synaptic efficacy. This measure takes full account of all the relevant nonlinearities in the dendrities and can be used during spiking activity. Isoma emphasizes current flowing in response to synaptic input rather than synaptically induced voltage change. This measure also permits explicit characterization of the input-output relationship of the entire neuron by computing the relationship between presynaptic input and postsynaptic output frequency. 3. Simulations were based on two models. The first was a biophysically detailed 400-compartment model of a morphologically characterized layer 5 pyramidal cell from striate cortex of an adult cat. In this model eight voltage-dependent conductances were incorporated into the somatic membrane to provide the observed firing behavior of a regular spiking cell. The second model was a highly simplified three-compartment equivalent electrical circuit. 4. If the dendritic tree is entirely passive, excitatory synaptic input of the non-N-methyl-D-aspartate (non-NMDA) type to layers 1, 2, and 3 saturate at very moderate input rates, because of the high input impedance of the apical tuft. Layers 1 and 2 together can deliver only 0.25 nA current to the soma. This modest effect is surprising in view of the important afferents that synapse on the apical tuft and is inconsistent with experimental data indicating a more powerful effect. 5. We introduced in a controlled manner a voltage-dependent potassium conductance in the apical tuft, gK, to prevent saturation of the synaptic response. This conductance was designed to linearize the relationship between presynaptic input frequency and the somatic current. We also introduced a voltage-dependent calcium conductance along the apical trunk, gCa, to amplify the apical signal, i.e., the synaptic current reaching the soma. 6. To arrive at a specific relationship between the presynaptic input rate and the somatic current delivered by the synaptic input, we derived the activation curves of gK and gCa either analytically or numerically. The resultant voltage-dependent behavior of both conductances was similar to experimentally measured activation curves.(ABSTRACT TRUNCATED AT 400 WORDS)

Synaptic Interactions in a Passive Dendritic Tree

1998 ◽  
Author(s):  
Christof Koch
Keyword(s):  
Nervous System ◽  
Dendritic Tree ◽  
Extreme Case ◽  
Pyramidal Cells ◽  
Inhibitory Synapses ◽  
Dendritic Trees ◽  
Central Processing ◽  
Voltage Dependent ◽  
Dendritic Spikes ◽  
Spatial Positioning

Nerve cells are the targets of many thousands of excitatory and inhibitory synapses. An extreme case are the Purkinje cells in the primate cerebellum, which receive between one and two hundred thousand synapses onto dendritic spines from an equal number of parallel fibers (Braitenberg and Atwood, 1958; Llinas and Walton, 1998). In fact, this structure has a crystalline-like quality to it, with each parallel fiber making exactly one synapse onto a spine of a Purkinje cell. For neocortical pyramidal cells, the total number of afferent synapses is about an order of magnitude lower (Larkman, 1991). These numbers need to be compared against the connectivity in the central processing unit (CPU) of modern computers, where the gate of a typical transistor usually receives input from one, two, or three other transistors or connects to one, two, or three other transistor gates. The large number of synapses converging onto a single cell provide the nervous system with a rich substratum for implementing a very large class of linear and nonlinear neuronal operations. As we discussed in the introductory chapter, it is only these latter ones, such as multiplication or a threshold operation, which are responsible for “computing” in the nontrivial sense of information processing. It therefore becomes crucial to study the nature of the interaction among two or more synaptic inputs located in the dendritic tree. Here, we restrict ourselves to passive dendritic trees, that is, to dendrites that do not contain voltage-dependent membrane conductances. While such an assumption seemed reasonable 20 or even 10 years ago, we now know that the dendritic trees of many, if not most, cells contain significant nonlinearities, including the ability to generate fast or slow all-or-none electrical events, so-called dendritic spikes. Indeed, truly passive dendrites may be the exception rather than the rule in the nervous In Sec. 1.5, we studied this interaction for the membrane patch model. With the addition of the dendritic tree, the nervous system has many more degrees of freedom to make use of, and the strength of the interaction depends on the relative spatial positioning, as we will see now. That this can be put to good use by the nervous system is shown by the following experimental observation and simple model.

