scholarly journals Somadendritic Backpropagation of Action Potentials in Cortical Pyramidal Cells of the Awake Rat

1998 ◽  
Vol 79 (3) ◽  
pp. 1587-1591 ◽  
Author(s):  
György Buzsáki ◽  
Adam Kandel
Keyword(s):  
Action Potentials ◽  
Pyramidal Neurons ◽  
Current Source ◽  
Pyramidal Cells ◽  
Apical Dendrite ◽  
Individual Layer ◽  
Awake Rat ◽  
Density Analysis ◽  
Freely Behaving ◽  
Layer V

Buzsáki, György and Adam Kandel. Somadendritic backpropagation of action potentials in cortical pyramidal cells of the awake rat. J. Neurophysiol. 79: 1587–1591, 1998. The invasion of fast (Na+) spikes from the soma into dendrites was studied in single pyramidal cells of the sensorimotor cortex by simultaneous extracellular recordings of the somatic and dendritic action potentials in freely behaving rats. Field potentials and unit activity were monitored with multiple-site silicon probes along trajectories perpendicular to the cortical layers at spatial intervals of 100 μm. Dendritic action potentials of individual layer V pyramidal neurons could be recorded up to 400 μm from the cell body. Action potentials were initiated at the somatic recording site and traveled back to the apical dendrite at a velocity of 0.67 m/s. Current source density analysis of the action potential revealed time shifted dipoles, supporting the view of active spike propagation in dendrites. The presented method is suitable for exploring the conditions affecting the somadendritic propagation action of potentials in the behaving animal.

High I h Channel Density in the Distal Apical Dendrite of Layer V Pyramidal Cells Increases Bidirectional Attenuation of EPSPs

2001 ◽  
Vol 85 (2) ◽  
pp. 855-868 ◽  
Author(s):  
Thomas Berger ◽  
Matthew E. Larkum ◽  
Hans-R. Lüscher
Keyword(s):  
Temporal Summation ◽  
Pyramidal Neurons ◽  
Brain Slices ◽  
Pyramidal Cells ◽  
Signal Propagation ◽  
Apical Dendrite ◽  
Distal Dendrite ◽  
Channel Density ◽  
Apical Tuft ◽  
Layer V

Despite the wealth of recent research on active signal propagation along the dendrites of layer V neocortical pyramidal neurons, there is still little known regarding the traffic of subthreshold synaptic signals. We present a study using three simultaneous whole cell recordings on the apical dendrites of these cells in acute rat brain slices to examine the spread and attenuation of spontaneous excitatory postsynaptic potentials (sEPSPs). Equal current injections at each of a pair of sites separated by ∼500 μm on the apical dendrite resulted in equal voltage transients at the other site (“reciprocity”), thus disclosing linear behavior of the neuron. The mean apparent “length constants” of the apical dendrite were 273 and 446 μm for somatopetal and somatofugal sEPSPs, respectively. Trains of artificial EPSPs did not show temporal summation. Blockade of the hyperpolarization-activated cation current ( I h) resulted in less attenuation by 17% for somatopetal and by 47% for somatofugal sEPSPs. A pronounced location-dependent temporal summation of EPSP trains was seen. The subcellular distribution and biophysical properties of I h were studied in cell-attached patches. Within less than ∼400 μm of the soma, a low density of ∼3 pA/μm2 was found, which increased to ∼40 pA/μm2 in the apical distal dendrite. I h showed activation and deactivation kinetics with time constants faster than 40 ms and half-maximal activation at −95 mV. These findings suggest that integration of synaptic input to the apical tuft and the basal dendrites occurs spatially independently. This is due to a high I h channel density in the apical tuft that increases the electrotonic distance between these two compartments in comparison to a passive dendrite.

