Back-propagation of physiological action potential output in dendrites of slender-tufted L5A pyramidal neurons
56
Citation
54
Reference
10
Related Paper
Citation Trend
Abstract:
Pyramidal neurons of layer 5A are a major neocortical output type and clearly distinguished from layer 5B pyramidal neurons with respect to morphology, in vivo firing patterns, and connectivity; yet knowledge of their dendritic properties is scant. We used a combination of whole-cell recordings and Ca(2+) imaging techniques in vitro to explore the specific dendritic signaling role of physiological action potential patterns recorded in vivo in layer 5A pyramidal neurons of the whisker-related 'barrel cortex'. Our data provide evidence that the temporal structure of physiological action potential patterns is crucial for an effective invasion of the main apical dendrites up to the major branch point. Both the critical frequency enabling action potential trains to invade efficiently and the dendritic calcium profile changed during postnatal development. In contrast to the main apical dendrite, the more passive properties of the short basal and apical tuft dendrites prevented an efficient back-propagation. Various Ca(2+) channel types contributed to the enhanced calcium signals during high-frequency firing activity, whereas A-type K(+) and BK(Ca) channels strongly suppressed it. Our data support models in which the interaction of synaptic input with action potential output is a function of the timing, rate and pattern of action potentials, and dendritic location.Keywords:
Dendritic spike
Apical dendrite
Barrel cortex
Dendrite (mathematics)
Pyramidal cell
Neocortex
Calcium imaging
Dendritic spike
Apical dendrite
Dendrite (mathematics)
Pyramidal cell
Schaffer collateral
Cite
Citations (17)
Pyramidal neurons of layer 5A are a major neocortical output type and clearly distinguished from layer 5B pyramidal neurons with respect to morphology, in vivo firing patterns, and connectivity; yet knowledge of their dendritic properties is scant. We used a combination of whole-cell recordings and Ca(2+) imaging techniques in vitro to explore the specific dendritic signaling role of physiological action potential patterns recorded in vivo in layer 5A pyramidal neurons of the whisker-related 'barrel cortex'. Our data provide evidence that the temporal structure of physiological action potential patterns is crucial for an effective invasion of the main apical dendrites up to the major branch point. Both the critical frequency enabling action potential trains to invade efficiently and the dendritic calcium profile changed during postnatal development. In contrast to the main apical dendrite, the more passive properties of the short basal and apical tuft dendrites prevented an efficient back-propagation. Various Ca(2+) channel types contributed to the enhanced calcium signals during high-frequency firing activity, whereas A-type K(+) and BK(Ca) channels strongly suppressed it. Our data support models in which the interaction of synaptic input with action potential output is a function of the timing, rate and pattern of action potentials, and dendritic location.
Dendritic spike
Apical dendrite
Barrel cortex
Dendrite (mathematics)
Pyramidal cell
Neocortex
Calcium imaging
Cite
Citations (56)
Synaptically coupled layer 2/3 (L2/3) pyramidal neurones located above the same layer 4 barrel ('barrel-related') were investigated using dual whole-cell voltage recordings in acute slices of rat somatosensory cortex. Recordings were followed by reconstructions of biocytin-filled neurones. The onset latency of unitary EPSPs was 1.1 +/- 0.4 ms, the 20-80% rise time was 0.7 +/- 0.2 ms, the average amplitude was 1.0 +/- 0.7 mV and the decay time constant was 15.7 +/- 4.5 ms. The coefficient of variation (c.v.) of unitary EPSP amplitudes decreased with increasing EPSP peak and was 0.33 +/- 0.18. Bursts of APs in the presynaptic pyramidal cell resulted in EPSPs that, over a wide range of frequencies (5-100 Hz), displayed amplitude depression. Anatomically the barrel-related pyramidal cells in the lower half of layer 2/3 have a long apical dendrite with a small terminal tuft, while pyramidal cells in the upper half of layer 2/3 have shorter and often more 'irregularly' shaped apical dendrites that branch profusely in layer 1. The number of putative excitatory synaptic contacts established by the axonal collaterals of a L2/3 pyramidal cell with a postsynaptic pyramidal cell in the same column varied between 2 and 4, with an average of 2.8 +/- 0.7 (n = 8 pairs). Synaptic contacts were established predominantly on the basal dendrites at a mean geometric distance of 91 +/- 47 mum from the pyramidal cell soma. L2/3-to-L2/3 connections formed a blob-like innervation domain containing 2.8 mm of the presynaptic axon collaterals with a bouton density of 0.3 boutons per mum axon. Within the supragranular layers of its home column a single L2/3 pyramidal cell established about 900 boutons suggesting that 270 pyramidal cells in layer 2/3 are innervated by an individual pyramidal cell. In turn, a single pyramidal cell received synaptic inputs from 270 other L2/3 pyramidal cells. The innervation domain of L2/3-to-L2/3 connections superimposes almost exactly with that of L4-to-L2/3 connections. This suggests that synchronous feed-forward excitation of L2/3 pyramidal cells arriving from layer 4 could be potentially amplified in layer 2/3 by feedback excitation within a column and then relayed to the neighbouring columns.
