P/Q-Type, But Not N-Type, Calcium Channels Mediate GABA Release From Fast-Spiking Interneurons to Pyramidal Cells in Rat Prefrontal Cortex

2007 ◽  
Vol 97 (5) ◽  
pp. 3567-3573 ◽  
Author(s):  
A. V. Zaitsev ◽  
N. V. Povysheva ◽  
D. A. Lewis ◽  
L. S. Krimer
Keyword(s):  
Prefrontal Cortex ◽  
Calcium Channels ◽  
Pyramidal Cells ◽  
Gaba Release ◽  
Differential Distribution ◽  
Bath Application ◽  
Rat Neocortex ◽  
Fast Spiking ◽  
Synaptic Dynamics ◽  
Central Synapses

The Cav2.1 (P/Q-) and Cav2.2 (N-type) voltage-gated calcium channels (VGCCs) play a predominant role in neurotransmitter release at central synapses, but their distribution is not uniform across different types of synapses. Although the functional significance of the differential distribution of N- and P/Q-type VGCCs is poorly understood, distinct types of VGCCs appear to differentially affect synaptic properties. For example, P/Q-type VGCCs are located closer to release sites and are less affected by G-protein-mediated inhibition than are N-type VGCCs. Thus P/Q-type VGCCs might be beneficial at synapses with high probability of release and precise timing of neurotransmission, such as the inhibitory inputs from parvalbumin-containing fast-spiking (FS) interneurons to pyramidal cells (PCs) in the neocortex. To determine whether VGCCs types predominate at synapses from FS interneurons to PCs in rat prefrontal cortex, whole cell paired recordings ( n = 14) combined with intracellular labeling and fluorescence immunohistochemistry for parvalbumin were performed in acute slices. Bath application of the specific N-type VGCC blocker ω-conotoxin-GVIa (1 μM) did not alter inhibitory postsynaptic potential amplitude, failure rate, or synaptic dynamics; in contrast, application of P/Q-type VGCC blocker ω-agatoxin-IVa (0.5 μM) completely and irreversibly blocked neurotransmission. These results indicate that P/Q-type VGCCs mediate the GABA release from parvalbumin-positive FS interneurons to PCs in the rat neocortex.

scholarly journals N-Type Calcium Channels Control GABAergic Transmission in Brain Areas related to Fear and Anxiety

2021 ◽  
Vol 5 (1) ◽  
Author(s):  
Maxwell Blazon ◽  
Brianna LaCarubba ◽  
Alexandra Bunda ◽  
Natalie Czepiel ◽  
Shayna Mallat ◽  
...  
Keyword(s):  
Prefrontal Cortex ◽  
Calcium Channels ◽  
Medial Prefrontal Cortex ◽  
Basolateral Amygdala ◽  
Pyramidal Cells ◽  
Gaba Release ◽  
Projection Neurons ◽  
Brain Areas ◽  
Fear And Anxiety ◽  
Central Level

N-type (CaV2.2) calcium channels are key for action potential-evoked transmitter release in the peripheral and central nervous system. Previous studies have highlighted the functional relevance of N-type calcium channels at both the peripheral and central level. In the periphery, N-type calcium channels regulate nociceptive and sympathetic responses. At the central level, N-type calcium channels have been linked to aggression, hyperlocomotion, and anxiety. Among the areas of the brain that are involved in anxiety are the basolateral amygdala, medial prefrontal cortex, and ventral hippocampus. These three areas share similar characteristics in their neuronal circuitry, where pyramidal projection neurons are under the inhibitory control of a wide array of interneurons including those that express the peptide cholecystokinin. This type of interneuron is well-known to rely on N-type calcium channels to release GABA in the hippocampus, however, whether these channels control GABA release from cholecystokinin-expressing interneurons in the basolateral amygdala and medial prefrontal cortex is not known. Here, using mouse models to genetically label cholecystokinin-expressing interneurons and electrophysiology, we found that in the basolateral amygdala, N-type calcium channels control ~50% of GABA release from these neurons onto pyramidal cells. By contrast, in the medial prefrontal cortex N-type calcium channels are functionally absent in synapses of cholecystokinin-expressing interneurons, but control ~40% of GABA release from other types of interneurons. Our findings provide insights into the precise localization of N-type calcium channels in interneurons of brain areas related to anxiety.