Electrophysiological and morphological characteristics of layer VI pyramidal cells in the cat motor cortex

1994 ◽  
Vol 72 (2) ◽  
pp. 578-591 ◽  
Author(s):  
Y. Kang ◽  
F. Kayano
Keyword(s):  
Motor Cortex ◽  
Action Potentials ◽  
Morphological Characteristics ◽  
Pyramidal Cells ◽  
Apical Dendrite ◽  
Current Pulses ◽  
Axon Collaterals ◽  
Layer V ◽  
Apical Dendrites ◽  
Layer Vi

1. Intracellular recordings were made from layer VI pyramidal cells in in vitro slice preparations of the cat motor cortex (area 4 gamma). Layer VI pyramidal cells were identified morphologically by intracellular injection of biocytin. 2. Of 22 layer VI pyramidal cells examined, single action potentials were followed by depolarizing afterpotentials (DAP) in 9 cells, but were not followed by DAP in the remaining 13 cells. The amplitude of DAP was 3.4 +/- 1.4 mV (mean +/- SD, n = 9) when measured from the negative peak of fast afterhyperpolarization to the peak of DAP. 3. In response to depolarizing current pulses with a duration of 300–400 ms, pyramidal cells showing DAP displayed a train of action potentials in a phasic-tonic pattern without any appreciable adaptation in the tonic firing, whereas pyramidal cells lacking DAP exhibited a weak adaptation after phasic firing. Anomalous rectification was seen in both pyramidal cells showing DAP and those lacking DAP. 4. Repetitive doublet or triplet spiking was induced in DAP-showing pyramidal cells in response to a depolarizing current pulse after injecting strong depolarizing current pulses of 400 ms duration at 1 Hz for 30–60 s, but was never induced in DAP-lacking pyramidal cells. Doublet/triplet spiking lasted 5–10 min and returned to the original single spiking. An application of CsCl induced a burst firing in DAP-showing pyramidal cells. 5. In the nine pyramidal cells showing DAP, seven cells had shorter apical dendrites that arborized extensively at layer V and terminated in the middle part of layer III. In the 13 pyramidal cells lacking DAP, 11 cells had longer apical dendrites that arborized less frequently and extended into layer II or I. Main axons could be traced into the deep white matter in 17 of the 22 layer VI pyramidal cells examined. 6. Ascending recurrent axon collaterals were more prominent in pyramidal cells with longer apical dendrites than in pyramidal cells with shorter apical dendrites. The terminal bouton-like swelling observed along the recurrent axon collaterals arising from the pyramidal cells with longer apical dendrite were distributed most densely at the level between the bottom part of layer III and the top part of layer V. In contrast, those arising from the pyramidal cells with shorter apical dendrite were distributed mainly at the levels of layers V and VI.(ABSTRACT TRUNCATED AT 400 WORDS)

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.

Distribution of Slow AHP Channels on Hippocampal CA1 Pyramidal Neurons

2000 ◽  
Vol 83 (3) ◽  
pp. 1756-1759 ◽  
Author(s):  
John M. Bekkers
Keyword(s):  
Action Potentials ◽  
Pyramidal Neurons ◽  
Pyramidal Cells ◽  
Apical Dendrite ◽  
Ca1 Pyramidal Cells ◽  
Ca1 Pyramidal Neurons ◽  
Basal Dendrites ◽  
Hippocampal Ca1 ◽  
Cell Current ◽  
Whole Cell Current

This work was designed to localize the Ca2+-activated K+ channels underlying the slow afterhyperpolarization (sAHP) in hippocampal CA1 pyramidal cells. Cell-attached patches on the proximal 100 μm of the apical dendrite contained K+ channels, but not sAHP channels, activated by backpropagating action potentials. Amputation of the apical dendrite ∼30 μm from the soma, while simultaneously recording the sAHP whole cell current at the soma, depressed the sAHP amplitude by only ∼30% compared with control. Somatic cell-attached and nucleated patches did not contain sAHP current. Amputation of the axon ≥20 μm from the soma had little effect on the amplitude of the sAHP recorded in cortical pyramidal cells. By this process of elimination, it is suggested that sAHP channels may be concentrated in the basal dendrites of CA1 pyramids.

scholarly journals GABAA Mediated Afterdepolarization in Pyramidal Neurons From Rat Neocortex

1997 ◽  
Vol 77 (2) ◽  
pp. 1039-1045 ◽  
Author(s):  
R. Cerne ◽  
W. J. Spain
Keyword(s):  
Action Potentials ◽  
Pyramidal Neurons ◽  
Brain Slices ◽  
Apical Dendrite ◽  
Dependent Manner ◽  
Voltage Dependent ◽  
Rat Neocortex ◽  
Layer V ◽  
Current Steps ◽  
Intense Activity

