Active propagation of somatic action potentials into neocortical pyramidal cell dendrites

Nature ◽  
1994 ◽  
Vol 367 (6458) ◽  
pp. 69-72 ◽  
Author(s):  
Greg J. Stuart ◽  
Bert Sakmann
1983 ◽  
Vol 50 (5) ◽  
pp. 1197-1219 ◽  
Author(s):  
T. W. Berger ◽  
P. C. Rinaldi ◽  
D. J. Weisz ◽  
R. F. Thompson

Extracellular single-unit recordings from neurons in the CA1 and CA3 regions of the dorsal hippocampus were monitored during classical conditioning of the rabbit nictitating membrane response. Neurons were classified as different cell types using response to fornix stimulation (i.e., antidromic or orthodromic activation) and spontaneous firing characteristics as criteria. Results showed that hippocampal pyramidal neurons exhibit learning-related neural plasticity that develops gradually over the course of classical conditioning. The learning-dependent pyramidal cell response is characterized by an increase in frequency of firing within conditioning trials and a within-trial pattern of discharge that correlates strongly with amplitude-time course of the behavioral response. In contrast, pyramidal cell activity recorded from control animals given unpaired presentations of the conditioned and unconditioned stimulus (CS and UCS) does not show enhanced discharge rates with repeated stimulation. Previous studies of hippocampal cellular electrophysiology have described what has been termed a theta-cell (19-21, 45), the activity of which correlates with slow-wave theta rhythm generated in the hippocampus. Neurons classified as theta-cells in the present study exhibit responses during conditioning that are distinctly different than pyramidal cells. theta-Cells respond during paired conditioning trials with a rhythmic bursting; the between-burst interval occurs at or near 8 Hz. In addition, two different types of theta-cells were distinguishable. One type of theta-cell increases firing frequency above pretrial levels while displaying the theta bursting pattern. The other type decreases firing frequency below pretrial rates while showing a theta-locked discharge. In addition to pyramidal and theta-neurons, several other cell types recorded in or near the pyramidal cell layer could be distinguished. One cell type was distinctive in that it could be activated with a short, invariant latency following fornix stimulation, but spontaneous action potentials of such neurons could not be collided with fornix shock-induced action potentials. These neurons exhibit a different profile of spontaneous firing characteristics than those of antidromically identified pyramidal cells. Nevertheless, neurons in this noncollidable category display the same learning-dependent response as pyramidal cells. It is suggested that the noncollidable neurons represent a subpopulation of pyramidal cells that do not project an axon via the fornix but project, instead, to other limbic cortical regions.(ABSTRACT TRUNCATED AT 400 WORDS)


1994 ◽  
Vol 72 (5) ◽  
pp. 2167-2180 ◽  
Author(s):  
H. E. Scharfman

1. Simultaneous intracellular recordings of area CA3 pyramidal cells and dentate hilar “mossy” cells were made in rat hippocampal slices to test the hypothesis that area CA3 pyramidal cells excite mossy cells monosynaptically. Mossy cells and pyramidal cells were differentiated by location and electrophysiological characteristics. When cells were impaled near the border of area CA3 and the hilus, their identity was confirmed morphologically after injection of the marker Neurobiotin. 2. Evidence for monosynaptic excitation of a mossy cell by a pyramidal cell was obtained in 7 of 481 (1.4%) paired recordings. In these cases, a pyramidal cell action potential was followed immediately by a 0.40 to 6.75 (mean, 2.26) mV depolarization in the simultaneously recorded mossy cell (mossy cell membrane potentials, -60 to -70 mV). Given that pyramidal cells used an excitatory amino acid as a neurotransmitter (Cotman and Nadler 1987; Ottersen and Storm-Mathisen 1987) and recordings were made in the presence of the GABAA receptor antagonist bicuculline (25 microM), it is likely that the depolarizations were unitary excitatory postsynaptic potentials (EPSPs). 3. Unitary EPSPs of mossy cells were prone to apparent “failure.” The probability of failure was extremely high (up to 0.72; mean = 0.48) if the effects of all presynaptic action potentials were examined, including action potentials triggered inadvertently during other spontaneous EPSPs of the mossy cell. Probability of failure was relatively low (as low as 0; mean = 0.24) if action potentials that occurred during spontaneous activity of the mossy cell were excluded. These data suggest that unitary EPSPs produced by pyramidal cells are strongly affected by concurrent synaptic inputs to the mossy cell. 4. Unitary EPSPs were not clearly affected by manipulation of the mossy cell's membrane potential. This is consistent with the recent report that area CA3 pyramidal cells innervate distal dendrites of mossy cells (Kunkel et al. 1993). Such a distal location also may contribute to the high incidence of apparent failures. 5. Characteristics of unitary EPSPs generated by pyramidal cells were compared with the properties of the unitary EPSPs produced by granule cells. In two slices, pyramidal cell and granule cell inputs to the same mossy cell were compared. In other slices, inputs to different mossy cells were compared. In all experiments, unitary EPSPs produced by granule cells were larger in amplitude but similar in time course to unitary EPSPs produced by pyramidal cells. Probability of failure was lower and paired-pulse facilitation more common among EPSPs triggered by granule cells.(ABSTRACT TRUNCATED AT 400 WORDS)


