Turtle hippocampal cortex contains distinct cell types, burst-firing neurons, and an epileptogenic subfield

1986 ◽  
Vol 56 (6) ◽  
pp. 1626-1649 ◽  
Author(s):  
J. M. Shen ◽  
A. R. Kriegstein
Keyword(s):  
Cortical Neurons ◽  
Lucifer Yellow ◽  
Molecular Layer ◽  
Pyramidal Cells ◽  
Stellate Cells ◽  
Cortical Region ◽  
Synaptic Response ◽  
Frequency Adaptation ◽  
Medial Cortex ◽  
Physiological Properties

The dorsal and medial telencephalon of reptiles consists of a simple trilaminar cortex. The turtle dorsal cortex has been identified as a favorable physiological preparation that may bear a phylogenetic relationship to mammalian neocortex. While anatomical studies have likened the reptilian medial cortical region to mammalian hippocampus, its physiological properties have not been explored. We therefore used intracellular and extracellular recording techniques to examine the cellular and synaptic physiology of turtle "hippocampal" or medial cortex. Turtle medial cortex contains two principal classes of neurons, pyramidal cells and stellate neurons. Recordings with Lucifer yellow CH (LY)-filled microelectrodes allowed us to correlate the physiological properties of medial cortical neurons with their cellular morphology. Pyramidal neurons were situated in a single cellular layer and had spiny apical dendrites extending into the molecular layer. These cells fired relatively long-duration action potentials (APs) and showed frequency adaptation to suprathreshold current pulse injections. Stellate cells were usually found in the subcellular and molecular layers and had aspiny dendrites. In contrast to pyramidal cells, they fired brief APs and displayed no frequency adaptation. A discrete population of cells in the dorsal portion of medial cortex (DMC) was capable of bursting endogenously or in response to synaptic activation. Bursts usually contained an underlying slow depolarization and often occurred at regular intervals. Intracellular LY injections confirmed that these cells were pyramidal in morphology. Electrical stimulation of afferent fibers revealed that pyramidal cells and stellate neurons differed in their synaptic responses. In ventral medial cortex (VMC), afferent stimulation evoked a multiphasic response in most pyramidal cells, whereas stellate cells were synaptically excited. Orthodromic activation of DMC bursting cells resulted in a powerful excitation--often a short burst--and subsequent inhibition. Stellate neurons in DMC also had a biphasic synaptic response consisting of both an early excitation and a late inhibition. Experiments using intracellular chloride (Cl-) injection or focal bicuculline application suggested that part of the inhibitory component of the pyramidal cell synaptic response was dependent on a gamma-aminobutyric acid (GABA)-mediated increase in Cl- conductance. These results correlated with our immunohistochemical studies that revealed the presence of GABAergic neurons in medial cortex.(ABSTRACT TRUNCATED AT 400 WORDS)

Distal Versus Proximal Inhibitory Shaping of Feedback Excitation in the Electrosensory Lateral Line Lobe: Implications for Sensory Filtering

1998 ◽  
Vol 80 (6) ◽  
pp. 3214-3232 ◽  
Author(s):  
Neil J. Berman ◽  
Leonard Maler
Keyword(s):  
Lateral Line ◽  
Pyramidal Cell ◽  
Stellate Cell ◽  
Molecular Layer ◽  
Pyramidal Cells ◽  
Stellate Cells ◽  
Decay Phase ◽  
Tetanic Stimulation ◽  
Parallel Fibers ◽  
Cell Inhibition