Cerne, R. and W. J. Spain. A GABAA mediated afterdepolarization in pyramidal neurons from rat neocortex. J. Neurophysiol. 77: 1039–1045, 1997. We report a novel slow afterdepolarization (sADP) in layer V pyramidal neurons when brain slices from somatosensory cortex are perfused with γ-aminobutyric acid (GABA). Whole cell recordings were made from visually identified neurons in slices from 3- to 5-wk-old rats. The firing of action potentials at 100 Hz for 1 s, evoked by a train of brief current pulses, typically is followed by a slow afterhyperpolarization (sAHP). When GABA (1 mM) was applied to the perfusate, the sAHP was replaced by a sADP of ≈18 mV in amplitude, which on average lasted for 26 s. The sADP was not evoked or terminated as an all-or-none event: it grew in amplitude and duration as the number of evoked action potentials was increased; and when the sADP was interrupted with hyperpolarizing current steps, its amplitude and duration were graded in a time- and voltage-dependent manner. The sADP did not depend on Ca2+ entry into the cell: it could be evoked when bath Ca2+ was replaced by Mn2+ or in neurons dialyzed with 20 mM bis-( o-aminophenoxy)- N,N,N′,N′-tetraacetic acid. We hypothesized that the sADP was generated predominantly in the dendrites because it was associated with the firing of small-amplitude action potentials that continued after the somatic membrane potential was repolarized to −70 mV by steady current injection. We tested this hypothesis by evoking the sADP in neurons with surgically amputated apical dendrites. In those neurons, the average duration of the sADP was 78% shorter than in neurons with an intact apical dendrite and there were no associated small action potentials. The sADP also was evoked by muscimol, but not by baclofen, and was blocked by bicuculline or picrotoxin but not by CGP 35348, indicating that it is mediated through the activation of GABAA receptors. Our results suggest that intense activity in the presence of GABA results in a long-lasting enhancement of excitability in the apical dendrite that in turn could lead to amplification of distal excitatory synaptic potentials.

scholarly journals Two Populations of Layer V Pyramidal Cells of the Mouse Neocortex: Development and Sensitivity to Anesthetics

2005 ◽  
Vol 94 (5) ◽  
pp. 3357-3367 ◽  
Author(s):  
Elodie Christophe ◽  
Nathalie Doerflinger ◽  
Daniel J. Lavery ◽  
Zoltán Molnár ◽  
Serge Charpak ◽  
...  
Keyword(s):  
Action Potential ◽  
Calcium Binding ◽  
Pyramidal Neurons ◽  
Pyramidal Cells ◽  
Membrane Properties ◽  
Subcortical Structures ◽  
Contralateral Cortex ◽  
Layer V ◽  
Intrinsic Membrane Properties ◽  
Two Populations

Previous studies have shown that layer V pyramidal neurons projecting either to subcortical structures or the contralateral cortex undergo different morphological and electrophysiological patterns of development during the first three postnatal weeks. To isolate the determinants of this differential maturation, we analyzed the gene expression and intrinsic membrane properties of layer V pyramidal neurons projecting either to the superior colliculus (SC cells) or the contralateral cortex (CC cells) by combining whole cell recordings and single-cell RT-PCR in acute slices prepared from postnatal day (P) 5–7 or P21–30 old mice. Among the 24 genes tested, the calcium channel subunits α1B and α1C, the protease Nexin 1, and the calcium-binding protein calbindin were differentially expressed in adult SC and CC cells and the potassium channel subunit Kv4.3 was expressed preferentially in CC cells at both stages of development. Intrinsic membrane properties, including input resistance, amplitude of the hyperpolarization-activated current, and action potential threshold, differed quantitatively between the two populations as early as from the first postnatal week and persisted throughout adulthood. However, the two cell types had similar regular action potential firing behaviors at all developmental stages. Surprisingly, when we increased the duration of anesthesia with ketamine–xylazine or pentobarbital before decapitation, a proportion of mature SC cells, but not CC cells, fired bursts of action potentials. Together these results indicate that the two populations of layer V pyramidal neurons already start to differ during the first postnatal week and exhibit different firing capabilities after anesthesia.

