scholarly journals An astrocytic signaling loop for frequency-dependent control of dendritic integration and spatial learning

2021 ◽  
Author(s):  
Kirsten Bohmbach ◽  
Nicola Masala ◽  
Eva M. Schönhense ◽  
Katharina Hill ◽  
André N. Haubrich ◽  
...  
Keyword(s):  
Pyramidal Cell ◽  
Cell Activity ◽  
Pyramidal Cells ◽  
Hcn Channels ◽  
Frequency Dependent ◽  
Dendritic Integration ◽  
Voltage Gated Sodium Channels ◽  
Whole Cell Patch Clamp ◽  
Photon Excitation ◽  
Dendritic Spikes

Dendrites of hippocampal CA1 pyramidal cells amplify clustered glutamatergic input by activation of voltage-gated sodium channels and N-methyl-D-aspartate receptors (NMDARs). NMDAR activity depends on the presence of NMDAR co-agonists such as D-serine, but how co-agonists influence dendritic integration is not well understood. Using combinations of whole-cell patch clamp, iontophoretic glutamate application, two-photon excitation fluorescence microscopy and glutamate uncaging we found that exogenous D-serine reduces the threshold of dendritic spikes and increases their amplitude. Triggering an astrocytic mechanism controlling endogenous D-serine supply via endocannabinoid receptors (CBRs) also increased dendritic spiking. Unexpectedly, this pathway was activated by pyramidal cell activity primarily in the theta range, which required HCN channels and astrocytic CB1Rs. Therefore, astrocytes close a positive and frequency-dependent feedback loop between pyramidal cell activity and their integration of dendritic input. Its disruption led to an impairment of spatial memory, which demonstrates its behavioral relevance.

Hippocampal Pyramidal Cell Activity Encodes Conditioned Stimulus Predictive Value During Classical Conditioning in Alert Cats

2001 ◽  
Vol 86 (5) ◽  
pp. 2571-2582 ◽  
Author(s):  
A. Múnera ◽  
A. Gruart ◽  
M. D. Muñoz ◽  
R. Fernández-Mas ◽  
J. M. Delgado-García
Keyword(s):  
Classical Conditioning ◽  
Pyramidal Cell ◽  
Predictive Value ◽  
Cell Activity ◽  
Pyramidal Cells ◽  
Neuronal Firing ◽  
Oscillatory Activity ◽  
Antidromic Activation ◽  
Cell Firing ◽  
Alert Cats

We have recorded the firing activities of hippocampal pyramidal cells throughout the classical conditioning of eyelid responses in alert cats. Pyramidal cells ( n = 220) were identified by their antidromic activation from the ipsilateral fornix and according to their spike properties. Upper eyelid movements were recorded with the search coil in a magnetic field technique. Latencies and firing profiles of recorded pyramidal cells following the paired presentation of conditioned (CS) and unconditioned (US) stimuli were similar, regardless of the different sensory modalities used as CS (tones, air puffs), the different conditioning paradigms (trace, delay), or the different latency and topography of the evoked eyelid conditioned responses. However, for the three paradigms used here, evoked neuronal firing to CS presentation increased across conditioning, but remained unchanged for US presentation. Contrarily, pyramidal cell firing was not modified when the same stimuli used here as CS and US were presented unpaired, during pseudoconditing sessions. Pyramidal cell firing did not seem to encode eyelid position, velocity, or acceleration for either reflex or conditioned eyelid responses. Evoked pyramidal cell responses were always in coincidence with a beta oscillatory activity in hippocampal extracellular field potentials. In this regard, the beta rhythm represents a facilitation, or permissive time window, for timed pyramidal cell firing. It is concluded that pyramidal cells encode CS-US associative strength or CS predictive value.

