scholarly journals Differences in sodium channel densities in the apical dendrites of pyramidal cells of the electrosensory lateral line lobe

2019 ◽  
Author(s):  
Sree I. Motipally ◽  
Kathryne M. Allen ◽  
Daniel K. Williamson ◽  
Gary Marsat
Keyword(s):  
Lateral Line ◽  
Pyramidal Cells ◽  
Receptor Expression ◽  
Weakly Electric Fish ◽  
Sk Channels ◽  
Voltage Gated ◽  
Channel Density ◽  
Lateral Segment ◽  
Medial Segment ◽  
Apical Dendrites

AbstractHeterogeneity of neural properties within a given neural class is ubiquitous in the nervous system and permits different sub-classes of neurons to specialize for specific purposes. This principle has been thoroughly investigated in the hindbrain of the weakly electric fish A. leptorhynchus in the primary electrosensory area, the Electrosensory Lateral Line lobe (ELL). The pyramidal cells that receive inputs from tuberous electroreceptors are organized in three maps in distinct segments of the ELL. The properties of these cells vary greatly across maps due to differences in connectivity, receptor expression, and ion channel composition. These cells are a seminal example of bursting neurons and their bursting dynamic relies on the presence of voltage-gated Na+ channels in the extensive apical dendrites of the superficial pyramidal cells. Other ion channels can affect burst generation and their expression varies across ELL neurons and segments. For example, SK channels cause hyperpolarizing after-potentials decreasing the likelihood of bursting, yet bursting propensity is similar across segments. We question whether the depolarizing mechanism that generates the bursts presents quantitative differences across segments that could counterbalance other differences having the opposite effect. Although their presence and role are established, the distribution and density of the apical dendrites’ Na+ channels have not been quantified and compared across ELL maps. Therefore, we test the hypothesis that Na+ channel density varies across segment by quantifying their distribution in the apical dendrites of immunolabeled ELL sections. We found the Na+ channels to be two-fold denser in the lateral segment than in the centro-medial segment, the centro-lateral segment being intermediate. Our results imply that this differential expression of voltage-gated Na+ channels could counterbalance or interact with other aspects of neuronal physiology that vary across segments (e.g. SK channels). We argue that burst coding of sensory signals, and the way the network regulates bursting, should be influenced by these variations in Na+ channel density.

Oscillatory and burst discharge in the apteronotid electrosensory lateral line lobe

1999 ◽  
Vol 202 (10) ◽  
pp. 1255-1265 ◽  
Author(s):  
R.W. Turner ◽  
L. Maler
Keyword(s):  
Feature Extraction ◽  
Lateral Line ◽  
Pyramidal Cell ◽  
Frequency Tuning ◽  
Pyramidal Cells ◽  
Weakly Electric Fish ◽  
Burst Discharge ◽  
Sensory Maps

Oscillatory and burst discharge is recognized as a key element of signal processing from the level of receptor to cortical output cells in most sensory systems. The relevance of this activity for electrosensory processing has become increasingly apparent for cells in the electrosensory lateral line lobe (ELL) of gymnotiform weakly electric fish. Burst discharge by ELL pyramidal cells can be recorded in vivo and has been directly associated with feature extraction of electrosensory input. In vivo recordings have also shown that pyramidal cells are differentially tuned to the frequency of amplitude modulations across three ELL topographic maps of electroreceptor distribution. Pyramidal cell recordings in vitro reveal two forms of oscillatory discharge with properties consistent with pyramidal cell frequency tuning in vivo. One is a slow oscillation of spike discharge arising from local circuit interactions that exhibits marked changes in several properties across the sensory maps. The second is a fast, intrinsic form of burst discharge that incorporates a newly recognized interaction between somatic and dendritic membranes. These findings suggest that a differential regulation of oscillatory discharge properties across sensory maps may underlie frequency tuning in the ELL and influence feature extraction in vivo.

