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.

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)

Distance-Dependent Ni2+-Sensitivity of Synaptic Plasticity in Apical Dendrites of Hippocampal CA1 Pyramidal Cells

2002 ◽  
Vol 87 (2) ◽  
pp. 1169-1174 ◽  
Author(s):  
Yoshikazu Isomura ◽  
Yoko Fujiwara-Tsukamoto ◽  
Michiko Imanishi ◽  
Atsushi Nambu ◽  
Masahiko Takada
Keyword(s):  
Calcium Influx ◽  
Critical Role ◽  
Field Potential ◽  
Pyramidal Cells ◽  
Long Term Potentiation ◽  
Apical Dendrite ◽  
Excitatory Postsynaptic Potential ◽  
Distal Dendrite ◽  
Ca1 Pyramidal Cells ◽  
Hippocampal Ca1

Low concentration of Ni2+, a T- and R-type voltage-dependent calcium channel (VDCC) blocker, is known to inhibit the induction of long-term potentiation (LTP) in the hippocampal CA1 pyramidal cells. These VDCCs are distributed more abundantly at the distal area of the apical dendrite than at the proximal dendritic area or soma. Therefore we investigated the relationship between the Ni2+-sensitivity of LTP induction and the synaptic location along the apical dendrite. Field potential recordings revealed that 25 μM Ni2+ hardly influenced LTP at the proximal dendritic area (50 μm distant from the somata). In contrast, the same concentration of Ni2+ inhibited the LTP induction mildly at the middle dendritic area (150 μm) and strongly at the distal dendritic area (250 μm). Ni2+ did not significantly affect either the synaptic transmission at the distal dendrite or the burst-firing ability at the soma. However, synaptically evoked population spikes recorded near the somata were slightly reduced by Ni2+ application, probably owing to occlusion of dendritic excitatory postsynaptic potential (EPSP) amplification. Even when the stimulating intensity was strengthened sufficiently to overcome such a reduction in spike generation during LTP induction, the magnitude of distal LTP was not significantly recovered from the Ni2+-dependent inhibition. These results suggest that Ni2+ may inhibit the induction of distal LTP directly by blocking calcium influx through T- and/or R-type VDCCs. The differentially distributed calcium channels may play a critical role in the induction of LTP at dendritic synapses of the hippocampal pyramidal cells.

Dendrosomatic Voltage and Charge Transfer in Rat Neocortical Pyramidal Cells In Vitro

2000 ◽  
Vol 84 (3) ◽  
pp. 1445-1452 ◽  
Author(s):  
Daniel Ulrich ◽  
Christian Stricker
Keyword(s):  
Membrane Potential ◽  
Time Course ◽  
Cutoff Frequency ◽  
Pyramidal Cells ◽  
Apical Dendrite ◽  
Resting Membrane Potential ◽  
Excitatory Postsynaptic Potential ◽  
Transfer Characteristics ◽  
Layer V

Most excitatory synapses on neocortical pyramidal cells are located on dendrites, which are endowed with a variety of active conductances. The main origin for action potentials is thought to be at the initial segment of the axon, although local regenerative activity can be initiated in the dendrites. The transfer characteristics of synaptic voltage and charge along the dendrite to the soma remains largely unknown, although this is an essential determinant of neural input-output transformations. Here we perform dual whole-cell recordings from layer V pyramidal cells in slices from somatosensory cortex of juvenile rats. Steady-state and sinusoidal current injections are applied to characterize the voltage transfer characteristics of the apical dendrite under resting conditions. Furthermore, dendrosomatic charge and voltage transfer are determined by mimicking synapses via dynamic current-clamping. We find that around rest, the dendrite behaves like a linear cable. The cutoff frequency for somatopetal current transfer is around 4 Hz, i.e., synaptic inputs are heavily low-pass filtered. In agreement with linearity, transfer resistances are reciprocal in opposite directions, and the centroids of the synaptic time course are on the order of the membrane time constant. Transfer of excitatory postsynaptic potential (EPSP) charge, but not peak amplitude, is positively correlated with membrane potential. We conclude that the integrative properties of dendrites in infragranular neocortical pyramidal cells appear to be linear near resting membrane potential. However, at polarized potentials charge transferred is voltage-dependent with a loss of charge at hyperpolarized and a gain of charge at depolarized potentials.