Berman, Neil J. and Leonard Maler. Distal versus proximal inhibitory shaping of feedback excitation in the electrosensory lateral line lobe: implications for sensory filtering. J. Neurophysiol. 80: 3214–3232, 1998. The inhibition controlling the indirect descending feedback (parallel fibers originating from cerebellar granule cells in the eminentia posterior pars granularis) to electrosensory lateral line lobe (ELL) pyramidal cells was studied using intracellular recording techniques in vitro. Parallel fibers (PF) contact stellate cells and dendrites of ventral molecular layer (VML) GABAergic interneurons. Stellate cells provide local input to pyramidal cell distal dendrites, whereas VML cells contact their somata and proximal dendrites. Single-pulse stimulation of PF evoked graded excitatory postsynaptic potentials (EPSPs) that were blocked by α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid and N-methyl-d-aspartate (NMDA) antagonists. The EPSPs peaked at 6.4 ± 1.8 ms (mean ± SE; n = 11) but took >50 ms to decay completely. Tetanic stimulation (100 ms, 100 Hz) produced a depolarizing wave with individual EPSPs superimposed. The absolute amplitude of the individual EPSPs decreased during the train. Spike rates, established by injected current, mostly were increased, but in some cells were decreased, by tetanic stimulation. Global application of a γ-aminobutyric acid-A (GABAA) antagonist to the recorded cell's soma and apical dendritic region increased the EPSP peak and decay phase amplitudes. Tetanic stimulation always increased current-evoked spike rates after GABAA blockade during, and for several hundred milliseconds after, the stimulus. Application of a GABAB antagonist did not have any significant effects on the PF-evoked response. This, and the lack of any long hyperpolarizing inhibitory postsynaptic potentials, suggests that VML and stellate cell inhibition does not involve GABAB receptors. Focal GABAA antagonist applications to the dorsal molecular layer (DML) and pyramidal cell layer (PCL) had contrasting effects on PF-evoked EPSPs. DML GABAA blockade significantly increased the EPSP peak amplitude but not the decay phase of the EPSP, whereas PCL GABAA-blockade significantly increased the decay phase, but not the EPSP peak, amplitude. The order of antagonist application did not affect the outcome. On the basis of the known circuitry of the ELL, we conclude that the distal inhibition originated from GABAergic molecular layer stellate cells and the proximal inhibition originated from GABAergic cells of the ventral molecular layer (VML cells). Computer modeling of distal and proximal inhibition suggests that intrinsic differences in IPSP dynamics between the distal and proximal sites may be amplified by voltage-dependent NMDA receptor and persistent sodium currents. We propose that the different time courses of stellate cell and VML cell inhibition allows them to act as low- and high-pass filters respectively on indirect descending feedback to ELL pyramidal cells.

scholarly journals Alzheimer’s disease brain-derived tau-containing extracellular vesicles: Pathobiology and GABAergic neuronal transmission

2020 ◽  
Author(s):  
Zhi Ruan ◽  
Dhruba Pathak ◽  
Srinidhi Venkatesan Kalavai ◽  
Asuka Yoshii-Kitahara ◽  
Satoshi Muraoka ◽  
...  
Keyword(s):  
Alzheimer’S Disease ◽  
Alzheimer's Disease ◽  
Extracellular Vesicles ◽  
Cortical Neurons ◽  
Pyramidal Neurons ◽  
Molecular Layer ◽  
Pyramidal Cells ◽  
Gabaergic Neurons ◽  
Dot Blot ◽  
Patch Clamp Recording

AbstractExtracellular vesicles (EVs) propagate tau pathology for Alzheimer’s disease (AD). How EV transmission influences AD are, nonetheless, poorly understood. To these ends, the physicochemical and molecular structure-function relationships of human brain-derived EVs, from AD and prodromal AD (pAD), were compared to non-demented controls (CTRL). AD EVs were shown to be significantly enriched in epitope-specific tau oligomers versus pAD or CTRL EVs assayed by dot-blot and atomic force microscopy tests. AD EVs were efficiently internalized by murine cortical neurons and transferred tau with higher aggregation potency than pAD and CTRL EVs. Strikingly, inoculation of tau-containing AD EVs into the outer molecular layer of the dentate gyrus induced tau propagation throughout the hippocampus. This was seen in 22 months-old C57BL/6 mice at 4.5 months post-injection by semiquantitative brain-wide immunohistochemistry tests with multiple anti-phospho-tau (p-tau) antibodies. Inoculation of the equal amount of tau from CTRL EVs or as oligomer or fibril-enriched fraction from the same AD donor showed little propagation. AD EVs induced tau accumulation in the hippocampus as oligomers or sarkosyl-insoluble proteins. Unexpectedly, p-tau cells were mostly GAD67+ GABAergic neurons and to a lesser extent, GluR2/3+ excitatory mossy cells, showing preferential EV-mediated GABAergic neuronal tau propagation. Whole-cell patch clamp recording of Cornu Ammonis (CA1) pyramidal cells showed significant reduction in the amplitude of spontaneous inhibitory post-synaptic currents. This was accompanied by reductions in c-fos+ GAD67+GABAergic neurons and GAD67+ GABAergic neuronal puncta surrounding pyramidal neurons in the CA1 region confirming reduced interneuronal projections. Our study posits a novel tau-associated pathological mechanism for brain-derived EVs.

scholarly journals Stellate cell computational modeling predicts signal filtering in the molecular layer circuit of cerebellum