Presynaptic Interneuron Subtype- and Age-Dependent Modulation of GABAergic Synaptic Transmission by β-Adrenoceptors in Rat Insular Cortex

2010 ◽  
Vol 103 (5) ◽  
pp. 2876-2888 ◽  
Author(s):  
Yuko Koyanagi ◽  
Kiyofumi Yamamoto ◽  
Yoshiyuki Oi ◽  
Noriaki Koshikawa ◽  
Masayuki Kobayashi
Keyword(s):  
Synaptic Transmission ◽  
Pyramidal Cell ◽  
Insular Cortex ◽  
Pyramidal Cells ◽  
Gaba Release ◽  
Taste Aversion Learning ◽  
Inhibitory Synaptic Transmission ◽  
Whole Cell Patch Clamp ◽  
Adrenergic Modulation ◽  
Layer V

β-Adrenoceptors play a crucial role in the regulation of taste aversion learning in the insular cortex (IC). However, β-adrenergic effects on inhibitory synaptic transmission mediated by γ-aminobutyric acid (GABA) remain unknown. To elucidate the mechanisms of β-adrenergic modulation of inhibitory synaptic transmission, we performed paired whole cell patch-clamp recordings from layer V GABAergic interneurons and pyramidal cells of rat IC aged from postnatal day 17 (PD17) to PD46 and examined the effects of isoproterenol, a β-adrenoceptor agonist, on unitary inhibitory postsynaptic currents (uIPSCs). Isoproterenol (100 μM) induced facilitating effects on uIPSCs in 33.3% of cell pairs accompanied by decreases in coefficient of variation (CV) of the first uIPSC amplitude and paired-pulse ratio (PPR) of the second to first uIPSC amplitude, whereas 35.9% of pairs showed suppressive effects of isoproterenol on uIPSC amplitude obtained from fast spiking (FS) to pyramidal cell pairs. Facilitatory effects of isoproterenol were frequently observed in FS–pyramidal cell pairs at ≥PD24. On the other hand, isoproterenol suppressed uIPSC amplitude by 52.3 and 39.8% in low-threshold spike (LTS)–pyramidal and late spiking (LS)–pyramidal cell pairs, respectively, with increases in CV and PPR. The isoproterenol-induced suppressive effects were blocked by preapplication of 100 μM propranolol, a β-adrenoceptor antagonist. There was no significant correlation between age and changes of uIPSCs in LTS–/LS–pyramidal cell pairs. These results suggest the presence of differential mechanisms in presynaptic GABA release and/or postsynaptic GABAA receptor-related assemblies among interneuron subtypes. Age- and interneuron subtype-specific β-adrenergic modulation of IPSCs may contribute to experience-dependent plasticity in the IC.

Plasticity in an electrosensory system. II. Postsynaptic events associated with a dynamic sensory filter

1996 ◽  
Vol 76 (4) ◽  
pp. 2497-2507 ◽  
Author(s):  
J. Bastian
Keyword(s):  
Pyramidal Cell ◽  
Cell Activity ◽  
Pyramidal Cells ◽  
Afferent Input ◽  
Current Injection ◽  
Inhibitory Input ◽  
Tetanic Stimulation ◽  
Negative Image ◽  
Postsynaptic Potentials ◽  
Stimulation Of

1. This report summarizes studies of the changes in postsynaptic potentials that occur as pyramidal cells within the primary electrosensory processing nucleus learn to reject repetitive patterns of afferent input. The rejection mechanism employs "negative image inputs" that oppose or cancel electroreceptor afferent inputs or patterns of pyramidal hyperpolarization or depolarization caused by intracellular current injection. Feedback pathways carrying descending electrosensory as well as other types of information provide the negative image inputs. This study focuses on the role of a directly descending projection from a second-order electrosensory nucleus the nucleus praeeminentialis (nP), which provides excitatory and inhibitory inputs to the apical dendrites of electrosensory lateral line lobe (ELL) pyramidal cells. 2. Electrical stimulation of the pathway linking the nP to the ELL was used to activate descending inputs to the pyramidal cells. Pyramidal cell activity was typically increased due to stimulation of this pathway. Tetanic stimulation of the descending pathway paired with either electrosensory stimuli that inhibited pyramidal cells, or hyperpolarizing current injection, increased the excitation provided by subsequent stimulation of this pathway. Pairing tetanic stimulation with excitatory electrosensory stimuli or depolarizing current injection had the opposite effect. Subsequent activation of the descending pathway inhibited pyramidal cells. 3. Intracellular recordings showed that the increased firing of pyramidal cells evoked by stimulation of the descending pathway following tetanic stimulation paired with postsynaptic hyperpolarization resulted from larger amplitude and longer-duration excitatory postsynaptic potentials (EPSPs). The shift in the effect of activity in this descending pathway to providing net inhibitory input to the pyramidal cells after paired presynaptic activity and postsynaptic depolarization probably results from the potentiation of inhibitory postsynaptic potentials (IPSPs). The EPSP and IPSPs evoked by activity in this descending pathway can be continuously adjusted in amplitude, thereby counterbalancing patterns of pyramidal cell excitation and inhibition received from the periphery with the result that repetitive patterns of afferent activity are strongly attenuated.