Pyramidal cell
Barrel cortex
Apical dendrite
Rheobase
Pyramidal tracts
Dendrite (mathematics)
Biocytin
Cite
Citations (327)
Layer 6 (L6) pyramidal neurons are the only neocortical pyramidal cell type whose apical dendrite terminates in layer 4 rather than layer 1. Like layer 5 pyramidal neurons, they participate in a feedback loop with the thalamus and project to other cortical areas. Despite their unique location in the cortical microcircuit, synaptic integration in dendrites of L6 neurons has never been investigated. Given that all other neocortical pyramidal neurons perform active integration of synaptic inputs via local dendritic spike generation, we were interested to establish the apical dendritic properties of L6 pyramidal neurons. We measured active and passive properties of the apical dendrites of L6 pyramidal neurons in the somatosensory region of rat cortical slices using dual patch-clamp recordings from somata and dendrites and calcium imaging. We found that L6 pyramidal neurons share many fundamental dendritic properties with other neocortical pyramidal neurons, including the generation of local dendritic spikes under the control of dendritic inhibition, voltage-dependent support of backpropagating action potentials, timing-dependent dendritic integration, distally located I h channels, frequency-dependent Ca 2+ spike activation, and NMDA spike electrogenesis in the distal apical dendrite. The results suggest that L6 pyramidal neurons integrate synaptic inputs in layer 4 similar to the way other neocortical pyramidal neurons integrate input to layer 1. Thus, L6 pyramidal neurons can perform a similar associational task operating on inputs arriving at the granular and subgranular layers.
Apical dendrite
Pyramidal cell
Dendritic spike
Dendrite (mathematics)
Pyramidal tracts
Cite
Citations (93)
Reversed somatodendritic Ih gradient in a class of rat hippocampal neurons with pyramidal morphology
In CA1 and neocortical pyramidal neurons, I(h) is present primarily in the dendrites. We asked if all neurons of a pyramidal morphology have a similar density of I(h). We characterized a novel class of hippocampal neurons with pyramidal morphology found in the stratum radiatum, which we termed the 'pyramidal-like principal' (PLP) neuron. Morphological similarities to pyramidal neurons were verified by filling the neurons with biocytin. PLPs did not stain for markers associated with interneurons, and projected to both the septum and olfactory bulb. By using cell-attached patch-clamp recordings, we found that these neurons expressed a high density of I(h) in the soma that declined to a lower density in the dendrites, a pattern that is reversed compared to pyramidal neurons. The voltage-dependent activation and activation time constants of I(h) in the PLPs were similar to pyramidal neurons. Whole-cell patch-clamp recordings from the soma and dendrites of PLP neurons showed no significant differences in input resistance and local temporal summation between the two locations. Blockade of I(h) by ZD7288 increased the input resistance and temporal summation of simulated EPSPs, as in pyramidal neurons. When NMDA receptors were blocked, temporal summation at the soma of distal synaptic potentials was similar to that seen with current injections at the soma, suggesting a 'normalization' of temporal summation similar to that observed in pyramidal neurons. Thus, we have characterized a principal neuronal subtype in the hippocampus with a similar morphology but reversed I(h) somatodendritic gradient to that previously observed in CA1 hippocampal and neocortical pyramidal neurons.
Pyramidal cell
Apical dendrite
Biocytin
Dendritic spike
Dendrite (mathematics)
Cite
Citations (40)
The voltage-dependent properties that have been directly demonstrated in Purkinje cell and hippocampal pyramidal cell dendrites play an important role in the integrative capacities of these neurons. By contrast, the properties of neocortical pyramidal cell dendritic membranes have been more difficult to assess. Active dendritic conductances near sites of synaptic input would have an important effect on the input-output characteristics of these neurons. In the experiments reported here, we obtained direct evidence for the existence of voltage-dependent Na+ channels on the dendrites of neocortical neurons by using cell-attached patch and whole cell recordings from acutely isolated rat neocortical pyramidal cells. The qualitative and quantitative properties of dendritic and somatic currents were indistinguishable. Insofar as Na+ currents are concerned, the soma and primary apical dendrite can be considered as one relatively uniform compartment. Similar dendritic Na+ currents on dendrites in mature neurons would play an important role in determining the integrative properties of these cortical units.
Dendritic spike
Dendrite (mathematics)
Apical dendrite
Pyramidal cell
Neocortex
Cortical neurons
Cite
Citations (189)
The dendritic tree of layer 5 (L5) pyramidal neurons spans the neocortical layers, allowing the integration of intra- and extracortical synaptic inputs. Here we investigate the postnatal development of the integrative properties of rat L5 pyramidal neurons using simultaneous whole cell recording from the soma and distal apical dendrite. In young (P9-10) neurons, apical dendritic excitatory synaptic input powerfully drove action potential output by efficiently summating at the axonal site of action potential generation. In contrast, in mature (P25-29) neurons, apical dendritic excitatory input provided little direct depolarization at the site of action potential generation but was integrated locally in the apical dendritic tree leading to the generation of dendritic spikes. Consequently, over the first postnatal month the fraction of action potentials driven by apical dendritic spikes increased dramatically. This developmental remodeling of the integrative operations of L5 pyramidal neurons was controlled by a >10-fold increase in the density of apical dendritic Hyperpolarization-activated cyclic nucleotide (HCN)-gated channels found in cell-attached patches or by immunostaining for the HCN channel isoform HCN1. Thus an age-dependent increase in apical dendritic HCN channel density ensures that L5 pyramidal neurons develop from compact temporal integrators to compartmentalized integrators of basal and apical dendritic synaptic input.