Neural architecture of the electrosensory lateral line lobe: adaptations for coincidence detection, a sensory searchlight and frequency-dependent adaptive filtering

1999 ◽  
Vol 202 (10) ◽  
pp. 1243-1253 ◽  
Author(s):  
N.J. Berman ◽  
L. Maler
Keyword(s):  
Lateral Line ◽  
Activity Patterns ◽  
Pyramidal Cells ◽  
Coincidence Detection ◽  
Weakly Electric Fish ◽  
In Vivo Studies ◽  
Frequency Dependent ◽  
Postsynaptic Potentials

The electrosensory lateral line lobe (ELL) of weakly electric fish is the only nucleus that receives direct input from peripheral electroreceptor afferents. This review summarises the neurotransmitters, receptors and second messengers identified in the intrinsic circuitry of the ELL and the extrinsic descending direct and indirect feedback pathways, as revealed by recent in vitro and in vivo studies. Several hypotheses of circuitry function are examined on this basis and on the basis of recent functional evidence: (1) fast primary afferent excitatory postsynaptic potentials (EPSPs) and fast granule cell 2 GABAA inhibitory postsynaptic potentials (IPSPs) suggest the involvement of basilar pyramidal cells in coincidence detection; (2) voltage-dependent EPSPs and IPSPs, dendritic spike bursts and frequency-dependent synaptic facilitation support a sensory searchlight role for the direct feedback pathway; and (3) the contributions of distal and proximal inhibition, anti-Hebbian plasticity and beam versus isolated fiber activity patterns are discussed with reference to an adaptive spatio-temporal filtering role for the indirect descending pathway.

Dendritic Modulation of Burst-Like Firing in Sensory Neurons

2001 ◽  
Vol 85 (1) ◽  
pp. 10-22 ◽  
Author(s):  
Joseph Bastian ◽  
Jerry Nguyenkim
Keyword(s):  
Spike Train ◽  
Sensory Neurons ◽  
Lateral Line ◽  
Interspike Interval ◽  
Pyramidal Cells ◽  
Spike Trains ◽  
Firing Frequency ◽  
Dendritic Morphology ◽  
Spontaneous Firing ◽  
Apical Dendrites

This report describes the variability of spontaneous firing characteristics of sensory neurons, electrosensory lateral line lobe (ELL) pyramidal cells, within the electrosensory lateral line lobe of weakly electric fish in vivo. We show that these cells' spontaneous firing frequency, measures of spike train regularity (interspike interval coefficient of variation), and the tendency of these cells to produce bursts of action potentials are correlated with the size of the cell's apical dendritic arbor. We also show that bursting behavior may be influenced or controlled by descending inputs from higher centers that provide excitatory and inhibitory inputs to the pyramidal cells' apical dendrites. Pyramidal cells were classified as “bursty” or “nonbursty” according to whether or not spike trains deviated significantly from the expected properties of random (Poisson) spike trains of the same average firing frequency, and, in the case of bursty cells, the maximum within-burst interspike interval characteristic of bursts was determined. Each cell's probability of producing bursts above the level expected for a Poisson spike train was determined and related to spontaneous firing frequency and dendritic morphology. Pyramidal cells with large apical dendritic arbors have lower rates of spontaneous activity and higher probabilities of producing bursts above the expected level, while cells with smaller apical dendrites fire at higher frequencies and are less bursty. The effect of blocking non- N-methyl-d-aspartate (non-NMDA) glutamatergic synaptic inputs to the apical dendrites of these cells, and to local inhibitory interneurons, significantly reduced the spontaneous occurrence of spike bursts and intracellular injection of hyperpolarizing current mimicked this effect. The results suggest that bursty firing of ELL pyramidal cells may be under descending control allowing activity in electrosensory feedback pathways to influence the firing properties of sensory neurons early in the processing hierarchy.

scholarly journals Neuron Class and Target Variability in the Three-Dimensional Localization of SK2 Channels in Hippocampal Neurons as Detected by Immunogold FIB-SEM

