scholarly journals Cell Type-Specific Modulation of Layer 6A Excitatory Microcircuits by Acetylcholine in Rat Barrel Cortex

2019 ◽  
Author(s):  
Danqing Yang ◽  
Robert Günter ◽  
Guanxiao Qi ◽  
Gabriele Radnikow ◽  
Dirk Feldmeyer
Keyword(s):  
Pyramidal Cell ◽  
Barrel Cortex ◽  
Glutamate Release ◽  
Synaptic Connections ◽  
Cell Type ◽  
Presynaptic Neuron ◽  
Synaptic Release ◽  
Low Concentrations ◽  
Cell Type Specific ◽  
Behavioral States

AbstractAcetylcholine (ACh) is known to regulate cortical activity during different behavioral states, e.g. wakefulness and attention. Here we show a differential expression of muscarinic ACh receptors (mAChRs) and nicotinic AChRs (nAChRs) in different layer 6A (L6A) pyramidal cell (PC) types of somatosensory cortex. At low concentrations, ACh induced a persistent hyperpolarization in corticocortical (CC) but a depolarization in corticothalamic (CT) L6A PCs via M4 and M1 mAChRs, respectively. At ∼1 mM ACh depolarized exclusively CT PCs via α4β2 subunit-containing nAChRs without affecting CC PCs. Miniature EPSC frequency in CC PCs was decreased by ACh but increased in CT PCs. In synaptic connections with a presynaptic CC PC, glutamate release was suppressed via M4 mAChR activation but enhanced by nAChRs via α4β2 nAChRs when the presynaptic neuron was a CT PC. Thus, in layer 6A the interaction of mAChRs and nAChRs results in an altered excitability and synaptic release, effectively strengthening corticothalamic output while weakening corticocortical synaptic signaling.

scholarly journals Muscarinic and Nicotinic Modulation of Neocortical Layer 6A Synaptic Microcircuits Is Cooperative and Cell-Specific

2019 ◽  
Vol 30 (6) ◽  
pp. 3528-3542 ◽  
Author(s):  
Danqing Yang ◽  
Robert Günter ◽  
Guanxiao Qi ◽  
Gabriele Radnikow ◽  
Dirk Feldmeyer
Keyword(s):  
Differential Expression ◽  
Somatosensory Cortex ◽  
Pyramidal Cell ◽  
Glutamate Release ◽  
Synaptic Connections ◽  
Presynaptic Neuron ◽  
Synaptic Release ◽  
Low Concentrations ◽  
Behavioral States ◽  
Ach Receptors

Abstract Acetylcholine (ACh) is known to regulate cortical activity during different behavioral states, for example, wakefulness and attention. Here we show a differential expression of muscarinic ACh receptors (mAChRs) and nicotinic ACh receptors (nAChRs) in different layer 6A (L6A) pyramidal cell (PC) types of somatosensory cortex. At low concentrations, ACh induced a persistent hyperpolarization in corticocortical (CC) but a depolarization in corticothalamic (CT) L6A PCs via M 4 and M1 mAChRs, respectively. At ~ 1 mM, ACh depolarized exclusively CT PCs via α4β2 subunit-containing nAChRs without affecting CC PCs. Miniature EPSC frequency in CC PCs was decreased by ACh but increased in CT PCs. In synaptic connections with a presynaptic CC PC, glutamate release was suppressed via M4 mAChR activation but enhanced by nAChRs via α4β2 nAChRs when the presynaptic neuron was a CT PC. Thus, in L6A, the interaction of mAChRs and nAChRs results in an altered excitability and synaptic release, effectively strengthening CT output while weakening CC synaptic signaling.

scholarly journals Layer 6A pyramidal cells subtypes form synaptic microcircuits with distinct functional and structural properties

2021 ◽  
Author(s):  
Danqing Yang ◽  
Guanxiao Qi ◽  
Dirk Feldmeyer
Keyword(s):  
Barrel Cortex ◽  
Dynamic Properties ◽  
Pyramidal Cells ◽  
Synaptic Connections ◽  
Cell Type ◽  
Short Term ◽  
Electrophysiological Properties ◽  
Cell Type Specific ◽  
Feedback Networks ◽  
Whole Cell Recordings

