Organization and Plasticity of Cortical Inhibition

2017 ◽  
Author(s):  
Bernard Kripkee ◽  
Robert C. Froemke
Keyword(s):  
Neural Activity ◽  
Cortical Inhibition ◽  
Network Activity ◽  
Inhibitory Neurons ◽  
Inhibitory Synapses ◽  
Inhibitory Interneurons ◽  
Excitatory Synapses ◽  
Different Types ◽  
Inhibitory Plasticity

Plasticity of inhibitory synapses keeps inhibition in balance and in register with excitation when changes occur in excitatory synapses. Inhibition has many functions to perform, and there are many kinds of inhibitory neurons to perform various computations and regulate network activity. Different forms of long-term changes in inhibitory synapses have been demonstrated that depend on neural activity. Inhibitory plasticity appears to be partly responsible for the specificity of the inhibitory connections needed to carry out some inhibitory functions. The evolving story of cortical inhibitory plasticity shows that different types of inhibitory interneurons play different roles in a variety of inhibitory functions, that several types of inhibitory plasticity have been attested, and that different forms of plasticity can be expected to have different effects on the organization and specificity of inhibitory connections.

scholarly journals Hippocampal Somatostatin Interneurons, Long-Term Synaptic Plasticity and Memory

2021 ◽  
Vol 15 ◽  
Author(s):  
Eve Honoré ◽  
Abdessattar Khlaifia ◽  
Anthony Bosson ◽  
Jean-Claude Lacaille
Keyword(s):  
Synaptic Plasticity ◽  
Learning And Memory ◽  
Inhibitory Neurons ◽  
Inhibitory Interneurons ◽  
Excitatory Synapses ◽  
Dynamic Regulation ◽  
Hippocampal Network ◽  
Hippocampal Networks ◽  
Hippocampal Structure

A distinctive feature of the hippocampal structure is the diversity of inhibitory interneurons. These complex inhibitory interconnections largely contribute to the tight modulation of hippocampal circuitry, as well as to the formation and coordination of neuronal assemblies underlying learning and memory. Inhibitory interneurons provide more than a simple transitory inhibition of hippocampal principal cells (PCs). The synaptic plasticity of inhibitory neurons provides long-lasting changes in the hippocampal network and is a key component of memory formation. The dendrite targeting interneurons expressing the peptide somatostatin (SOM) are particularly interesting in this regard because they display unique long-lasting synaptic changes leading to metaplastic regulation of hippocampal networks. In this article, we examine the actions of the neuropeptide SOM on hippocampal cells, synaptic plasticity, learning, and memory. We address the different subtypes of hippocampal SOM interneurons. We describe the long-term synaptic plasticity that takes place at the excitatory synapses of SOM interneurons, its singular induction and expression mechanisms, as well as the consequences of these changes on the hippocampal network, learning, and memory. We also review evidence that astrocytes provide cell-specific dynamic regulation of inhibition of PC dendrites by SOM interneurons. Finally, we cover how, in mouse models of Alzheimer’s disease (AD), dysfunction of plasticity of SOM interneuron excitatory synapses may also contribute to cognitive impairments in brain disorders.

scholarly journals Heterosynaptic GABAergic plasticity bidirectionally driven by the activity of pre- and postsynaptic NMDA receptors

2016 ◽  
Vol 113 (35) ◽  
pp. 9898-9903 ◽  
Author(s):  
Jonathan Mapelli ◽  
Daniela Gandolfi ◽  
Antonietta Vilella ◽  
Michele Zoli ◽  
Albertino Bigiani
Keyword(s):  
Nmda Receptor ◽  
Granule Cells ◽  
Dynamic Control ◽  
Long Term Potentiation ◽  
Receptor Activation ◽  
Network Activity ◽  
Inhibitory Synapses ◽  
Golgi Cells ◽  
Neural Information

Dynamic changes of the strength of inhibitory synapses play a crucial role in processing neural information and in balancing network activity. Here, we report that the efficacy of GABAergic connections between Golgi cells and granule cells in the cerebellum is persistently altered by the activity of glutamatergic synapses. This form of plasticity is heterosynaptic and is expressed as an increase (long-term potentiation, LTPGABA) or a decrease (long-term depression, LTDGABA) of neurotransmitter release. LTPGABA is induced by postsynaptic NMDA receptor activation, leading to calcium increase and retrograde diffusion of nitric oxide, whereas LTDGABA depends on presynaptic NMDA receptor opening. The sign of plasticity is determined by the activation state of target granule and Golgi cells during the induction processes. By controlling the timing of spikes emitted by granule cells, this form of bidirectional plasticity provides a dynamic control of the granular layer encoding capacity.