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Martina Francesca Rizza ◽  
Francesca Locatelli ◽  
Stefano Masoli ◽  
Diana Sánchez-Ponce ◽  
Alberto Muñoz ◽  
...  
Keyword(s):  
Purkinje Cell ◽  
Stellate Cell ◽  
Molecular Layer ◽  
Stellate Cells ◽  
Parallel Fiber ◽  
Cell Discharge ◽  
Physiological Properties ◽  
Low Pass ◽  
Band Pass ◽  
Very High Frequencies

AbstractThe functional properties of cerebellar stellate cells and the way they regulate molecular layer activity are still unclear. We have measured stellate cells electroresponsiveness and their activation by parallel fiber bursts. Stellate cells showed intrinsic pacemaking, along with characteristic responses to depolarization and hyperpolarization, and showed a marked short-term facilitation during repetitive parallel fiber transmission. Spikes were emitted after a lag and only at high frequency, making stellate cells to operate as delay-high-pass filters. A detailed computational model summarizing these physiological properties allowed to explore different functional configurations of the parallel fiber—stellate cell—Purkinje cell circuit. Simulations showed that, following parallel fiber stimulation, Purkinje cells almost linearly increased their response with input frequency, but such an increase was inhibited by stellate cells, which leveled the Purkinje cell gain curve to its 4 Hz value. When reciprocal inhibitory connections between stellate cells were activated, the control of stellate cells over Purkinje cell discharge was maintained only at very high frequencies. These simulations thus predict a new role for stellate cells, which could endow the molecular layer with low-pass and band-pass filtering properties regulating Purkinje cell gain and, along with this, also burst delay and the burst-pause responses pattern.

Electrophysiological Classes of Cat Primary Visual Cortical Neurons In Vivo as Revealed by Quantitative Analyses

2003 ◽  
Vol 89 (3) ◽  
pp. 1541-1566 ◽  
Author(s):  
Lionel G. Nowak ◽  
Rony Azouz ◽  
Maria V. Sanchez-Vives ◽  
Charles M. Gray ◽  
David A. McCormick
Keyword(s):  
Short Duration ◽  
Cortical Neurons ◽  
Action Potentials ◽  
Low Frequency ◽  
Pyramidal Cells ◽  
Spike Frequency ◽  
Spike Frequency Adaptation ◽  
Frequency Adaptation ◽  
Layer 4

To facilitate the characterization of cortical neuronal function, the responses of cells in cat area 17 to intracellular injection of current pulses were quantitatively analyzed. A variety of response variables were used to separate the cells into subtypes using cluster analysis. Four main classes of neurons could be clearly distinguished: regular spiking (RS), fast spiking (FS), intrinsic bursting (IB), and chattering (CH). Each of these contained significant subclasses. RS neurons were characterized by trains of action potentials that exhibited spike frequency adaptation. Morphologically, these cells were spiny stellate cells in layer 4 and pyramidal cells in layers 2, 3, 5, and 6. FS neurons had short-duration action potentials (<0.5 ms at half height), little or no spike frequency adaptation, and a steep relationship between injected current intensity and spike discharge frequency. Morphologically, these cells were sparsely spiny or aspiny nonpyramidal cells. IB neurons typically generated a low frequency (<425 Hz) burst of spikes at the beginning of a depolarizing current pulse followed by a tonic train of action potentials for the remainder of the pulse. These cells were observed in all cortical layers, but were most abundant in layer 5. Finally, CH neurons generated repetitive, high-frequency (350–700 Hz) bursts of short-duration (<0.55 ms) action potentials. Morphologically, these cells were layer 2–4 (mainly layer 3) pyramidal or spiny stellate neurons. These results indicate that firing properties do not form a continuum and that cortical neurons are members of distinct electrophysiological classes and subclasses.

scholarly journals Stellate cell computational modelling predicts signal filtering in the molecular layer circuit of cerebellum

2020 ◽  
Author(s):  
Martina Francesca Rizza ◽  
Francesca Locatelli ◽  
Stefano Masoli ◽  
Diana Sánchez Ponce ◽  
Alberto Muñoz ◽  
...  
Keyword(s):  
Purkinje Cell ◽  
Stellate Cell ◽  
Molecular Layer ◽  
Computational Modelling ◽  
Stellate Cells ◽  
Parallel Fiber ◽  
Cell Discharge ◽  
Physiological Properties ◽  
Low Pass ◽  
Very High Frequencies