Dendritic spike
Apical dendrite
Pyramidal cell
Dendritic filopodia
Dendrite (mathematics)
HCN channel
Cite
Citations (71)
Signal propagation in the dendrites of many neurons, including cortical pyramidal neurons in sensory cortex, is characterized by strong attenuation toward the soma. In contrast, using dual whole-cell recordings from the apical dendrite and soma of layer 5 (L5) pyramidal neurons in the anterior cingulate cortex (ACC) of adult male mice we found good coupling, particularly of slow subthreshold potentials like NMDA spikes or trains of EPSPs from dendrite to soma. Only the fastest EPSPs in the ACC were reduced to a similar degree as in primary somatosensory cortex, revealing differential low-pass filtering capabilities. Furthermore, L5 pyramidal neurons in the ACC did not exhibit dendritic Ca 2+ spikes as prominently found in the apical dendrite of S1 (somatosensory cortex) pyramidal neurons. Fitting the experimental data to a NEURON model revealed that the specific distribution of I leak , I ir , I m , and I h was sufficient to explain the electrotonic dendritic structure causing a leaky distal dendritic compartment with correspondingly low input resistance and a compact perisomatic region, resulting in a decoupling of distal tuft branches from each other while at the same time efficiently connecting them to the soma. Our results give a biophysically plausible explanation of how a class of prefrontal cortical pyramidal neurons achieve efficient integration of subthreshold distal synaptic inputs compared with the same cell type in sensory cortices. SIGNIFICANCE STATEMENT Understanding cortical computation requires the understanding of its fundamental computational subunits. Layer 5 pyramidal neurons are the main output neurons of the cortex, integrating synaptic inputs across different cortical layers. Their elaborate dendritic tree receives, propagates, and transforms synaptic inputs into action potential output. We found good coupling of slow subthreshold potentials like NMDA spikes or trains of EPSPs from the distal apical dendrite to the soma in pyramidal neurons in the ACC, which was significantly better compared with S1. This suggests that frontal pyramidal neurons use a different integration scheme compared with the same cell type in somatosensory cortex, which has important implications for our understanding of information processing across different parts of the neocortex.
Apical dendrite
Pyramidal cell
Dendrite (mathematics)
Dendritic spike
Cite
Citations (11)
Journal Article Regenerative Activity in Apical Dendrites of Pyramidal Cells in Neocortex Get access Y. Amitai, Y. Amitai 1Unit of Physiology, Faculty of Health Sciences, Ben-Gurion University of the NegevBeer-Sheva 84105, Israel Search for other works by this author on: Oxford Academic PubMed Google Scholar A. Friedman, A. Friedman 1Unit of Physiology, Faculty of Health Sciences, Ben-Gurion University of the NegevBeer-Sheva 84105, Israel Search for other works by this author on: Oxford Academic PubMed Google Scholar B. W. Connors, B. W. Connors 2Department of Neuroscience, Brown UniversityProvidence, Rhode Island 02912 Search for other works by this author on: Oxford Academic PubMed Google Scholar M. J. Gutnick M. J. Gutnick 1Unit of Physiology, Faculty of Health Sciences, Ben-Gurion University of the NegevBeer-Sheva 84105, Israel Search for other works by this author on: Oxford Academic PubMed Google Scholar Cerebral Cortex, Volume 3, Issue 1, January 1993, Pages 26–38, https://doi.org/10.1093/cercor/3.1.26 Published: 01 January 1993
Neocortex
Apical dendrite
Pyramidal cell
Dendritic spike
Dendrite (mathematics)
Tuft
Cite
Citations (251)
Action potentials backpropagate into the dendritic trees of pyramidal neurons, reporting output activity to the sites of synaptic input and provoking long-lasting changes in synaptic strength. It is unclear how this retrograde signal is modified by neural network activity. Using whole-cell recordings from somata, apical trunks, and dendritic tuft branches of layer 2/3 pyramidal neurons in vivo , we show that network-driven subthreshold membrane depolarizations (“up states”) occur simultaneously throughout the apical dendritic tree. This spontaneous synaptic activity enhances action potential-evoked calcium influx into the distal apical dendrite by promoting action potential backpropagation. Hence, somatic feedback to the dendrites becomes stronger with increasing network activity.
Dendritic spike
Apical dendrite
Pyramidal cell
Neocortex
Barrel cortex
Dendrite (mathematics)
Dendritic filopodia
Biological neural network
Bursting
Subthreshold conduction
Cite
Citations (108)