scholarly journals The Entorhinal Cortical Alvear Pathway Differentially Excites Pyramidal Cells and Interneuron Subtypes in Hippocampal CA1

2020 ◽  
Author(s):  
Karen A Bell ◽  
Rayne Delong ◽  
Priyodarshan Goswamee ◽  
A Rory McQuiston
Keyword(s):  
Brain Slices ◽  
Pyramidal Cells ◽  
Excitatory Input ◽  
Theta Burst Stimulation ◽  
Ca1 Pyramidal Cells ◽  
Whole Cell Patch Clamp ◽  
Hippocampal Ca1 ◽  
Physiological Impact ◽  
Theta Burst ◽  
Synaptic Responses

Abstract The entorhinal cortex alvear pathway is a major excitatory input to hippocampal CA1, yet nothing is known about its physiological impact. We investigated the alvear pathway projection and innervation of neurons in CA1 using optogenetics and whole cell patch clamp methods in transgenic mouse brain slices. Using this approach, we show that the medial entorhinal cortical alvear inputs onto CA1 pyramidal cells (PCs) and interneurons with cell bodies located in stratum oriens were monosynaptic, had low release probability, and were mediated by glutamate receptors. Optogenetic theta burst stimulation was unable to elicit suprathreshold activation of CA1 PCs but was capable of activating CA1 interneurons. However, different subtypes of interneurons were not equally affected. Higher burst action potential frequencies were observed in parvalbumin-expressing interneurons relative to vasoactive-intestinal peptide-expressing or a subset of oriens lacunosum-moleculare (O-LM) interneurons. Furthermore, alvear excitatory synaptic responses were observed in greater than 70% of PV and VIP interneurons and less than 20% of O-LM cells. Finally, greater than 50% of theta burst-driven inhibitory postsynaptic current amplitudes in CA1 PCs were inhibited by optogenetic suppression of PV interneurons. Therefore, our data suggest that the alvear pathway primarily affects hippocampal CA1 function through feedforward inhibition of select interneuron subtypes.

Single-unit analysis of different hippocampal cell types during classical conditioning of rabbit nictitating membrane response

1983 ◽  
Vol 50 (5) ◽  
pp. 1197-1219 ◽  
Author(s):  
T. W. Berger ◽  
P. C. Rinaldi ◽  
D. J. Weisz ◽  
R. F. Thompson
Keyword(s):  
Classical Conditioning ◽  
Pyramidal Cell ◽  
Action Potentials ◽  
Pyramidal Cells ◽  
Cell Types ◽  
Firing Frequency ◽  
Spontaneous Firing ◽  
Nictitating Membrane ◽  
Nictitating Membrane Response ◽  
Firing Characteristics

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)

Asymptotic Input-Output Relationship Predicts Electric Field Effect on Sublinear Dendritic Integration of AMPA Synapses

2021 ◽  
pp. 1-37
Author(s):  
Yaqin Fan ◽  
Xile Wei ◽  
Guosheng Yi ◽  
Meili Lu ◽  
Jiang Wang ◽  
...  
Keyword(s):  
Electric Field ◽  
Pyramidal Cells ◽  
Excitatory Postsynaptic Potential ◽  
Electric Field Effect ◽  
Modulation Effect ◽  
Input Output ◽  
Dendritic Integration ◽  
Relative Contribution ◽  
Singular Perturbation Analysis ◽  
Neuronal Computation