Synaptic integration in an excitable dendritic tree

1993 ◽  
Vol 70 (3) ◽  
pp. 1086-1101 ◽  
Author(s):  
B. W. Mel
Keyword(s):  
Pyramidal Cell ◽  
Neuronal Response ◽  
Dendritic Tree ◽  
Pattern Discrimination ◽  
Synaptic Activity ◽  
Visual Neurons ◽  
Voltage Dependent ◽  
Sum Of Products ◽  
Very High ◽  
Synaptic Drive

1. Compartmental modeling experiments were carried out in an anatomically characterized neocortical pyramidal cell to study the integrative behavior of a complex dendritic tree containing active membrane mechanisms. Building on a previously presented hypothesis, this work provides further support for a novel principle of dendritic information processing that could underlie a capacity for nonlinear pattern discrimination and/or sensory processing within the dendritic trees of individual nerve cells. 2. It was previously demonstrated that when excitatory synaptic input to a pyramidal cell is dominated by voltage-dependent N-methyl-D-aspartate (NMDA)-type channels, the cell responds more strongly when synaptic drive is concentrated within several dendritic regions than when it is delivered diffusely across the dendritic arbor. This effect, called dendritic "cluster sensitivity," persisted under wide-ranging parameter variations and directly implicated the spatial ordering of afferent synaptic connections onto the dendritic tree as an important determinant of neuronal response selectivity. 3. In this work, the sensitivity of neocortical dendrites to spatially clustered synaptic drive has been further studied with fast sodium and slow calcium spiking mechanisms present in the dendritic membrane. Several spatial distributions of the dendritic spiking mechanisms were tested with and without NMDA synapses. Results of numerous simulations reveal that dendritic cluster sensitivity is a highly robust phenomenon in dendrites containing a sufficiency of excitatory membrane mechanisms and is only weakly dependent on their detailed spatial distribution, peak conductances, or kinetics. Factors that either work against or make irrelevant the dendritic cluster sensitivity effect include 1) very high-resistance spine necks, 2) very large synaptic conductances, 3) very high baseline levels of synaptic activity, and 4) large fluctuations in level of synaptic activity on short time scales. 4. The functional significance of dendritic cluster sensitivity has been previously discussed in the context of associative learning and memory. Here it is demonstrated that the dendritic tree of a cluster-sensitive neuron implements an approximative spatial correlation, or sum of products operation, such as that which could underlie nonlinear disparity tuning in binocular visual neurons.

Synaptic Input to a Passive Tree

1998 ◽  
Author(s):  
Christof Koch
Keyword(s):  
Pyramidal Cell ◽  
Synaptic Input ◽  
Stellate Cell ◽  
Dendritic Tree ◽  
Excitatory Postsynaptic Potential ◽  
Excitatory Synapses ◽  
Artificial Condition ◽  
Layer 4 ◽  
Current Steps ◽  
The One

Now that we have quantified the behavior of the cell in response to current pulses and current steps as delivered by the physiologist's microelectrode, let us study the behavior of the cell responding to a more physiological input. For instance, a visual stimulus in the environment will activate cells in the retina and its target, neurons in the lateral geniculate nucleus. These, in turn, make on the order of 50 excitatory synapses onto the apical tree of a layer 5 pyramidal cell in primary visual cortex such as the one we use throughout the book, and about 100-150 synapses onto a layer 4 spiny stellate cell (Peters and Payne, 1993; Ahmed et al., 1994, 1996; Peters, Payne, and Rudd, 1994). All of these synapses will be triggered within a fraction of a millisecond (Alonso, Usrey, and Reid, 1996). Thus, any sensory input to a neuron is likely to activate on the order of 102 synapses, rather than one or two very specific synapses as envisioned in Chap. 5 in the discussion of synaptic AND-NOT logic. This chapter will reexamine the effect of synaptic input to a realistic dendritic tree. We will commence by considering a single synaptic input as a sort of baseline condition. This represents a rather artificial condition; but because the excitatory postsynaptic potential and current at the soma are frequently experimentally recorded and provide important insights into the situation prevailing in the presence of massive synaptic input, we will discuss them in detail. Next we will treat the case of many temporally dispersed synaptic inputs to a leaky integrate-and-fire model and to the passive dendritic tree of the pyramidal cell. In particular, we are interested in uncovering the exact relationship between the temporal input jitter and the output jitter. The bulk of this chapter deals with the effect of massive synaptic input onto the firing behavior of the cell, by making use of the convenient fiction that the detailed temporal arrangement of action potentials is irrelevant for neuronal information processing. This allows us to derive an analytical expression relating the synaptic input to the somatic current and ultimately to the output frequency of the cell.

scholarly journals Balanced ionotropic receptor dynamics support signal estimation via voltage-dependent membrane noise