1999 ◽  
Vol 81 (3) ◽  
pp. 1412-1417 ◽  
Author(s):  
Toby J. Velte ◽  
Richard H. Masland

Action potentials in the dendrites of retinal ganglion cells. The somas and dendrites of intact retinal ganglion cells were exposed by enzymatic removal of the overlying endfeet of the Müller glia. Simultaneous whole cell patch recordings were made from a ganglion cell’s dendrite and the cell’s soma. When a dendrite was stimulated with depolarizing current, impulses often propagated to the soma, where they appeared as a mixture of small depolarizations and action potentials. When the soma was stimulated, action potentials always propagated back through the dendrite. The site of initiation of action potentials, as judged by their timing, could be shifted between soma and dendrite by changing the site of stimulation. Applying QX-314 to the soma could eliminate somatic action potentials while leaving dendritic impulses intact. The absolute amplitudes of the dendritic action potentials varied somewhat at different distances from the soma, and it is not clear whether these variations are real or technical. Nonetheless, the qualitative experiments clearly suggest that the dendrites of retinal ganglion cells generate regenerative Na+ action potentials, at least in response to large direct depolarizations.


1984 ◽  
Vol 52 (1) ◽  
pp. 126-142 ◽  
Author(s):  
C. P. Taylor ◽  
F. E. Dudek

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.


2015 ◽  
Vol 61 (1) ◽  
pp. 15-24 ◽  
Author(s):  
Júlia Metz ◽  
T. Szilágyi ◽  
M. Perian ◽  
K. Orbán-Kis

Abstract Objective. In silico experiments use mathematical models that capture as much as possible from the properties of the biological system under investigation. Our aim was to test the publicly available CA1 pyramidal cell models using the same simulation tasks, to compare them, and provide a systematic overview of their properties in order to improve the usefulness of these models as a tool for in silico experiments. Methods. Parameters describing the morphology of the cells and the implemented biophysical mechanisms were collected from the Model DB database of Sense Lab Project. This data was analyzed in correlation with the purpose for which each particular model was developed. Multicompartmental simulations were run using the Neuron modeling platform. The properties of the action potentials generated in response to current injection, the firing pattern and the dendritic back-propagation were analyzed. Results. The studied models were optimized to explore different physiological and pathological properties of the CA1 pyramidal cells. We could identify four broad classes of models focusing on: (i) initiation of the action potential, firing pattern and spike timing, (ii) dendritic backpropagation, (iii) dendritic integration of synaptic inputs and (iv) neuronal network activity. Despite the large variation of the active conductances implemented in the models, the properties of the individual action potentials were quite similar, but even the most complex models could not reproduce all studied biological phenomena. Conclusions. At the moment the “perfect” pyramidal cell model is not yet available. Our work, hopefully, will help finding the best model for each scientific question under investigation.


2021 ◽  
Author(s):  
Jung Ho Hyun ◽  
Kenichiro Nagahama ◽  
Ho Namkung ◽  
Neymi Mignocchi ◽  
Patrick Hannan ◽  
...  