2021 ◽  
Vol 15 ◽  
Author(s):  
Rafael Luján ◽  
Angel Merchán-Pérez ◽  
Joaquim Soriano ◽  
Alejandro Martín-Belmonte ◽  
Carolina Aguado ◽  
...  
Keyword(s):  
Hippocampal Neurons ◽  
Spatial Organization ◽  
Ion Beam ◽  
Pyramidal Cells ◽  
Inhibitory Neurons ◽  
Stratum Radiatum ◽  
Inhibitory Synapses ◽  
Sk Channels ◽  
Large Variability ◽  
Channel Density

Small-conductance calcium-activated potassium (SK) channels are crucial for learning and memory. However, many aspects of their spatial organization in neurons are still unknown. In this study, we have taken a novel approach to answering these questions combining a pre-embedding immunogold labeling with an automated dual-beam electron microscope that integrates focused ion beam milling and scanning electron microscopy (FIB/SEM) to gather 3D map ultrastructural and biomolecular information simultaneously. Using this new approach, we evaluated the number and variability in the density of extrasynaptic SK2 channels in 3D reconstructions from six dendritic segments of excitatory neurons and six inhibitory neurons present in the stratum radiatum of the CA1 region of the mouse. SK2 immunoparticles were observed throughout the surface of hippocampal neurons, either scattered or clustered, as well as at intracellular sites. Quantitative volumetric evaluations revealed that the extrasynaptic SK2 channel density in spines was seven times higher than in dendritic shafts and thirty-five times higher than in interneurons. Spines showed a heterogeneous population of SK2 expression, some spines having a high SK2 content, others having a low content and others lacking SK2 channels. SK2 immunonegative spines were significantly smaller than those immunopositive. These results show that SK2 channel density differs between excitatory and inhibitory neurons and demonstrates a large variability in the density of SK2 channels in spines. Furthermore, we demonstrated that SK2 expression was associated with excitatory synapses, but not with inhibitory synapses in CA1 pyramidal cells. Consequently, regulation of excitability and synaptic plasticity by SK2 channels is expected to be neuron class- and target-specific. These data show that immunogold FIB/SEM represent a new powerful EM tool to correlate structure and function of ion channels with nanoscale resolution.

scholarly journals A sodium-activated potassium channel supports high-frequency firing and reduces energetic costs during rapid modulations of action potential amplitude

2013 ◽  
Vol 109 (7) ◽  
pp. 1713-1723 ◽  
Author(s):  
Michael R. Markham ◽  
Leonard K. Kaczmarek ◽  
Harold H. Zakon
Keyword(s):  
Action Potential ◽  
High Frequency ◽  
Electric Fish ◽  
Electric Organ Discharge ◽  
Electric Organ ◽  
Weakly Electric Fish ◽  
Energetic Costs ◽  
Dynamic Regulation ◽  
Voltage Gated

We investigated the ionic mechanisms that allow dynamic regulation of action potential (AP) amplitude as a means of regulating energetic costs of AP signaling. Weakly electric fish generate an electric organ discharge (EOD) by summing the APs of their electric organ cells (electrocytes). Some electric fish increase AP amplitude during active periods or social interactions and decrease AP amplitude when inactive, regulated by melanocortin peptide hormones. This modulates signal amplitude and conserves energy. The gymnotiform Eigenmannia virescens generates EODs at frequencies that can exceed 500 Hz, which is energetically challenging. We examined how E. virescens meets that challenge. E. virescens electrocytes exhibit a voltage-gated Na+current ( INa) with extremely rapid recovery from inactivation (τrecov= 0.3 ms) allowing complete recovery of Na+current between APs even in fish with the highest EOD frequencies. Electrocytes also possess an inwardly rectifying K+current and a Na+-activated K+current ( IKNa), the latter not yet identified in any gymnotiform species. In vitro application of melanocortins increases electrocyte AP amplitude and the magnitudes of all three currents, but increased IKNais a function of enhanced Na+influx. Numerical simulations suggest that changing INamagnitude produces corresponding changes in AP amplitude and that KNachannels increase AP energy efficiency (10–30% less Na+influx/AP) over model cells with only voltage-gated K+channels. These findings suggest the possibility that E. virescens reduces the energetic demands of high-frequency APs through rapidly recovering Na+channels and the novel use of KNachannels to maximize AP amplitude at a given Na+conductance.