2016 ◽  
Vol 115 (1) ◽  
pp. 530-545 ◽  
Author(s):  
Curtis M. Marcoux ◽  
Stephen E. Clarke ◽  
William H. Nesse ◽  
Andre Longtin ◽  
Leonard Maler
Keyword(s):  
Pyramidal Cell ◽  
Pyramidal Neurons ◽  
Dynamic Balance ◽  
Significant Proportion ◽  
Low Frequency ◽  
Pyramidal Cells ◽  
Weakly Electric Fish ◽  
Ionotropic Receptor ◽  
Membrane Noise ◽  
Voltage Dependent

Encoding behaviorally relevant stimuli in a noisy background is critical for animals to survive in their natural environment. We identify core biophysical and synaptic mechanisms that permit the encoding of low-frequency signals in pyramidal neurons of the weakly electric fish Apteronotus leptorhynchus, an animal that can accurately encode even miniscule amplitude modulations of its self-generated electric field. We demonstrate that slow NMDA receptor (NMDA-R)-mediated excitatory postsynaptic potentials (EPSPs) are able to summate over many interspike intervals (ISIs) of the primary electrosensory afferents (EAs), effectively eliminating the baseline EA ISI correlations from the pyramidal cell input. Together with a dynamic balance of NMDA-R and GABA-A-R currents, this permits stimulus-evoked changes in EA spiking to be transmitted efficiently to target electrosensory lobe (ELL) pyramidal cells, for encoding low-frequency signals. Interestingly, AMPA-R activity is depressed and appears to play a negligible role in the generation of action potentials. Instead, we hypothesize that cell-intrinsic voltage-dependent membrane noise supports the encoding of perithreshold sensory input; this noise drives a significant proportion of pyramidal cell spikes. Together, these mechanisms may be sufficient for the ELL to encode signals near the threshold of behavioral detection.

scholarly journals NMDA-Based Pattern Discrimination in a Modeled Cortical Neuron

1992 ◽  
Vol 4 (4) ◽  
pp. 502-517 ◽  
Author(s):  
Bartlett W. Mel
Keyword(s):  
Pyramidal Cell ◽  
Dendritic Tree ◽  
Pattern Discrimination ◽  
Information Storage ◽  
Processing Power ◽  
Excitatory Synaptic Input ◽  
Voltage Dependent ◽  
Nmda Channels ◽  
Pattern Information

Compartmental simulations of an anatomically characterized cortical pyramidal cell were carried out to study the integrative behavior of a complex dendritic tree. Previous theoretical (Feldman and Ballard 1982; Durbin and Rumelhart 1989; Mel 1990; Mel and Koch 1990; Poggio and Girosi 1990) and compartmental modeling (Koch et al. 1983; Shepherd et al. 1985; Koch and Poggio 1987; Rall and Segev 1987; Shepherd and Brayton 1987; Shepherd et al. 1989; Brown et al. 1991) work had suggested that multiplicative interactions among groups of neighboring synapses could greatly enhance the processing power of a neuron relative to a unit with only a single global firing threshold. This issue was investigated here, with a particular focus on the role of voltage-dependent N-methyl-D-asparate (NMDA) channels in the generation of cell responses. First, it was found that when a large proportion of the excitatory synaptic input to dendritic spines is carried by NMDA channels, the pyramidal cell responds preferentially to spatially clustered, rather than random, distributions of activated synapses. Second, based on this mechanism, the NMDA-rich neuron is shown to be capable of solving a nonlinear pattern discrimination task. We propose that manipulation of the spatial ordering of afferent synaptic connections onto the dendritic arbor is a possible biological strategy for pattern information storage during learning.

Function of NMDA Receptors and Persistent Sodium Channels in a Feedback Pathway of the Electrosensory System

2001 ◽  
Vol 86 (4) ◽  
pp. 1612-1621 ◽  
Author(s):  
Neil Berman ◽  
Robert J. Dunn ◽  
Leonard Maler
Keyword(s):  
Nmda Receptors ◽  
Sodium Channels ◽  
Pyramidal Cell ◽  
Voltage Dependence ◽  
Late Phase ◽  
Pyramidal Cells ◽  
Receptor Component ◽  
Voltage Dependent ◽  
Gymnotiform Fish ◽  
Apical Dendrites