Cluster Analysis–Based Physiological Classification and Morphological Properties of Inhibitory Neurons in Layers 2–3 of Monkey Dorsolateral Prefrontal Cortex

2005 ◽  
Vol 94 (5) ◽  
pp. 3009-3022 ◽  
Author(s):  
Leonid S. Krimer ◽  
Aleksey V. Zaitsev ◽  
Gabriela Czanner ◽  
Sven Kröner ◽  
Guillermo González-Burgos ◽  
...  
Keyword(s):  
Cluster Analysis ◽  
Prefrontal Cortex ◽  
Dorsolateral Prefrontal Cortex ◽  
Pyramidal Cells ◽  
Inhibitory Neurons ◽  
Morphological Properties ◽  
Electrophysiological Properties ◽  
Dorsolateral Prefrontal ◽  
Fast Spiking ◽  
Monkey Prefrontal Cortex

In primates, little is known about intrinsic electrophysiological properties of neocortical neurons and their morphological correlates. To classify inhibitory cells (interneurons) in layers 2–3 of monkey dorsolateral prefrontal cortex we used whole cell voltage recordings and intracellular labeling in slice preparation with subsequent morphological reconstructions. Regular spiking pyramidal cells have been also included in the sample. Neurons were successfully segregated into three physiological clusters: regular-, intermediate-, and fast-spiking cells using cluster analysis as a multivariate exploratory technique. When morphological types of neurons were mapped on the physiological clusters, the cluster of regular spiking cells contained all pyramidal cells, whereas the intermediate- and fast-spiking clusters consisted exclusively of interneurons. The cluster of fast-spiking cells contained all of the chandelier cells and the majority of local, medium, and wide arbor (basket) interneurons. The cluster of intermediate spiking cells predominantly consisted of cells with the morphology of neurogliaform or vertically oriented (double-bouquet) interneurons. Thus a quantitative approach enabled us to demonstrate that intrinsic electrophysiological properties of neurons in the monkey prefrontal cortex define distinct cell types, which also display distinct morphologies.

Isodirectional Tuning of Adjacent Interneurons and Pyramidal Cells During Working Memory: Evidence for Microcolumnar Organization in PFC

1999 ◽  
Vol 81 (4) ◽  
pp. 1903-1916 ◽  
Author(s):  
Srinivas G. Rao ◽  
Graham V. Williams ◽  
Patricia S. Goldman-Rakic
Keyword(s):  
Working Memory ◽  
Prefrontal Cortex ◽  
Receptive Fields ◽  
Pyramidal Cells ◽  
Delayed Response ◽  
Cellular Mechanisms ◽  
Threshold Response ◽  
Dorsolateral Prefrontal ◽  
Fast Spiking ◽  
Spatially Oriented

Isodirectional tuning of adjacent interneurons and pyramidal cells during working memory: evidence for microcolumnar organization in PFC. Studies on the cellular mechanisms of working memory demonstrated that neurons in dorsolateral prefrontal cortex (dPFC) exhibit directionally tuned activity during an oculomotor delayed response. To determine the particular contributions of pyramidal cells and interneurons to spatial tuning in dPFC, we examined both individually and in pairs the tuning properties of regular-spiking (RS) and fast-spiking (FS) units that represent putative pyramidal cells and interneurons, respectively. Our main finding is that FS units possess spatially tuned sensory, motor, and delay activity (i.e., “memory fields”) similar to those found in RS units. Furthermore, when recorded simultaneously at the same site, the majority of neighboring neurons, whether FS or RS, displayed isodirectional tuning, i.e., they shared very similar tuning angles for the sensory and delay phases of the task. As the trial entered the response phase of the task, many FS units shifted their direction of tuning and became cross-directional to adjacent RS units by the end of the trial. These results establish that a large part of inhibition in prefrontal cortex is spatially oriented rather than being untuned and simply regulating the threshold response of pyramidal cell output. Moreover, the isodirectional tuning between adjacent neurons supports a functional microcolumnar organization in dPFC for spatial memory fields similar to that found in other areas of cortex for sensory receptive fields.

