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.

scholarly journals Distance- and activity-dependent modulation of spike back-propagation in layer V pyramidal neurons of the medial entorhinal cortex

2011 ◽  
Vol 105 (3) ◽  
pp. 1372-1379 ◽  
Author(s):  
Sonia Gasparini
Keyword(s):  
Entorhinal Cortex ◽  
High Speed ◽  
Pyramidal Neurons ◽  
Back Propagation ◽  
Medial Entorhinal Cortex ◽  
Type K ◽  
Whole Cell Patch Clamp ◽  
Voltage Dependent ◽  
Layer V ◽  
Activity Dependent

Layer V principal neurons of the medial entorhinal cortex receive the main hippocampal output and relay processed information to the neocortex. Despite the fundamental role hypothesized for these neurons in memory replay and consolidation, their dendritic features are largely unknown. High-speed confocal and two-photon Ca2+ imaging coupled with somatic whole cell patch-clamp recordings were used to investigate spike back-propagation in these neurons. The Ca2+ transient associated with a single back-propagating action potential was considerably smaller at distal dendritic locations (>200 μm from the soma) compared with proximal ones. Perfusion of Ba2+ (150 μM) or 4-aminopyridine (2 mM) to block A-type K+ currents significantly increased the amplitude of the distal, but not proximal, Ca2+ transients, which is strong evidence for an increased density of these channels at distal dendritic locations. In addition, the Ca2+ transients decreased with each subsequent spike in a 20-Hz train; this activity-dependent decrease was also more prominent at more distal locations and was attenuated by the perfusion of the protein kinase C activator phorbol-di-acetate. These data are consistent with a phosphorylation-dependent control of back-propagation during trains of action potentials, attributable mainly to an increase in the time constant of recovery from voltage-dependent inactivation of dendritic Na+ channels. In summary, dendritic Na+ and A-type K+ channels control spike back-propagation in layer V entorhinal neurons. Because the activity of these channels is highly modulated, the extent of the dendritic Ca2+ influx is as well, with important functional implications for dendritic integration and associative synaptic plasticity.

scholarly journals The Role of NMDA Receptor Subtypes in Short-Term Plasticity in the Rat Entorhinal Cortex

2008 ◽  
Vol 2008 ◽  
pp. 1-13 ◽  
Author(s):  
Sophie E. L. Chamberlain ◽  
Jian Yang ◽  
Roland S. G. Jones
Keyword(s):  
Entorhinal Cortex ◽  
Glutamate Release ◽  
Receptor Subtypes ◽  
Short Term ◽  
Low Frequencies ◽  
Short Term Plasticity ◽  
Whole Cell Patch Clamp ◽  
Layer V ◽  
Presynaptic Nmda Receptors

We have previously shown that spontaneous release of glutamate in the entorhinal cortex (EC) is tonically facilitated via activation of presynaptic NMDA receptors (NMDAr) containing the NR2B subunit. Here we show that the same receptors mediate short-term plasticity manifested by frequency-dependent facilitation of evoked glutamate release at these synapses. Whole-cell patch-clamp recordings were made from layer V pyramidal neurones in rat EC slices. Evoked excitatory postsynaptic currents showed strong facilitation at relatively low frequencies (3 Hz) of activation. Facilitation was abolished by an NR2B-selective blocker (Ro 25-6981), but unaffected by NR2A-selective antagonists (Zn2+, NVP-AAM077). In contrast, postsynaptic NMDAr-mediated responses could be reduced by subunit-selective concentrations of all three antagonists. The data suggest that NMDAr involved in presynaptic plasticity in layer V are exclusively NR1/NR2B diheteromers, whilst postsynaptically they are probably a mixture of NR1/NR2A, NR1/NR2B diheteromers and NR1/NR2A/NR2B triheteromeric receptors.

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.

Kinetics of GABAB autoreceptor-mediated suppression of GABA release in rat insular cortex

2012 ◽  
Vol 107 (5) ◽  
pp. 1431-1442 ◽  
Author(s):  
Masayuki Kobayashi ◽  
Hiroki Takei ◽  
Kiyofumi Yamamoto ◽  
Hiroshige Hatanaka ◽  
Noriaki Koshikawa
Keyword(s):  
Insular Cortex ◽  
Pyramidal Cells ◽  
Gaba Release ◽  
Paired Pulse ◽  
Whole Cell Patch Clamp ◽  
Pulse Ratio ◽  
Presynaptic Mechanisms ◽  
Fast Spiking ◽  
Layer V ◽  
Interevent Interval