Neocortical layer 6 plays a crucial role in sensorimotor coordination and integration through functionally segregated circuits linking intracortical and subcortical areas. However, because of the high neuronal heterogeneity and sparse intralaminar connectivity data on the cell-type specific synaptic microcircuits in layer 6 remain few and far between. To address this issue, whole-cell recordings combined with morphological reconstructions have been used to identify morphoelectric types of layer 6A pyramidal cells (PCs) in rat barrel cortex. Cortico-thalamic (CT), corticocortical (CC) and cortico-claustral (CCla) pyramidal cells have been distinguished based on to their distinct dendritic and axonal morphologies as well as their different electrophysiological properties. Here we demonstrate that these three types of layer 6A pyramidal cells innervate neighboring excitatory neurons with distinct synaptic properties: CT PCs establish weak facilitating synapses to other L6A PCs; CC PCs form synapses of moderate efficacy; while synapses made by putative CCla PCs display the highest release probability and a marked short-term depression. Furthermore, for excitatory-inhibitory synaptic connections in layer 6 we were able to show that both the presynaptic PC type and the postsynaptic interneuron type govern the dynamic properties of the of the respective synaptic connections. We have identified a functional division of local layer 6A excitatory microcircuits which may be responsible of the differential temporal engagement of layer 6 feed-forward and feedback networks. Our results provides a basis for further investigations on the long-range cortico-cortical, cortico-thalamic and cortico-claustral pathways.

scholarly journals Cell-type specific neuromodulation of excitatory and inhibitory neurons via muscarinic acetylcholine receptors in layer 4 of rat barrel cortex

2021 ◽  
Author(s):  
Guanxiao Qi ◽  
Dirk Feldmeyer
Keyword(s):  
Barrel Cortex ◽  
Muscarinic Acetylcholine Receptors ◽  
Inhibitory Neurons ◽  
Cell Type ◽  
Specific Expression ◽  
Low Concentrations ◽  
Layer 4 ◽  
Cell Type Specific ◽  
Fast Spiking ◽  
Ach Receptors

The neuromodulator acetylcholine (ACh) plays an important role in arousal, attention, vigilance, learning and memory. ACh is released during different behavioural states and affects the brain microcircuit by regulating neuronal and synaptic properties. Here, we investigated how a low concentration of ACh (30 μM) affects the intrinsic properties of electrophysiologically and morphologically identified excitatory and inhibitory neurons in layer 4 (L4) of rat barrel cortex. ACh altered the membrane potential of L4 neurons in a heterogeneous manner. Nearly all L4 regular spiking (RS) neurons responded to bath-application of ACh with a M4 muscarinic ACh receptor-mediated hyperpolarisation. In contrast, in the majority of L4 fast spiking (FS) and non-fast spiking (nFS) interneurons 30 μM ACh induced a depolarisation while the remainder showed a hyperpolarisation or no response. The ACh-induced depolarisation of L4 FS interneurons was much weaker than that in L4 nFS interneurons. There was no clear difference in the response to ACh for three morphological subtypes of L4 FS interneurons. However, in four morpho-electrophysiological subtypes of L4 nFS interneurons, VIP+-like interneurons showed the strongest ACh-induced depolarisation; occasionally, even action potential (AP) firing was elicited. The ACh-induced depolarisation in L4 FS interneurons was exclusively mediated by M1 muscarinic ACh receptors; in L4 nFS interneurons it was mainly mediated by M1 and/or M3/5 muscarinic ACh receptors. In a subset of L4 nFS interneurons, a co-operative activation of nicotinic ACh receptors was also observed. The present study demonstrates that low-concentrations of ACh affect the different L4 neurons types in a cell-type specific way. These effects result from a specific expression of different muscarinic and/or nicotinic ACh receptors on the somatodendritic compartments of L4 neurons. This suggests that even at low concentrations ACh may tune the excitability of L4 excitatory and inhibitory neurons and their synaptic microcircuits differentially depending on the behavioural state during which ACh is released.