scholarly journals Apical length governs computational diversity of L5 pyramidal neurons

2019 ◽  
Author(s):  
Alessandro R. Galloni ◽  
Aeron Laffere ◽  
Ede Rancz
Keyword(s):  
Action Potentials ◽  
Pyramidal Neurons ◽  
Apical Dendrite ◽  
Common Assumption ◽  
Dendritic Excitability ◽  
Visual Cortices ◽  
The Common ◽  
Channel Dependent ◽  
Apical Dendrites ◽  
The Brain

AbstractAnatomical similarity across the neocortex has led to the common assumption that the circuitry is modular and performs stereotyped computations. Layer 5 pyramidal neurons (L5PNs) in particular are thought to be central to cortical computation because of their extensive arborisation and nonlinear dendritic operations. Here, we demonstrate that computations associated with dendritic Ca2+ plateaus in L5PNs vary substantially between the primary and secondary visual cortices. L5PNs in the secondary visual cortex show reduced dendritic excitability and smaller propensity for burst firing. This reduced excitability is correlated with shorter apical dendrites. Using numerical modelling, we uncover a universal principle underlying the influence of apical length on dendritic backpropagation and excitability, based on a Na+ channel-dependent broadening of backpropagating action potentials. In summary, we provide new insights into the modulation of dendritic excitability by apical dendrite length and show that the operational repertoire of L5 neurons is not universal throughout the brain.

scholarly journals Bayesian modeling of BAC firing as a mechanism for apical amplification in neocortical pyramidal neurons

2019 ◽  
Author(s):  
Jim W. Kay ◽  
W. A. Phillips ◽  
Jaan Aru ◽  
Bruce P. Graham ◽  
Matthew E. Larkum
Keyword(s):  
Action Potentials ◽  
Pyramidal Neurons ◽  
Pyramidal Cells ◽  
Single Site ◽  
Biophysical Model ◽  
Cellular Mechanisms ◽  
Context Sensitive ◽  
Dendritic Shaft ◽  
Current Task ◽  
Integration Sites

AbstractPyramidal cells in layer 5 of the neocortex have two distinct integration sites. These cells integrate inputs to basal dendrites in the soma while integrating inputs to the tuft in a site at the top of the apical trunk. The two sites communicate by action potentials that backpropagate to the apical site and by backpropagation-activated calcium spikes (BAC firing) that travel from the apical to the somatic site. Six key messages arise from the probabilistic information-theoretic analyses of BAC firing presented here. First, we suggest that pyramidal neurons with BAC firing could convert the odds in favour of the presence of a feature given the basal data into the odds in favour of the presence of a feature given the basal data and the apical input, by a simple Bayesian calculation. Second, the strength of the cell’s response to basal input can be amplified when relevant to the current context, as specified by the apical input, without corrupting the message that it sends. Third, these analyses show rigorously how this apical amplification depends upon communication between the sites. Fourth, we use data on action potentials from a very detailed multi-compartmental biophysical model to study our general model in a more realistic setting, and demonstrate that it describes the data well. Fifth, this form of BAC firing meets criteria for distinguishing modulatory from driving interactions that have been specified using recent definitions of multivariate mutual information. Sixth, our general decomposition can be extended to cases where, instead of being purely driving or purely amplifying, apical and basal inputs can be partly driving and partly amplifying to various extents. These conclusions imply that an advance beyond the assumption of a single site of integration within pyramidal cells is needed, and suggest that the evolutionary success of neocortex may depend upon the cellular mechanisms of context-sensitive selective amplification hypothesized here.Author summaryThe cerebral cortex has a key role in conscious perception, thought, and action, and is predominantly composed of a particular kind of neuron: the pyramidal cells. The distinct shape of the pyramidal neuron with a long dendritic shaft separating two regions of profuse dendrites allows them to integrate inputs to the two regions separately and combine the results non-linearly to produce output. Here we show how inputs to this more distant site strengthen the cell’s output when it is relevant to the current task and environment. By showing that such neurons have capabilities that transcend those of neurons with the single site of integration assumed by many neuroscientists, this ‘splitting of the neuronal atom’ offers a radically new viewpoint from which to understand the evolution of the cortex and some of its many pathologies. This also suggests that approaches to artificial intelligence using neural networks might come closer to something analogous to real intelligence, if, instead of basing them on processing elements with a single site of integration, they were based on elements with two sites, as in cortex.