AbstractThe functional properties of cerebellar stellate cells and the way they regulate molecular layer activity are still unclear. We have measured stellate cells electroresponsiveness and their activation by parallel fiber bursts. Stellate cells showed intrinsic pacemaking, along with characteristic responses to depolarization and hyperpolarization, and showed a marked short-term facilitation during repetitive parallel fiber transmission. Spikes were emitted after a lag and only at high frequency, making stellate cells to operate as delay-high-pass filters. A detailed computational model summarizing these physiological properties allowed to explore different functional configurations of the parallel fiber – stellate cell – Purkinje cell circuit. Simulations showed that, following parallel fiber stimulation, Purkinje cells almost linearly increased their response with input frequency but such an increase was inhibited by stellate cells, which leveled the Purkinje cell gain curve to its 4 Hz value. When reciprocal inhibitory connections between stellate cells were activated, the control of stellate cells over Purkinje cell discharge was maintained only at very high frequencies. These simulations thus predict a new role for stellate cells, which could endow the molecular layer with low-pass and band-pass filtering properties regulating Purkinje cell gain and, along with this, also burst delay and the burst-pause responses pattern.

A study of the axon initial segment and proximal axon of neurons in the primate motor and somatic sensory cortices

1979 ◽  
Vol 285 (1006) ◽  
pp. 173-197 ◽  
Keyword(s):  
Initial Segment ◽  
Pyramidal Cells ◽  
Stellate Cells ◽  
Myelinated Axon ◽  
Full Length ◽  
Unmyelinated Axon ◽  
Parent Cell ◽  
Axon Terminals ◽  
Sensory Cortices ◽  
Axon Initial Segments

The axon initial segments of pyramidal cells and large and small stellate cells in the primate sensori-motor cortex have a typical membrane undercoating and bundles of neurotubules. Those of pyramidal cells are directed towards the white matter whereas those of large and small stellate cells often run obliquely or towards the cortical surface and may be curved. Cisternal organs in these initial segments are related to symmetrical axon terminals, frequently coming into close apposition to the non-synaptic part of these terminals adjacent to the synapse between the axon terminal and initial segment. The dense plates of cisternal organs and the membrane undercoating of the initial segment are specifically stained by ethanolic phosphotungstic acid (ethanolic PTA). Pyramidal initial segments have spines which receive only symmetrical synapses, as do the shafts of the initial segments of each cell type. The full length of the initial segment was studied for fourteen pyramidal and two large stellate cells. All gave rise to myelinated axons although two pyramidal cells had lengths of unmyelinated axon between the initial segment and myelinated axon. One of these lengths of unmyelinated axon made an asymmetric synapse on to a dendrite just after losing its initial segment features. Quantitative analysis of these complete initial segments showed that whereas the diameter of the initial segment and the axon it gave rise to were approximately proportional to the size of the parent cell soma over a considerable range of cell diameters, the length of the initial segment appeared to be unrelated to either its diameter or the size of its parent soma but varied between 30 and 55 μm apparently at random. Synapses were evenly distributed along the full length of the complete pyramidal initial segments, but the density of synapses on the initial segments of supragranular pyramids was about three times that on those of infragranular pyramids and cisternal organs were similarly more frequent in the initial segments of supragranular pyramids.

Gustatory neural coding in the monkey cortex: stimulus quality

1991 ◽  
Vol 66 (4) ◽  
pp. 1156-1165 ◽  
Author(s):  
V. L. Smith-Swintosky ◽  
C. R. Plata-Salaman ◽  
T. R. Scott
Keyword(s):  
Cortical Neurons ◽  
Neural Coding ◽  
Monosodium Glutamate ◽  
Stimulus Array ◽  
Cortical Region ◽  
Stimulus Similarity ◽  
Somatosensory Stimulation ◽  
Wide Range ◽  
Response Profiles ◽  
Stimulation Of