Release of GABA is controlled by presynaptic GABA receptor type B (GABAB) autoreceptors at GABAergic terminals. However, there is no direct evidence that GABAB autoreceptors are activated by GABA release from their own terminals, and precise profiles of GABAB autoreceptor-mediated suppression of GABA release remain unknown. To explore these issues, we performed multiple whole-cell, patch-clamp recordings from layer V rat insular cortex. Both unitary inhibitory and excitatory postsynaptic currents (uIPSCs and uEPSCs, respectively) were recorded by applying a five-train depolarizing pulse injection at 20 Hz. In connections from both fast-spiking (FS) and non-FS interneurons to pyramidal cells, the GABAB receptor antagonist CGP 52432 had little effect on the initial uIPSC amplitude. However, uIPSCs, responding to later pulses, were effectively facilitated. This CGP 52432-induced facilitation was prominent in the fourth uIPSCs, which were evoked 150 ms after the first uIPSC. The facilitation of uIPSCs was accompanied by an increase in the paired-pulse ratio. In addition, analysis of the coefficient of variation suggests the involvement of presynaptic mechanisms in CGP 52432-induced uIPSC facilitation. Paired-pulse stimulation (interstimulus interval = 150 ms) of presynaptic FS cells revealed that the second uIPSC was also facilitated by CGP 52432, which had little effect on the amplitude and interevent interval of miniature IPSCs. In contrast, uEPSCs, responding to all five stimulations of a presynaptic pyramidal cell, were less affected by CGP 52432. These results suggest that a single presynaptic action potential is sufficient to activate GABAB autoreceptors and to suppress GABA release in the cerebral cortex.

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.

Threshold Firing Frequency–Current Relationships of Neurons in Rat Somatosensory Cortex: Type 1 and Type 2 Dynamics

2004 ◽  
Vol 92 (4) ◽  
pp. 2283-2294 ◽  
Author(s):  
T. Tateno ◽  
A. Harsch ◽  
H. P. C. Robinson
Keyword(s):  
Somatosensory Cortex ◽  
Low Frequency ◽  
Firing Frequency ◽  
Spike Generation ◽  
Low Frequencies ◽  
Subthreshold Oscillations ◽  
Wide Range ◽  
Rat Somatosensory Cortex

Neurons and dynamical models of spike generation display two different types of threshold behavior, with steady current stimulation: type 1 [the firing frequency vs. current ( f– I) relationship is continuous at threshold) and type 2 (discontinuous f– I)]. The dynamics at threshold can have profound effects on the encoding of input as spikes, the sensitivity of spike generation to input noise, and the coherence of population firing. We have examined the f– I and frequency–conductance ( f– g) relationships of cells in layer 2/3 of slices of young (15–21 DIV) rat somatosensory cortex, focusing in detail on the nature of the threshold. Using white-noise stimulation, we also measured firing frequency and interspike interval variability as a function of noise amplitude. Regular-spiking (RS) pyramidal neurons show a type 1 threshold, consistent with their well-known ability to fire regularly at very low frequencies. In fast-spiking (FS) inhibitory interneurons, although regular firing is supported over a wide range of frequencies, there is a clear discontinuity in their f– I relationship at threshold (type 2), which has not previously been highlighted. FS neurons are unable to support maintained periodic firing below a critical frequency fc, in the range of 10 to 30 Hz. Very close to threshold, FS cells switch irregularly between bursts of periodic firing and subthreshold oscillations. These characteristics mean that the dynamics of RS neurons are well suited to encoding inputs into low-frequency firing rates, whereas the dynamics of FS neurons are suited to maintaining and quickly synchronizing to gamma and higher-frequency input.

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.

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.

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)

scholarly journals Thalamic circuitry and thalamocortical synchrony

2002 ◽  
Vol 357 (1428) ◽  
pp. 1659-1673 ◽  
Author(s):  
Edward G. Jones
Keyword(s):  
Cortical Neurons ◽  
Low Frequency ◽  
Oscillatory Activity ◽  
Reticular Nucleus ◽  
Cortical Cells ◽  
Dorsal Thalamus ◽  
High Frequency Oscillations ◽  
Voltage Dependent ◽  
Layer V ◽  
Layer Vi

The corticothalamic system has an important role in synchronizing the activities of thalamic and cortical neurons. Numerically, its synapses dominate the inputs to relay cells and to the γ–amino butyric acid (GABA)ergic cells of the reticular nucleus (RTN). The capacity of relay neurons to operate in different voltage–dependent functional modes determines that the inputs from the cortex have the capacity directly to excite the relay cells, or indirectly to inhibit them via the RTN, serving to synchronize high– or low–frequency oscillatory activity respectively in the thalamocorticothalamic network. Differences in the α–amino–3–hydroxy–5–methyl–4–isoxazolepropionic acid (AMPA) subunit composition of receptors at synapses formed by branches of the same corticothalamic axon in the RTN and dorsal thalamus are an important element in the capacity of the cortex to synchronize low–frequency oscillations in the network. Interactions of focused corticothalamic axons arising from layer VI cortical cells and diffuse corticothalamic axons arising from layer V cortical cells, with the specifically projecting core relay cells and diffusely projecting matrix cells of the dorsal thalamus, form a substrate for synchronization of widespread populations of cortical and thalamic cells during high–frequency oscillations that underlie discrete conscious events.

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