Voltage-dependent amplification of ionotropic glutamatergic excitatory postsynaptic potentials (EPSPs) can, in many vertebrate neurons, be due either to the intrinsic voltage dependence of N-methyl-d-aspartate (NMDA) receptors, or voltage-dependent persistent sodium channels expressed on postsynaptic dendrites or somata. In the electrosensory lateral line lobe (ELL) of the gymnotiform fish Apteronotus leptorhynchus,glutamatergic inputs onto pyramidal cell apical dendrites provide a system where both amplification mechanisms are possible. We have now examined the roles for both NMDA receptors and sodium channels in the control of EPSP amplitude at these synapses. An antibody specific for the A. leptorhynchus NR1 subunit reacted strongly with ELL pyramidal cells and were particularly abundant in the spines of pyramidal cell apical dendrites. We have also shown that NMDA receptors contributed strongly to the late phase of EPSPs evoked by stimulation of the feedback fibers terminating on the apical dendritic spines; further, these EPSPs were voltage dependent. Blockade of NMDA receptors did not, however, eliminate the voltage dependence of these EPSPs. Blockade of somatic sodium channels by local somatic ejection of tetrodotoxin (TTX), or inclusion of QX314 (an intracellular sodium channel blocker) in the recording pipette, reduced the evoked EPSPs and completely eliminated their voltage dependence. We therefore conclude that, in the subthreshold range, persistent sodium currents are the main contributor to voltage-dependent boosting of EPSPs, even when they have a large NMDA receptor component.

Synchronization of GABAergic Inputs to CA3 Pyramidal Cells Precedes Seizure-Like Event Onset in Juvenile Rat Hippocampal Slices

2009 ◽  
Vol 102 (4) ◽  
pp. 2538-2553 ◽  
Author(s):  
Bálint Lasztóczi ◽  
Gabriella Nyitrai ◽  
László Héja ◽  
Julianna Kardos
Keyword(s):  
Pyramidal Cell ◽  
Synaptic Input ◽  
Hippocampal Slices ◽  
Field Potential ◽  
Reversal Potential ◽  
Pyramidal Cells ◽  
High Frequency Oscillation ◽  
Recurrent Seizure ◽  
Cell Firing ◽  
Ca3 Pyramidal Cells

Here we address how dynamics of glutamatergic and GABAergic synaptic input to CA3 pyramidal cells contribute to spontaneous emergence and evolution of recurrent seizure-like events (SLEs) in juvenile (P10-13) rat hippocampal slices bathed in low-[Mg2+] artificial cerebrospinal fluid. In field potential recordings from the CA3 pyramidal layer, a short epoch of high-frequency oscillation (HFO; 400–800 Hz) was observed during the first 10 ms of SLE onset. GABAergic synaptic input currents to CA3 pyramidal cells were synchronized and coincided with HFO, whereas the glutamatergic input lagged by ∼10 ms. If the intracellular [Cl−] remained unperturbed (cell-attached recordings) or was set high with whole cell electrode solution, CA3 pyramidal cell firing peaked with HFO and GABAergic input. By contrast, with low intracellular [Cl−], spikes of CA3 pyramidal cells lagged behind HFO and GABAergic input. This temporal arrangement of HFO, synaptic input sequence, synchrony of GABAergic currents, and pyramidal cell firing emerged gradually with preictal discharges until the SLE onset. Blockade of GABAA receptor-mediated currents by picrotoxin reduced the inter-SLE interval and the number of preictal discharges and did not block recurrent SLEs. Our data suggest that dynamic changes of the functional properties of GABAergic input contribute to ictogenesis and GABAergic and glutamatergic inputs are both excitatory at the instant of SLE onset. At the SLE onset GABAergic input contributes to synchronization and recruitment of pyramidal cells. We conjecture that this network state is reached by an activity-dependent shift in GABA reversal potential during the preictal phase.

SHAPING NEURONAL DENDRITES: INTERPLAY OF TOPOLOGICAL AND METRICAL PARAMETERS

1995 ◽  
Vol 03 (04) ◽  
pp. 1193-1200 ◽  
Author(s):  
ANDREAS K. SCHIERWAGEN ◽  
JAAP VAN PELT
Keyword(s):  
Radial Distance ◽  
Dendritic Tree ◽  
Pyramidal Cells ◽  
Topological Parameters ◽  
Neuronal Dendrites ◽  
Simulation Results ◽  
Superior Colliculus Neurons ◽  
The Relationship ◽  
Cat Superior Colliculus

The functional role of a neuron within a network is influenced by the geometry of its dendrites. In the present study we have used a new model of dendritic arborization to analyze how metrical and topological parameters interact to shape a certain dendritic tree. One of the specific questions addressed is how to change topological variability in a systematic way while preserving the metrical features. The second problem concerns the effect of topology on the relationship between dendritic size and the distribution of dendritic surface area with radial distance from soma. The simulation results reproduce features of dendritic architecture found in neocortical pyramidal cells and cat superior colliculus neurons.

scholarly journals Dendritic branch structure compartmentalizes voltage-dependent calcium influx in cortical layer 2/3 pyramidal cells