scholarly journals Untangling stability and gain modulation in cortical circuits with multiple interneuron classes

2020 ◽  
Author(s):  
Hannah Bos ◽  
Anne-Marie Oswald ◽  
Brent Doiron
Keyword(s):  
Pyramidal Neurons ◽  
Mean Field ◽  
Gain Control ◽  
Cell Types ◽  
High Gain ◽  
Cortical Inhibition ◽  
Network Activity ◽  
Inhibitory Neurons ◽  
Neuron Models ◽  
Cortical Circuit

AbstractSynaptic inhibition is the mechanistic backbone of a suite of cortical functions, not the least of which is maintaining overall network stability as well as modulating neuronal gain. Past cortical models have assumed simplified recurrent networks in which all inhibitory neurons are lumped into a single effective pool. In such models the mechanics of inhibitory stabilization and gain control are tightly linked in opposition to one another – meaning high gain coincides with low stability and vice versa. This tethering of stability and response gain restricts the possible operative regimes of the network. However, it is now well known that cortical inhibition is very diverse, with molecularly distinguished cell classes having distinct positions within the cortical circuit. In this study, we analyze populations of spiking neuron models and associated mean-field theories capturing circuits with pyramidal neurons as well as parvalbumin (PV) and somatostatin (SOM) expressing interneurons. Our study outlines arguments for a division of labor within the full cortical circuit where PV interneurons are ideally positioned to stabilize network activity, whereas SOM interneurons serve to modulate pyramidal cell gain. This segregation of inhibitory function supports stable cortical dynamics over a large range of modulation states. Our study offers a blueprint for how to relate the circuit structure of cortical networks with diverse cell types to the underlying population dynamics and stimulus response.

scholarly journals Measuring Learning in the Blink of an Eye: Adolescents' Neurophysiological Reactions Predict Long-Term Memory for Stories

2021 ◽  
Vol 5 ◽  
Author(s):  
Rebecca J. M. Gotlieb ◽  
Xiao-Fei Yang ◽  
Mary Helen Immordino-Yang
Keyword(s):  
Neural Activity ◽  
Default Mode Network ◽  
Cued Recall ◽  
Network Activity ◽  
Long Term Memory ◽  
Blink Rate ◽  
Additive Variance ◽  
Term Memory ◽  
Default Mode

Anticipating what adolescents will remember is a common goal in education research, but what tools allow us to predict adolescents' memory without interrupting the learning process as it naturally occurs? To attempt to identify neurophysiological markers of deep processing that may predict long-term retention, here we conducted an exploratory study by adding a cued recall probe to the last wave of data collection in a longitudinal psychosocial and neuroimaging study of 65 urban adolescents. Five years prior, and again 3 years prior, participants had reacted to the same emotionally evocative true stories during a videotaped interview that allowed us to measure eye-blink rate (EBR), and again during fMRI scanning. We analyzed EBR and neural data from the initial story exposure. We found that memory for a story was predicted by both EBR (a proxy for striatal dopamine) and default mode network neural activity to that story (involved in integrative memory and processing of emotional feelings). EBR and default mode network activity were uncorrelated and explained additive variance. Though more work is needed, our study contributes preliminary supportive evidence linking EBR and neural activity trial-by-trial to long-term memory in a naturalistic task. The analyses suggest that including EBR, a non-invasive, portable, and inexpensive measure that can be coded from high-quality video recording, could be useful in future studies of adolescents' learning.

Presynaptic Activity and Ca2+ Entry Are Required for the Maintenance of NMDA Receptor–Independent LTP at Visual Cortical Excitatory Synapses

2004 ◽  
Vol 92 (2) ◽  
pp. 1077-1087 ◽  
Author(s):  
Hong Nian Liu ◽  
Tohru Kurotani ◽  
Ming Ren ◽  
Kazumasa Yamada ◽  
Yumiko Yoshimura ◽  
...  
Keyword(s):  
Nmda Receptor ◽  
Long Term Potentiation ◽  
Inhibitory Synapses ◽  
Excitatory Synapses ◽  
Test Stimulation ◽  
Term Potentiation ◽  
Pharmacological Blockade ◽  
Visual Cortical ◽  
P Type

