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

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.

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.

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.

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.

scholarly journals Postsynaptic Glutamate Receptors and Integrative Properties of Fast-Spiking Interneurons in the Rat Neocortex

1999 ◽  
Vol 82 (3) ◽  
pp. 1295-1302 ◽  
Author(s):  
Maria Cecilia Angulo ◽  
Jean Rossier ◽  
Etienne Audinat
Keyword(s):  
Membrane Potential ◽  
Action Potential ◽  
Receptor Antagonist ◽  
Ampa Receptors ◽  
Temporal Summation ◽  
Pyramidal Cells ◽  
Resting Membrane Potential ◽  
Mean Width ◽  
Fast Spiking ◽  
Synaptic Responses

The glutamate-mediated synaptic responses of neocortical pyramidal cell to fast-spiking interneuron (pyramidal-FS) connections were studied by performing paired recordings at 30–33°C in acute slices of 14- to 35-day-old rats ( n = 39). Postsynaptic fast-spiking (FS) cells were recorded in whole cell configuration with a patch pipette, and presynaptic pyramidal cells were impaled with sharp intracellular electrodes. At a holding potential of −72 mV (near the resting membrane potential), unitary excitatory postsynaptic potentials (EPSPs) had a mean amplitude of 2.1 ± 1.3 mV and a mean width at half-amplitude of 10.5 ± 3.7 ms ( n = 18). Bath application of the N-methyl-d-aspartate (NMDA) receptor antagonist d(−)2-amino-5-phosphonovaleric acid (d-AP5) had minor effects on both the amplitude and the duration of unitary EPSPs, whereas the α-amino-3-hydroxy-5-methyl-4-isoxazole-propionate (AMPA)/kainate receptor antagonist 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) almost completely blocked the synaptic responses. In voltage-clamp mode, the selective antagonist of AMPA receptors 1-(4-aminophenyl)-3-methylcarbamyl-4-methyl-7,8-methylenedioxy-3,4-dihydro-5H-2,3-benzodiazepine (GYKI 53655; 40–66 μM) blocked 96 ± 1.9% ofd-AP5–insensitive unitary excitatory postsynaptic currents (EPSCs), confirming the predominance of AMPA receptors, as opposed to kainate receptors, at pyramidal-FS connections ( n = 3). Unitary EPSCs mediated by AMPA receptors had fast rise times (0.29 ± 0.04 ms) and amplitude-weighted decay time constants (2 ± 0.8 ms; n = 16). In the presence of intracellular spermine, these currents showed the characteristic rectifying current-voltage ( I-V) curve of calcium-permeable AMPA receptors. A slower component mediated by NMDA receptors was observed when unitary synaptic currents were recorded at a membrane potential more positive than −50 mV. In response to short trains of moderately high-frequency (67 Hz) presynaptic action potentials, we observed only a limited temporal summation of unitary EPSPs, probably because of the rapid kinetics of AMPA receptors and the absence of NMDA component in these subthreshold synaptic responses. By combining paired recordings with extracellular stimulations ( n = 11), we demonstrated that EPSPs elicited by two different inputs were summed linearly by FS interneurons at membrane potentials below the action potential threshold. We estimated that, in our in vitro recording conditions, 8 ± 5 pyramidal cells ( n = 18) should be activated simultaneously to make FS interneurons fire an action potential from −72 mV. The low level of temporal summation and the linear summation of excitatory inputs in FS cells favor the role of coincidence detectors of these interneurons in neocortical circuits.

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.

scholarly journals Spatially structured inhibition defined by polarized parvalbumin interneuron axons promotes head direction tuning

2021 ◽  
Vol 7 (25) ◽  
pp. eabg4693
Author(s):  
Yangfan Peng ◽  
Federico J. Barreda Tomas ◽  
Paul Pfeiffer ◽  
Moritz Drangmeister ◽  
Susanne Schreiber ◽  
...  
Keyword(s):  
Spatial Organization ◽  
Pyramidal Cells ◽  
Brain Regions ◽  
Head Direction ◽  
Spatial Connectivity ◽  
Parvalbumin Interneurons ◽  
Parvalbumin Interneuron ◽  
Network Simulations ◽  
Fast Spiking ◽  
Direction Tuning

In cortical microcircuits, it is generally assumed that fast-spiking parvalbumin interneurons mediate dense and nonselective inhibition. Some reports indicate sparse and structured inhibitory connectivity, but the computational relevance and the underlying spatial organization remain unresolved. In the rat superficial presubiculum, we find that inhibition by fast-spiking interneurons is organized in the form of a dominant super-reciprocal microcircuit motif where multiple pyramidal cells recurrently inhibit each other via a single interneuron. Multineuron recordings and subsequent 3D reconstructions and analysis further show that this nonrandom connectivity arises from an asymmetric, polarized morphology of fast-spiking interneuron axons, which individually cover different directions in the same volume. Network simulations assuming topographically organized input demonstrate that such polarized inhibition can improve head direction tuning of pyramidal cells in comparison to a “blanket of inhibition.” We propose that structured inhibition based on asymmetrical axons is an overarching spatial connectivity principle for tailored computation across brain regions.

Sign in / Sign up

Export Citation Format

Share Document