Neuronal Circuits in Barrel Cortex for Whisker Sensory Perception

2021 ◽  
Vol 101 (1) ◽  
pp. 353-415
Author(s):  
Jochen F. Staiger ◽  
Carl C. H. Petersen
Keyword(s):  
Barrel Cortex ◽  
Specific Activity ◽  
Sensory Information ◽  
Inhibitory Neurons ◽  
Future Research ◽  
Cell Type ◽  
Molecular Features ◽  
Somatotopic Map ◽  
Cell Type Specific ◽  
The Impact

The array of whiskers on the snout provides rodents with tactile sensory information relating to the size, shape and texture of objects in their immediate environment. Rodents can use their whiskers to detect stimuli, distinguish textures, locate objects and navigate. Important aspects of whisker sensation are thought to result from neuronal computations in the whisker somatosensory cortex (wS1). Each whisker is individually represented in the somatotopic map of wS1 by an anatomical unit named a ‘barrel’ (hence also called barrel cortex). This allows precise investigation of sensory processing in the context of a well-defined map. Here, we first review the signaling pathways from the whiskers to wS1, and then discuss current understanding of the various types of excitatory and inhibitory neurons present within wS1. Different classes of cells can be defined according to anatomical, electrophysiological and molecular features. The synaptic connectivity of neurons within local wS1 microcircuits, as well as their long-range interactions and the impact of neuromodulators, are beginning to be understood. Recent technological progress has allowed cell-type-specific connectivity to be related to cell-type-specific activity during whisker-related behaviors. An important goal for future research is to obtain a causal and mechanistic understanding of how selected aspects of tactile sensory information are processed by specific types of neurons in the synaptically connected neuronal networks of wS1 and signaled to downstream brain areas, thus contributing to sensory-guided decision-making.

scholarly journals Cell-type–specific neuromodulation guides synaptic credit assignment in a spiking neural network

2021 ◽  
Vol 118 (51) ◽  
pp. e2111821118
Author(s):  
Yuhan Helena Liu ◽  
Stephen Smith ◽  
Stefan Mihalas ◽  
Eric Shea-Brown ◽  
Uygar Sümbül
Keyword(s):  
Neural Network ◽  
Normative Theory ◽  
Synaptic Connections ◽  
Neuron Type ◽  
Cell Type ◽  
Credit Assignment ◽  
Neural Network Learning ◽  
Network Learning ◽  
Cell Type Specific ◽  
Synaptic Learning

Brains learn tasks via experience-driven differential adjustment of their myriad individual synaptic connections, but the mechanisms that target appropriate adjustment to particular connections remain deeply enigmatic. While Hebbian synaptic plasticity, synaptic eligibility traces, and top-down feedback signals surely contribute to solving this synaptic credit-assignment problem, alone, they appear to be insufficient. Inspired by new genetic perspectives on neuronal signaling architectures, here, we present a normative theory for synaptic learning, where we predict that neurons communicate their contribution to the learning outcome to nearby neurons via cell-type–specific local neuromodulation. Computational tests suggest that neuron-type diversity and neuron-type–specific local neuromodulation may be critical pieces of the biological credit-assignment puzzle. They also suggest algorithms for improved artificial neural network learning efficiency.

scholarly journals State-dependent cell-type-specific membrane potential dynamics and unitary synaptic inputs in awake mice

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Aurélie Pala ◽  
Carl CH Petersen
Keyword(s):  
Membrane Potential ◽  
Barrel Cortex ◽  
Field Potential ◽  
Low Frequency ◽  
Inhibitory Neuron ◽  
Single Layer ◽  
Cell Type ◽  
State Dependent ◽  
Layer 2 ◽  
Cell Type Specific

The cellular and synaptic mechanisms driving cell-type-specific function during various cortical network activities and behaviors are poorly understood. Here, we targeted whole-cell recordings to two classes of inhibitory GABAergic neurons in layer 2/3 of the barrel cortex of awake head-restrained mice and correlated spontaneous membrane potential dynamics with cortical state and whisking behavior. Using optogenetic stimulation of single layer 2/3 excitatory neurons we measured unitary excitatory postsynaptic potentials (uEPSPs) across states. During active states, characterized by whisking and reduced low-frequency activity in the local field potential, parvalbumin-expressing neurons depolarized and, albeit in a small number of recordings, received uEPSPs with increased amplitude. In contrast, somatostatin-expressing neurons hyperpolarized and reduced firing rates during active states without consistent change in uEPSP amplitude. These results further our understanding of neocortical inhibitory neuron function in awake mice and are consistent with the hypothesis that distinct genetically-defined cell classes have different state-dependent patterns of activity.