Innervation of interneurons immunoreactive for VIP by intrinsically bursting pyramidal cells and fast-spiking interneurons in infragranular layers of juvenile rat neocortex

2002 ◽  
Vol 16 (1) ◽  
pp. 11-20 ◽  
Author(s):  
Jochen F. Staiger ◽  
Dirk Schubert ◽  
Werner Zuschratter ◽  
Rolf Kötter ◽  
Heiko J. Luhmann ◽  
...  
Keyword(s):  
Pyramidal Cells ◽  
Rat Neocortex ◽  
Fast Spiking

scholarly journals Glucocorticoid receptors in the prefrontal cortex regulate dopamine efflux to stress via descending glutamatergic feedback to the ventral tegmental area

2013 ◽  
Vol 16 (8) ◽  
pp. 1799-1807 ◽  
Author(s):  
Kelly A. Butts ◽  
Anthony G. Phillips
Keyword(s):  
Prefrontal Cortex ◽  
Ventral Tegmental Area ◽  
Glucocorticoid Receptors ◽  
Acute Stress ◽  
Pyramidal Cells ◽  
Gaba Release ◽  
Underlying Mechanism ◽  
Ventral Tegmental ◽  
Glutamate Efflux

Abstract Enhanced dopamine (DA) efflux in the medial prefrontal cortex (mPFC) is a well-documented response to acute stress. We have previously shown that glucocorticoid receptors in the mPFC regulate stress-evoked DA efflux but the underlying mechanism is unknown. DA neurons in the ventral tegmental area (VTA) receive excitatory input from and send reciprocal projections to the mPFC. We hypothesize that blockade of prefrontal glucocorticoid receptors can reduce activity of descending glutamatergic input to the VTA, thereby attenuating stress-evoked DA efflux in the mPFC. Using in vivo microdialysis, we demonstrate that acute tail-pinch stress leads to a significant increase in glutamate efflux in the VTA. Blockade of prefrontal glucocorticoid receptors with the selective antagonist CORT 108297 attenuates stress-evoked glutamate efflux in the VTA together with DA efflux in the mPFC. Furthermore, blockade of ionotrophic glutamate receptors in the VTA attenuates stress-evoked DA efflux in the mPFC. We also examine the possible role of glucocorticoid-induced synthesis and release of endocannabinoids acting presynaptically via cannabinoid CB1 receptors to inhibit GABA release onto prefrontal pyramidal cells, thus enhancing descending glutamatergic input to the VTA leading to an increase in mPFC DA efflux during stress. However, administration of the cannabinoid CB1 receptor antagonist into the mPFC does not attenuate stress-evoked DA efflux in the mPFC. Taken together, our data indicate that glucocorticoids act locally within the mPFC to modulate mesocortical DA efflux by potentiation of glutamatergic drive onto DA neurons in the VTA.

Kinetics of GABAB autoreceptor-mediated suppression of GABA release in rat insular cortex

2012 ◽  
Vol 107 (5) ◽  
pp. 1431-1442 ◽  
Author(s):  
Masayuki Kobayashi ◽  
Hiroki Takei ◽  
Kiyofumi Yamamoto ◽  
Hiroshige Hatanaka ◽  
Noriaki Koshikawa
Keyword(s):  
Insular Cortex ◽  
Pyramidal Cells ◽  
Gaba Release ◽  
Paired Pulse ◽  
Whole Cell Patch Clamp ◽  
Pulse Ratio ◽  
Presynaptic Mechanisms ◽  
Fast Spiking ◽  
Layer V ◽  
Interevent Interval