scholarly journals Developmental regulation of voltage-gated K+ channel and GABAA receptor expression in Bergmann glial cells

1994 ◽  
Vol 14 (5) ◽  
pp. 2503-2514 ◽  
Author(s):  
T Muller ◽  
JM Fritschy ◽  
J Grosche ◽  
GD Pratt ◽  
H Mohler ◽  
...  
Keyword(s):  
Gabaa Receptor ◽  
Glial Cells ◽  
Developmental Regulation ◽  
Receptor Expression ◽  
K Channel ◽  
Voltage Gated ◽  
Bergmann Glial Cells

scholarly journals Cell-type specific innervation of cortical pyramidal cells at their apical dendrites

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Ali Karimi ◽  
Jan Odenthal ◽  
Florian Drawitsch ◽  
Kevin M Boergens ◽  
Moritz Helmstaedter
Keyword(s):  
Electron Microscopy ◽  
Pyramidal Cells ◽  
Inhibitory Input ◽  
Cell Type ◽  
Cell Type Specific ◽  
Cortical Regions ◽  
Apical Dendrites ◽  
Computational Properties

We investigated the synaptic innervation of apical dendrites of cortical pyramidal cells in a region between layers (L) 1 and 2 using 3-D electron microscopy applied to four cortical regions in mouse. We found the relative inhibitory input at the apical dendrite’s main bifurcation to be more than 2-fold larger for L2 than L3 and L5 thick-tufted pyramidal cells. Towards the distal tuft dendrites in upper L1, the relative inhibitory input was at least about 2-fold larger for L5 pyramidal cells than for all others. Only L3 pyramidal cells showed homogeneous inhibitory input fraction. The inhibitory-to-excitatory synaptic ratio is thus specific for the types of pyramidal cells. Inhibitory axons preferentially innervated either L2 or L3/5 apical dendrites, but not both. These findings describe connectomic principles for the control of pyramidal cells at their apical dendrites and support differential computational properties of L2, L3 and subtypes of L5 pyramidal cells in cortex.

A unitary hypothesis of mind-brain interaction in the cerebral cortex

1990 ◽  
Vol 240 (1299) ◽  
pp. 433-451 ◽  
Keyword(s):  
Cerebral Cortex ◽  
Pyramidal Cells ◽  
Neuronal Structure ◽  
Mental Experience ◽  
Effective Selection ◽  
Global Nature ◽  
The Mind ◽  
Mental Events ◽  
Apical Dendrites ◽  
The Brain

A brief introduction to the brain-mind problem leads on to a survey of the neuronal structure of the cerebral cortex. It is proposed that the basic receptive units are the bundles or clusters of apical dendrites of the pyramidal cells of laminae V and III-II as described by Fleischhauer and Peters and their associates. There are up to 100 apical dendrites in these receptive units, named dendrons. Each dendron would have an input of up to 100000 spine synapses. There are about 40 million dendrons in the human cerebral cortex. A study of the influence of mental events on the brain leads to the hypothesis that all mental events, the whole of the World 2 of Popper, are composed of mental units, each carrying its own characteristic mental experience. It is further proposed that each mental unit, named psychon, is uniquely linked to a dendron. So the mind-brain problem reduces to the interaction between a dendron and its psychon for all the 40 million linked units. In my 1986 paper ( Proc. R. Soc. Lond . B 227, 411-428) on the mind-brain problem, there was developed the concept that the operation of the synaptic microsites involved displacement of particles so small that they were within range of the uncertainty principle of Heisenberg. The psychon-dendron interaction provides a much improved basis for effective selection by a process analogous to a quantal probability field. In the fully developed hypothesis psychons act on dendrons in the whole world of conscious experiences and dendrons act on psychons in all perceptions and memories. It is shown how these interactions involve no violation of the conservation laws. There are great potentialities of these unitary concepts, for example as an explanation of the global nature of a visual experience from moment to moment. It would seem that there can be psychons not linked to dendrons, but only to other psychons, creating what we may call a psychon world.

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