2022 ◽  
Author(s):  
Andrew Tyler Landau ◽  
Pojeong Park ◽  
David Wong-Campos ◽  
Tian He ◽  
Adam Ezra Cohen ◽  
...  
Keyword(s):  
Calcium Influx ◽  
Dendritic Tree ◽  
Pyramidal Cells ◽  
Cortical Layer ◽  
Calcium Signals ◽  
Local Reduction ◽  
Layer 2 ◽  
Voltage Dependent ◽  
Dendritic Branches ◽  
Kinetics Of

Back-propagating action potentials (bAPs) regulate synaptic plasticity by evoking voltage-dependent calcium influx throughout dendrites. Attenuation of bAP amplitude in distal dendritic compartments alters plasticity in a location-specific manner by reducing bAP-dependent calcium influx. However, it is not known if neurons exhibit branch-specific variability in bAP-dependent calcium signals, independent of distance-dependent attenuation. Here, we reveal that bAPs fail to evoke calcium influx through voltage-gated calcium channels (VGCCs) in a specific population of dendritic branches in cortical layer 2/3 pyramidal cells, despite evoking substantial VGCC-mediated calcium influx in sister branches. These branches contain VGCCs and successfully propagate bAPs in the absence of synaptic input; nevertheless, they fail to exhibit bAP-evoked calcium influx due to a branch-specific reduction in bAP amplitude. We demonstrate that these branches have more elaborate branch structure compared to sister branches, which causes a local reduction in electrotonic impedance and bAP amplitude. Finally, we show that bAPs still amplify synaptically-mediated calcium influx in these branches because of differences in the voltage-dependence and kinetics of VGCCs and NMDA-type glutamate receptors. Branch-specific compartmentalization of bAP-dependent calcium signals may provide a mechanism for neurons to diversify synaptic tuning across the dendritic tree.

Model of gradual phase shift of theta rhythm in the rat

1984 ◽  
Vol 52 (6) ◽  
pp. 1051-1065 ◽  
Author(s):  
L. W. Leung
Keyword(s):  
Phase Shift ◽  
Pyramidal Cell ◽  
Theta Rhythm ◽  
Dendritic Tree ◽  
Pyramidal Cells ◽  
Phase Reversal ◽  
Freely Moving Rats ◽  
Theta Frequency ◽  
Freely Moving ◽  
Somatic Inhibition

CA1 pyramidal cell is modeled by a linked series of passive compartments representing the soma and different parts of the dendritic tree. Intracellular postsynaptic potentials are simulated by conductance changes at one or more compartments. By assuming an infinite homogeneous extracellular medium and a particular geometrical arrangement of pyramidal cells, field potential profiles are generated from the current source-sinks of the compartments. The pyramidal cells are driven at the theta (theta)-frequency at different sites of the dendritic tree in order to simulate external driving of hippocampus by the septal cells. Inhibitory or excitatory driving at different sites gives extracellular dipole fields of different null zones and maxima. Phase reversal (180 degrees) of a dipole field generated by synchronous synaptic currents is completed within a depth of 150 micron. By driving two spatially distinct but overlapping dipole fields slightly phase-shifted (30-90 degrees) from each other, the resultant field shows a gradual phase shift of 180 degrees in over 400 micron depth and no (stationary) null zones. The latter field correspond to the theta-profiles seen in the freely moving rat. Somatic inhibition is proposed to be the synaptic process generating the theta-field potentials (named dipole I) in the urethananesthetized or curarized rat. Dipole I has amplitude maxima at the basal dendritic and the distal apical dendritic layers, with a distinct null zone and phase reversal at the apical side of the CA1 pyramidal cell layer. Rhythmic distal dendritic excitation, time-delayed to somatic inhibition, is proposed to be the additional dipole (dipole II) found in freely moving rats. The combination of dipoles I and II, phase-shifted from each other, causes the gradual theta-field phase shift. Experimental studies indicate that dipole I is atropine-sensitive and probably driven by a cholinergic septohippocampal input, whereas dipole II is atropine-resistant and may come from a pathway through both the septum and the entorhinal cortex. Variations of the phase profiles of the theta-field in freely moving rats by administration of anesthetic and cholinergic drugs and by normal changes in theta-frequency could be accounted for by the proposed model. Changes of the intracellular membrane potential, cellular firing rate, and evoked excitability at different phases of the theta-rhythm in anesthetized and freely moving rats can be predicted from the model, and they are in general agreement with the extant literature. In conclusion, theta-field is generated by a rhythmic somatic inhibition phase-shifted with a distal apical-dendritic excitation.(ABSTRACT TRUNCATED AT 400 WORDS)

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