Release of GABA is controlled by presynaptic GABA receptor type B (GABAB) autoreceptors at GABAergic terminals. However, there is no direct evidence that GABAB autoreceptors are activated by GABA release from their own terminals, and precise profiles of GABAB autoreceptor-mediated suppression of GABA release remain unknown. To explore these issues, we performed multiple whole-cell, patch-clamp recordings from layer V rat insular cortex. Both unitary inhibitory and excitatory postsynaptic currents (uIPSCs and uEPSCs, respectively) were recorded by applying a five-train depolarizing pulse injection at 20 Hz. In connections from both fast-spiking (FS) and non-FS interneurons to pyramidal cells, the GABAB receptor antagonist CGP 52432 had little effect on the initial uIPSC amplitude. However, uIPSCs, responding to later pulses, were effectively facilitated. This CGP 52432-induced facilitation was prominent in the fourth uIPSCs, which were evoked 150 ms after the first uIPSC. The facilitation of uIPSCs was accompanied by an increase in the paired-pulse ratio. In addition, analysis of the coefficient of variation suggests the involvement of presynaptic mechanisms in CGP 52432-induced uIPSC facilitation. Paired-pulse stimulation (interstimulus interval = 150 ms) of presynaptic FS cells revealed that the second uIPSC was also facilitated by CGP 52432, which had little effect on the amplitude and interevent interval of miniature IPSCs. In contrast, uEPSCs, responding to all five stimulations of a presynaptic pyramidal cell, were less affected by CGP 52432. These results suggest that a single presynaptic action potential is sufficient to activate GABAB autoreceptors and to suppress GABA release in the cerebral cortex.

Functional Properties of Fast Spiking Interneurons and Their Synaptic Connections With Pyramidal Cells in Primate Dorsolateral Prefrontal Cortex

2005 ◽  
Vol 93 (2) ◽  
pp. 942-953 ◽  
Author(s):  
Guillermo González-Burgos ◽  
Leonid S. Krimer ◽  
Nadya V. Povysheva ◽  
German Barrionuevo ◽  
David A. Lewis
Keyword(s):  
Prefrontal Cortex ◽  
Dorsolateral Prefrontal Cortex ◽  
Pyramidal Cells ◽  
Synaptic Connections ◽  
Electrophysiological Properties ◽  
Axonal Arborization ◽  
Presynaptic Mechanisms ◽  
Dorsolateral Prefrontal ◽  
Fast Spiking

Recent studies suggest that fast-spiking (FS) interneurons of the monkey dorsolateral prefrontal cortex (DLPFC) exhibit task-related firing during working-memory tasks. To gain further understanding of the functional role of FS neurons in monkey DLPFC, we described the in vitro electrophysiological properties of FS interneurons and their synaptic connections with pyramidal cells in layers 2/3 of areas 9 and 46. Extracellular spike duration was found to distinguish FS cells from non-FS interneuron subtypes. However, a substantial overlap in extracellular spike duration between these populations would make classification of individual interneurons difficult. FS neurons could be divided into two main morphological groups, chandelier and basket neurons, with very similar electrophysiological properties but significantly different horizontal spread of the axonal arborization. In paired cell recordings, unitary inhibitory postsynaptic potentials (IPSPs) elicited by FS neurons in pyramidal cells had rapid time course, small amplitude at resting membrane potential, and were mediated by GABAA receptors. Repetitive FS neuron stimulation, partially mimicking the sustained firing of interneurons in vivo, produced short-term depression of the unitary IPSPs, present at connections made by both basket and chandelier neurons and due at least in part to presynaptic mechanisms. These results suggest that FS neurons and their synaptic connections with pyramidal cells have homogeneous physiological properties. Thus different functional roles of basket and chandelier neurons in the DLPFC in vivo must arise from the distinct properties of the interneuronal axonal arborization or from a different functional pattern of excitatory and inhibitory connections with other components of the DLPFC neuronal network.

scholarly journals Properties of Excitatory Synaptic Responses in Fast-spiking Interneurons and Pyramidal Cells from Monkey and Rat Prefrontal Cortex