Verifying causal effects of neural circuits is essential for proving direct a circuit-behavior relationship. However, techniques for tagging only active neurons with high spatiotemporal precision remain at the beginning stages. Here we developed the soma-targeted Cal-Light (ST-Cal-Light) which selectively converts somatic calcium rise triggered by action potentials into gene expression. Such modification simultaneously increases the signal-to-noise ratio (SNR) of reporter gene expression and reduces the light requirement for successful labeling. Because of the enhanced efficacy, the ST-Cal-Light enables the tagging of functionally engaged neurons in various forms of behaviors, including context-dependent fear conditioning, lever-pressing choice behavior, and social interaction behaviors. We also targeted kainic acid-sensitive neuronal populations in the hippocampus which subsequently suppressed seizure symptoms, suggesting its applicability in controlling disease-related neurons. Furthermore, the generation of a conditional ST-Cal-Light knock-in (KI) mouse provides an opportunity to tag active neurons in a region- or cell-type specific manner via crossing with other Cre-driver lines. Thus, the versatile ST-Cal-Light system links somatic action potentials to behaviors with high temporal precision, and ultimately allows functional circuit dissection at a single cell resolution.


F1000Research ◽  
2017 ◽  
Vol 5 ◽  
pp. 1945 ◽  
Author(s):  
Hyeon Seo ◽  
Natalie Schaworonkow ◽  
Sung Chan Jun ◽  
Jochen Triesch

The detailed biophysical mechanisms through which transcranial magnetic stimulation (TMS) activates cortical circuits are still not fully understood. Here we present a multi-scale computational model to describe and explain the activation of different pyramidal cell types in motor cortex due to TMS. Our model determines precise electric fields based on an individual head model derived from magnetic resonance imaging and calculates how these electric fields activate morphologically detailed models of different neuron types. We predict neural activation patterns for different coil orientations consistent with experimental findings. Beyond this, our model allows us to calculate activation thresholds for individual neurons and precise initiation sites of individual action potentials on the neurons’ complex morphologies. Specifically, our model predicts that cortical layer 3 pyramidal neurons are generally easier to stimulate than layer 5 pyramidal neurons, thereby explaining the lower stimulation thresholds observed for I-waves compared to D-waves. It also shows differences in the regions of activated cortical layer 5 and layer 3 pyramidal cells depending on coil orientation. Finally, it predicts that under standard stimulation conditions, action potentials are mostly generated at the axon initial segment of cortical pyramidal cells, with a much less important activation site being the part of a layer 5 pyramidal cell axon where it crosses the boundary between grey matter and white matter. In conclusion, our computational model offers a detailed account of the mechanisms through which TMS activates different cortical pyramidal cell types, paving the way for more targeted application of TMS based on individual brain morphology in clinical and basic research settings.


2012 ◽  
Vol 107 (10) ◽  
pp. 2833-2852 ◽  
Author(s):  
Erin Munro ◽  
Nancy Kopell

There is suggestive evidence that pyramidal cell axons in neocortex may be coupled by gap junctions into an “axonal plexus” capable of generating very fast oscillations (VFOs) with frequencies exceeding 80 Hz. It is not obvious, however, how a pyramidal cell in such a network could control its output when action potentials are free to propagate from the axons of other pyramidal cells into its own axon. We address this problem by means of simulations based on three-dimensional reconstructions of pyramidal cells from rat somatosensory cortex. We show that somatic depolarization enables propagation via gap junctions into the initial segment and main axon, while somatic hyperpolarization disables it. We show further that somatic voltage cannot effectively control action potential propagation through gap junctions on minor collaterals; action potentials may therefore propagate freely from such collaterals regardless of somatic voltage. In previous work, VFOs are all but abolished during the hyperpolarization phase of slow oscillations induced by anesthesia in vivo. This finding constrains the density of gap junctions on collaterals in our model and suggests that axonal sprouting due to cortical lesions may result in abnormally high gap junction density on collaterals, leading in turn to excessive VFO activity and hence to epilepsy via kindling.


1995 ◽  
Vol 73 (6) ◽  
pp. 2553-2557 ◽  
Author(s):  
B. R. Christie ◽  
L. S. Eliot ◽  
K. Ito ◽  
H. Miyakawa ◽  
D. Johnston

1. Intracellular recordings, in conjunction with fura-2 fluorescence imaging, were used to evaluate the contribution of the different Ca2+ channel subtypes to the Ca2+ influx induced by back-propagating trains of action potentials. High-threshold channels contributed mainly to Ca2+ influx in pyramidal cell somata and proximal dendrites, whereas low-threshold and other Ni(2+)-sensitive channels played a greater role in more distal dendritic signaling. These data suggest that the different Ca2+ channel types participate in distinct physiological functions; low-threshold channels likely play a greater role in dendritic integration, whereas high-threshold channels are more important for somatic Ca(2+)-dependent processes.


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