scholarly journals α2-Adrenergic Receptors Modify Dendritic Spike Generation Via HCN Channels in the Prefrontal Cortex

2008 ◽  
Vol 99 (1) ◽  
pp. 394-401 ◽  
Author(s):  
Albert M. I. Barth ◽  
E. Sylvester Vizi ◽  
Tibor Zelles ◽  
Balazs Lendvai
Keyword(s):  
Prefrontal Cortex ◽  
Adrenergic Receptors ◽  
Action Potentials ◽  
Pyramidal Neurons ◽  
Apical Dendrite ◽  
Hcn Channels ◽  
Transient Activation ◽  
Dendritic Spikes ◽  
Dendritic Spike ◽  
Frequency Threshold

Although dendritic spikes are generally thought to be restricted to the distal apical dendrite, we know very little about the possible modulatory mechanisms that set the spatial limits of dendritic spikes. Our experiments demonstrated that high-frequency trains of backpropagating action potentials avoided filtering in the apical dendrite and initiated all-or-none dendritic Ca2+ transients associated with dendritic spikes in layer 5 pyramidal neurons of the prefrontal cortex. The block of hyperpolarization-activated currents ( Ih) by ZD7288 could shift the frequency threshold and decreased the number of action potentials required to produce the all-or-none Ca2+ transient. Activation of α2-adrenergic receptors could also shift the frequency domain of spike induction to lower frequencies. Our data suggest that noradrenergic activity in the prefrontal cortex influences dendritic Ih and extends the zone of dendritic spikes in the apical dendrite via α2-adrenergic receptors. This mechanism might be one cellular correlate of the α2-receptor–mediated actions on working memory.

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.

Dendritic Resonance in Rat Neocortical Pyramidal Cells

2002 ◽  
Vol 87 (6) ◽  
pp. 2753-2759 ◽  
Author(s):  
Daniel Ulrich
Keyword(s):  
Low Frequency ◽  
Pyramidal Cells ◽  
Apical Dendrite ◽  
Threshold Current ◽  
Low Frequencies ◽  
Transfer Impedance ◽  
Whole Cell Patch Clamp ◽  
Voltage Dependent ◽  
Layer V ◽  
Rat Somatosensory Cortex

Dendritic integration of synaptic signals is likely to be an important process by which nerve cells encode synaptic input into spike output. However, the response properties of dendrites to time-varying inputs are largely unknown. Here, I determine the transfer impedance of the apical dendrite in layer V pyramidal cells by dual whole cell patch-clamp recordings in slices of rat somatosensory cortex. Sinusoidal current waveforms of linearly changing frequencies (0.1–25 Hz) were alternately injected into the soma or apical dendrite and the resulting voltage oscillations recorded by the second electrode. Dendrosomatic and somatodendritic transfer impedances were calculated by Fourier analysis. At near physiological temperatures ( T∼35°C), the transfer impedance had a maximal magnitude at low frequencies ( f res ∼6 Hz). In addition, voltage led current up to ∼3 Hz, followed by a current lead over voltage at higher frequencies. Thus the transfer impedance of the apical dendrite is characterized by a low-frequency resonance. The frequency of the resonance was voltage dependent, and its strength increased with dendritic distance. The resonance was completely abolished by the I h channel blocker ZD 7288. Dendrosomatic and somatodendritic transfer properties of the apical dendrite were independent of direction or amplitude of the input current, and the responses of individual versus distributed inputs were additive, thus implying linearity. For just threshold current injections, action potentials were generated preferentially at the resonating frequency. I conclude that due to the interplay of a sag current ( I h) with the membrane capacitance, layer V pyramids can act as linear band-pass filters with a frequency preference in the theta frequency band.

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