1. Extracellular action potentials were recorded from 50 single neurons in the insular-opercular cortex of two alert cynomolgus monkeys during gustatory stimulation of the tongue and palate. 2. Sixteen stimuli, including salts, sugars, acids, alkaloids, monosodium glutamate, and aspartame, were chosen to represent a wide range of taste qualities. Concentrations were selected to elicit a moderate gustatory response, as determined by reference to previous electrophysiological data or to the human psychophysical literature. 3. The cortical region over which taste-evoked activity could be recorded included the frontal operculum and anterior insula, an area of approximately 75 mm3. Taste-responsive cells constituted 50 (2.7%) of the 1,863 neurons tested. Nongustatory cells responded to mouth movement (20.7%), somatosensory stimulation of the tongue (9.6%), stimulus approach or anticipation (1.7%), and tongue extension (0.6%). The sensitivities of 64.6% of these cortical neurons could not be identified by our stimulation techniques. 4. Taste cells had low spontaneous activity levels (3.7 +/- 3.0 spikes/s, mean +/- SD) and showed little inhibition. They were moderately broadly tuned, with a mean entropy coefficient of 0.76 +/- 0.17. Excitatory responses were typically not robust. 5. Hierarchical cluster analysis was used to determine whether neurons could be divided into discrete types, as defined by their response profiles to the entire stimulus array. There was an apparent division of response profiles into four general categories, with primary sensitivities to sodium (n = 18), glucose (n = 15), quinine (n = 12), and acid (n = 5). However, these categories were not statistically independent. Therefore the notion of functionally distinct neuron types was not supported by an analysis of the distribution of response profiles. It was the case, however, that neurons in the sodium category could be distinguished from other neurons by their relative specificity. 6. The similarity among the taste qualities represented by this stimulus array was assessed by calculating correlations between the activity profiles they elicited from these 50 neurons. The results generally confirmed expectations derived from human psychophysical studies. In a multidimensional representation of stimulus similarity, there were groups that contained acids, sodium salts, and chemicals that humans label bitter and sweet. 7. The small proportion of insular-opercular neurons that are taste sensitive and the low discharge rates that taste stimuli are able to evoke from them suggest a wider role for this cortical area than just gustatory coding.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Direct and Collateral Alterations of Functional Cortical Circuits in a Rat Model of Subcortical Band Heterotopia

2018 ◽  
Vol 29 (10) ◽  
pp. 4253-4262 ◽  
Author(s):  
Vanessa Plantier ◽  
Françoise Watrin ◽  
Emmanuelle Buhler ◽  
Fanny Sandrine Martineau ◽  
Surajit Sahu ◽  
...  
Keyword(s):  
Barrel Cortex ◽  
Intractable Epilepsy ◽  
Pyramidal Cells ◽  
Cortical Region ◽  
Cortical Networks ◽  
Causative Gene ◽  
Double Cortex Syndrome ◽  
Subcortical Band Heterotopia ◽  
Migration Disorder ◽  
Band Heterotopia

Abstract Subcortical band heterotopia (SBH), also known as double-cortex syndrome, is a neuronal migration disorder characterized by an accumulation of neurons in a heterotopic band below the normotopic cortex. The majority of patients with SBH have mild to moderate intellectual disability and intractable epilepsy. However, it is still not clear how cortical networks are organized in SBH patients and how this abnormal organization contributes to improper brain function. In this study, cortical networks were investigated in the barrel cortex in an animal model of SBH induced by in utero knockdown of Dcx, main causative gene of this condition in human patients. When the SBH was localized below the Barrel Field (BF), layer (L) four projection to correctly positioned L2/3 pyramidal cells was weakened due to lower connectivity. Conversely, when the SBH was below an adjacent cortical region, the excitatory L4 to L2/3 projection was stronger due to increased L4 neuron excitability, synaptic strength and excitation/inhibition ratio of L4 to L2/3 connection. We propose that these developmental alterations contribute to the spectrum of clinical dysfunctions reported in patients with SBH.

scholarly journals Selective attenuation of Ether-a-go-go related K+ currents by endogenous acetylcholine reduces spike-frequency adaptation and network correlation

eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Edward D Cui ◽  
Ben W Strowbridge
Keyword(s):  
Late Phase ◽  
Pyramidal Cells ◽  
Spike Frequency ◽  
Spike Frequency Adaptation ◽  
Firing Rates ◽  
Frequency Adaptation ◽  
Rat Neocortex ◽  
Persistent Firing ◽  
K Current

Most neurons do not simply convert inputs into firing rates. Instead, moment-to-moment firing rates reflect interactions between synaptic inputs and intrinsic currents. Few studies investigated how intrinsic currents function together to modulate output discharges and which of the currents attenuated by synthetic cholinergic ligands are actually modulated by endogenous acetylcholine (ACh). In this study we optogenetically stimulated cholinergic fibers in rat neocortex and find that ACh enhances excitability by reducing Ether-à-go-go Related Gene (ERG) K+ current. We find ERG mediates the late phase of spike-frequency adaptation in pyramidal cells and is recruited later than both SK and M currents. Attenuation of ERG during coincident depolarization and ACh release leads to reduced late phase spike-frequency adaptation and persistent firing. In neuronal ensembles, attenuating ERG enhanced signal-to-noise ratios and reduced signal correlation, suggesting that these two hallmarks of cholinergic function in vivo may result from modulation of intrinsic properties.

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