scholarly journals Cell type-specific regulation of inhibition via cannabinoid type 1 receptors in rat neocortex

2013 ◽  
Vol 109 (1) ◽  
pp. 216-224 ◽  
Author(s):  
Claire L. De-May ◽  
Afia B. Ali
Keyword(s):  
Synaptic Transmission ◽  
Pyramidal Cell ◽  
Metabotropic Glutamate Receptor ◽  
Pyramidal Cells ◽  
Cb1 Receptor ◽  
Cb1 Receptors ◽  
Cell Type ◽  
Group I ◽  
Cell Type Specific

Endogenous cannabinoid type 1 (CB1) receptors demonstrate a cell type-specific expression and are potent modulators of synaptic transmission within the central nervous system. We aimed to investigate whether two classes of multipolar interneuron in the neocortex displayed a form of short-term synaptic plasticity, depolarization-induced suppression of inhibition (DSI), and whether the DSI was mediated by a common receptor. Paired whole cell recordings combined with biocytin labeling were performed between pyramidal cells and either multipolar adapting or multipolar nonadapting interneurons in layers II–IV of male Wistar rat (postnatal day 17–22) somatosensory cortex. Inhibitory postsynaptic potentials elicited by multipolar adapting interneurons were sensitive to DSI, which was blocked by the CB1 receptor antagonist AM-251 (8 μM), indicating that the suppression of inhibition was mediated by CB1 receptors. Two subpopulations of multipolar nonadapting interneuron-to-pyramidal cell connections were discovered on the basis of their susceptibility to DSI. Whereas 50% were insensitive to DSI, the remaining half were sensitive to DSI, which could not be prevented by AM-251. DSI at these connections was also insensitive to the group I (mGluRIa) and III metabotropic glutamate receptor antagonists ( RS)-1-aminoindan-1,5-dicarboxylic acid (100 μM) and ( RS)-α-cyclopropyl-4-phosphonophenylglycine (100 μM) and the group III agonist l-2-amino-4-phosphonobutanoate (50 μM). However, multipolar nonadapting interneuron-to-pyramidal cell connections were sensitive to the endocannabinoid anandamide (9 μM), mimicking the effects of DSI, which also could not be prevented by AM-251, implying a CB1 receptor-independent suppression of inhibition. These results reveal an interneuron type-specific modulation of synaptic transmission via CB receptors in the neocortex.

Layer- and Cell-Type-Specific Effects of Neonatal Whisker-Trimming in Adult Rat Barrel Cortex

2007 ◽  
Vol 97 (6) ◽  
pp. 4380-4385 ◽  
Author(s):  
Soo-Hyun Lee ◽  
Peter W. Land ◽  
Daniel J. Simons
Keyword(s):  
Barrel Cortex ◽  
Sensory Deprivation ◽  
Cell Type ◽  
Growth Layer ◽  
Adult Rat ◽  
Specific Effects ◽  
Layer 2 ◽  
Layer 4 ◽  
Cell Type Specific ◽  
Fast Spike

Tactile deprivation in rats produced by whisker-trimming early in life leads to abnormally robust responses of excitatory neurons in layer 4 of primary somatosensory cortex when the re-grown whiskers are stimulated. Present findings from fast-spike neurons indicate that presumed inhibitory cells fire less robustly under the same conditions. These contrasting effects may reflect altered patterns of thalamocortical input to excitatory versus inhibitory cells and/or changes in the strength of intracortical connections. Despite increased excitability of layer 4, neurons in layer 2/3 respond at control levels even after full whisker re-growth. Layer 4 synapses onto supragranular neurons may be permanently depressed as a result of neonatal sensory deprivation.

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