Current Source Density Profiles of Stimulus-Specific Adaptation in Rat Auditory Cortex

2009 ◽  
Vol 102 (3) ◽  
pp. 1483-1490 ◽  
Author(s):  
Francois D. Szymanski ◽  
Jose A. Garcia-Lazaro ◽  
Jan W. H. Schnupp
Keyword(s):  
Auditory Cortex ◽  
Current Source ◽  
Primary Auditory Cortex ◽  
Auditory Pathway ◽  
Afferent Input ◽  
Current Source Density ◽  
Specific Adaptation ◽  
Source Density ◽  
Density Analysis ◽  
Layer V

Neurons in primary auditory cortex (A1) are known to exhibit a phenomenon known as stimulus-specific adaptation (SSA), which means that, when tested with pure tones, they will respond more strongly to a particular frequency if it is presented as a rare, unexpected “oddball” stimulus than when the same stimulus forms part of a series of common, “standard” stimuli. Although SSA has occasionally been observed in midbrain neurons that form part of the paraleminscal auditory pathway, it is thought to be weak, rare, or nonexistent among neurons of the leminscal pathway that provide the main afferent input to A1, so that SSA seen in A1 is likely generated within A1 by local mechanisms. To study the contributions that neural processing within the different cytoarchitectonic layers of A1 may make to SSA, we recorded local field potentials in A1 of the rat in response to standard and oddball tones and subjected these to current source density analysis. Although our results show that SSA can be observed throughout all layers of A1, right from the earliest part of the response, there are nevertheless significant differences between layers, with SSA becoming significantly stronger as stimulus-related activity passes from the main thalamorecipient layers III and IV to layer V.

Excitation of hippocampal pyramidal cells by an electrical field effect

1984 ◽  
Vol 52 (1) ◽  
pp. 126-142 ◽  
Author(s):  
C. P. Taylor ◽  
F. E. Dudek
Keyword(s):  
Cell Body ◽  
Pyramidal Cell ◽  
Action Potentials ◽  
Current Source ◽  
Extracellular Recording ◽  
Pyramidal Cells ◽  
Physiological Solution ◽  
Adjacent Cell ◽  
Electrical Field ◽  
Population Spikes

The effects of electrical fields from antidromic stimulation of CA1 pyramidal cells were studied in slices of rat hippocampus in which chemical synaptic transmission had been blocked by superfusion with physiological solution containing Mn2+ and lowered concentration of Ca2+. Differential voltage recordings were made between two microelectrode positions, on intracellular to a pyramidal cell and the other in the adjacent extracellular space. This technique revealed brief transmembrane depolarizations that occurred synchronously with negative-going extracellular population spikes in the adjacent cell body layer. Glial cells in this region did not exhibit these depolarizations. In some pyramidal cells, alvear stimulation that was too weak to excite the axon of the impaled cell elicited action potentials, which appeared to arise from transmembrane depolarizations at the soma. When subthreshold transmembrane depolarizations were superimposed on subthreshold depolarizing current pulses, somatic action potentials were generated synchronously with the antidromic population spikes. The depolarizations of pyramidal somata were finely graded with stimulus intensity, were unaffected by polarization of the membrane, and were not occluded by preceding action potentials. The laminar profile of extracellular field potentials perpendicular to the cell body layer was obtained with an array of extracellular recording locations. Numerical techniques of current source-density analysis indicated that at the peak of the somatic population spike, there was an extracellular current sink near pyramidal somata and sources in distal dendritic regions. It is concluded that during population spikes an extracellular electrical field causes currents to flow passively across inactive pyramidal cell membranes, thus depolarizing their somata. The transmembrane depolarizations associated with population spikes would tend to excite and synchronize the population of pyramidal cells.

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