Abstract An extracellular electric field (EF) induces transmembrane polarizations on extremely inhomogeneous spaces Evidence shows that EF-induced somatic polarization in pyramidal cells can modulate the neuronal input-output (I/O) function. However, it remains unclear whether and how dendritic polarization participates in the dendritic integration and contributes to the neuronal I/O function. To this end, we built a computational model of a simplified pyramidal cell with multi-dendritic tufts, one dendritic trunk, and one soma to describe the interactions among EF, dendritic integration, and somatic output, in which the EFs were modeled by inserting inhomogeneous extracellular potentials. We aimed to establish the underlying relationship between dendritic polarization and dendritic integration by analyzing the dynamics of subthreshold membrane potentials in response to AMPA synapses in the presence of constant EFs. The model-based singular perturbation analysis showed that the equilibrium mapping of a fast subsystem can serve as the asymptotic subthreshold I/O relationship for sublinear dendritic integration. This allows us to predict the tendency of EF-mediated dendritic integration by showing how EF changes modify equilibrium mapping. EF-induced hyperpolarization of distal dendrites receiving synapses inputs was found to play a key role in facilitating the AMPA receptor-evoked excitatory postsynaptic potential (EPSP) by enhancing the driving force of synaptic inputs. A significantly higher efficacy of EF modulation effect on global AMPA-type dendritic integration was found compared with local AMPA-type dendritic integration. During the generation of an action potential (AP), the relative contribution of EF-modulated dendritic integration and EF-induced somatic polarization was determined to show their collaboration in promoting or inhibiting the somatic excitability, depending on the EF polarity. These findings are crucial for understanding the EF modulation effect on neuronal computation, which provides insight into the modulation mechanism of noninvasive brain modulation.

Synaptic Interactions in a Passive Dendritic Tree

1998 ◽  
Author(s):  
Christof Koch
Keyword(s):  
Nervous System ◽  
Dendritic Tree ◽  
Extreme Case ◽  
Pyramidal Cells ◽  
Inhibitory Synapses ◽  
Dendritic Trees ◽  
Central Processing ◽  
Voltage Dependent ◽  
Dendritic Spikes ◽  
Spatial Positioning

Nerve cells are the targets of many thousands of excitatory and inhibitory synapses. An extreme case are the Purkinje cells in the primate cerebellum, which receive between one and two hundred thousand synapses onto dendritic spines from an equal number of parallel fibers (Braitenberg and Atwood, 1958; Llinas and Walton, 1998). In fact, this structure has a crystalline-like quality to it, with each parallel fiber making exactly one synapse onto a spine of a Purkinje cell. For neocortical pyramidal cells, the total number of afferent synapses is about an order of magnitude lower (Larkman, 1991). These numbers need to be compared against the connectivity in the central processing unit (CPU) of modern computers, where the gate of a typical transistor usually receives input from one, two, or three other transistors or connects to one, two, or three other transistor gates. The large number of synapses converging onto a single cell provide the nervous system with a rich substratum for implementing a very large class of linear and nonlinear neuronal operations. As we discussed in the introductory chapter, it is only these latter ones, such as multiplication or a threshold operation, which are responsible for “computing” in the nontrivial sense of information processing. It therefore becomes crucial to study the nature of the interaction among two or more synaptic inputs located in the dendritic tree. Here, we restrict ourselves to passive dendritic trees, that is, to dendrites that do not contain voltage-dependent membrane conductances. While such an assumption seemed reasonable 20 or even 10 years ago, we now know that the dendritic trees of many, if not most, cells contain significant nonlinearities, including the ability to generate fast or slow all-or-none electrical events, so-called dendritic spikes. Indeed, truly passive dendrites may be the exception rather than the rule in the nervous In Sec. 1.5, we studied this interaction for the membrane patch model. With the addition of the dendritic tree, the nervous system has many more degrees of freedom to make use of, and the strength of the interaction depends on the relative spatial positioning, as we will see now. That this can be put to good use by the nervous system is shown by the following experimental observation and simple model.

Evidence from simultaneous intracellular recordings in rat hippocampal slices that area CA3 pyramidal cells innervate dentate hilar mossy cells

1994 ◽  
Vol 72 (5) ◽  
pp. 2167-2180 ◽  
Author(s):  
H. E. Scharfman
Keyword(s):  
Pyramidal Cell ◽  
Action Potentials ◽  
Granule Cells ◽  
Hippocampal Slices ◽  
Pyramidal Cells ◽  
Probability Of Failure ◽  
Mossy Cells ◽  
Mossy Cell ◽  
Ca3 Pyramidal Cells ◽  
Area Ca3

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)

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