2005 ◽  
Vol 16 (4) ◽  
pp. 541-552 ◽  
Author(s):  
N.V. Povysheva ◽  
G. Gonzalez-Burgos ◽  
A.V. Zaitsev ◽  
S. Kröner ◽  
G. Barrionuevo ◽  
...  
Keyword(s):  
Prefrontal Cortex ◽  
Pyramidal Cells ◽  
Fast Spiking ◽  
Synaptic Responses

scholarly journals Differential Synaptic Dynamics and Circuit Connectivity of Hippocampal and Thalamic Inputs to the Prefrontal Cortex

2020 ◽  
Vol 1 (1) ◽  
Author(s):  
Sarah Canetta ◽  
Eric Teboul ◽  
Emma Holt ◽  
Scott S Bolkan ◽  
Nancy Padilla-Coreano ◽  
...  
Keyword(s):  
Prefrontal Cortex ◽  
Vasoactive Intestinal Peptide ◽  
Medial Prefrontal Cortex ◽  
Pyramidal Neurons ◽  
Pyramidal Cells ◽  
Mediodorsal Nucleus ◽  
Layer 2 ◽  
Communication Frequency ◽  
Synaptic Dynamics ◽  
Subcortical Regions

Abstract The medial prefrontal cortex (mPFC) integrates inputs from multiple subcortical regions including the mediodorsal nucleus of the thalamus (MD) and the ventral hippocampus (vHPC). How the mPFC differentially processes these inputs is not known. One possibility is that these two inputs target discreet populations of mPFC cells. Alternatively, individual prefrontal cells could receive convergent inputs but distinguish between both inputs based on synaptic differences, such as communication frequency. To address this, we utilized a dual wavelength optogenetic approach to stimulate MD and vHPC inputs onto single, genetically defined mPFC neuronal subtypes. Specifically, we compared the convergence and synaptic dynamics of both inputs onto mPFC pyramidal cells, and parvalbumin (PV)- and vasoactive intestinal peptide (VIP)-expressing interneurons. We found that all individual pyramidal neurons in layer 2/3 of the mPFC receive convergent input from both MD and vHPC. In contrast, PV neurons receive input biased from the MD, while VIP cells receive input biased from the vHPC. Independent of the target, MD inputs transferred information more reliably at higher frequencies (20 Hz) than vHPC inputs. Thus, MD and vHPC projections converge functionally onto mPFC pyramidal cells, but both inputs are distinguished by frequency-dependent synaptic dynamics and preferential engagement of discreet interneuron populations.

Disparities in Short-Term Depression Among Prefrontal Cortex Synapses Sustain Persistent Activity in a Balanced Network

2019 ◽  
Vol 30 (1) ◽  
pp. 113-134 ◽  
Author(s):  
Jae Young Yoon ◽  
Hyoung Ro Lee ◽  
Won-Kyung Ho ◽  
Suk-Ho Lee
Keyword(s):  
Prefrontal Cortex ◽  
Pyramidal Cells ◽  
Excitatory Synapses ◽  
Persistent Activity ◽  
Neural Basis ◽  
Short Term ◽  
Postsynaptic Currents ◽  
Different Types ◽  
Fast Spiking ◽  
Balanced Network

Abstract Persistent activity of cue-representing neurons in the prefrontal cortex (PFC) is regarded as a neural basis for working memory. The contribution of short-term synaptic plasticity (STP) at different types of synapses comprising the cortical network to persistent activity, however, remains unclear. Characterizing STP at synapses of the rat PFC layer 5 network, we found that PFC synapses exhibit distinct STP patterns according to presynaptic and postsynaptic identities. Excitatory postsynaptic currents (EPSCs) from corticopontine (Cpn) neurons were well sustained throughout continued activity, with stronger depression at synapses onto fast-spiking interneurons than those onto pyramidal cells. Inhibitory postsynaptic currents (IPSCs) were sustained at a weaker level compared with EPSC from Cpn synapses. Computational modeling of a balanced network incorporating empirically observed STP revealed that little depression at recurrent excitatory synapses, combined with stronger depression at other synapses, could provide the PFC with a unique synaptic mechanism for the generation and maintenance of persistent activity.

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