We have shown that some neural activity is required for the maintenance of long-term potentiation (LTP) at visual cortical inhibitory synapses. We tested whether this was also the case in N-methyl-d-aspartate (NMDA) receptor–independent LTP of excitatory connections in layer 2/3 cells of developing rat visual cortex. This LTP occurred after 2-Hz stimulation was applied for 15 min and always persisted for several hours while test stimulation was continued at 0.1 Hz. When test stimulation was stopped for 1 h after LTP induction, only one-third of the LTP instances disappeared, but most did disappear under a pharmacological suppression of spontaneous firing, indicating that LTP maintenance requires either evoked or spontaneous activities. LTP was totally abolished by a temporary blockade of action potentials with lidocaine or the removal of extracellular Ca2+ after LTP induction, but it persisted under a voltage clamp of postsynaptic cells or after a temporary blockade of postsynaptic activity with the glutamate receptor antagonist kynurenate, suggesting that LTP maintenance requires presynaptic, but not postsynaptic, firing and Ca2+ entry. More than one-half of the LTP instances were abolished after a pharmacological blockade of P-type Ca2+ channels, whereas it persisted after either L-type or Ni2+-sensitive Ca2+ channel blockades. These results show that the maintenance of NMDA receptor–independent excitatory LTP requires presynaptic firing and Ca2+ channel activation as inhibitory LTP, although the necessary level of firing and Ca2+ entry seems lower for the former than the latter and the Ca2+ channel types involved are only partly the same.

scholarly journals Inhibitory microcircuits for top-down plasticity of sensory representations

2019 ◽  
Vol 10 (1) ◽  
Author(s):  
Katharina Anna Wilmes ◽  
Claudia Clopath
Keyword(s):  
Inhibitory Neurons ◽  
Translation Invariance ◽  
Stage Model ◽  
Top Down ◽  
Inhibitory Circuits ◽  
Stimulus Representation ◽  
Pyramidal Layer ◽  
Inhibitory Plasticity ◽  
Experimental Findings

Abstract Rewards influence plasticity of early sensory representations, but the underlying changes in circuitry are unclear. Recent experimental findings suggest that inhibitory circuits regulate learning. In addition, inhibitory neurons are highly modulated by diverse long-range inputs, including reward signals. We, therefore, hypothesise that inhibitory plasticity plays a major role in adjusting stimulus representations. We investigate how top-down modulation by rewards interacts with local plasticity to induce long-lasting changes in circuitry. Using a computational model of layer 2/3 primary visual cortex, we demonstrate how interneuron circuits can store information about rewarded stimuli to instruct long-term changes in excitatory connectivity in the absence of further reward. In our model, stimulus-tuned somatostatin-positive interneurons develop strong connections to parvalbumin-positive interneurons during reward such that they selectively disinhibit the pyramidal layer henceforth. This triggers excitatory plasticity, leading to increased stimulus representation. We make specific testable predictions and show that this two-stage model allows for translation invariance of the learned representation.

scholarly journals Sustained Activation of PV+ Interneurons in Core Auditory Cortex Enables Robust Divisive Gain Control for Complex and Naturalistic Stimuli

2019 ◽  
Author(s):  
Tina Gothner ◽  
Pedro J. Gonçalves ◽  
Maneesh Sahani ◽  
Jennifer F. Linden ◽  
K. Jannis Hildebrandt
Keyword(s):  
Auditory Cortex ◽  
Gain Control ◽  
Recurrent Network ◽  
Cortical Inhibition ◽  
Network Activity ◽  
Inhibitory Interneurons ◽  
Simple Complex ◽  
Internal States ◽  
Sensory Cortices ◽  
Sustained Activation

ABSTRACTSensory cortices must flexibly adapt their operations to internal states and external requirements. Modulation of specific inhibitory interneurons may provide a network-level mechanism for adjustments on behaviourally relevant timescales. Understanding of the computational roles of such modulation has mostly been restricted to phasic optogenetic activation and short, transient stimuli. Here, we aimed to extend the understanding of modulation of cortical inhibition by using sustained, network-wide optogenetic activation of parvalbumin-positive interneurons in core auditory cortex to study modulation of responses to transient, sustained, and naturalistic stimuli. We found highly conserved spectral and temporal tuning, despite profoundly reduced overall network activity. This reduction was predominantly divisive, and consistent across simple, complex, and naturalistic stimuli. A recurrent network model with power-law input-output functions replicated our results. We conclude that modulation of parvalbumin-positive interneurons on timescales typical of more sustained neuromodulation may provide a means for robust divisive gain control conserving stimulus representations.

scholarly journals The generation of cortical novelty responses through inhibitory plasticity

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Auguste Schulz ◽  
Christoph Miehl ◽  
Michael J Berry ◽  
Julijana Gjorgjieva
Keyword(s):  
Spike Timing ◽  
Inhibitory Neurons ◽  
Excitatory Synapses ◽  
Spiking Network ◽  
Reliable Detection ◽  
Plausible Mechanism ◽  
Novelty Response ◽  
Inhibitory Plasticity ◽  
Familiar Stimuli ◽  
Synaptic Mechanisms

Animals depend on fast and reliable detection of novel stimuli in their environment. Neurons in multiple sensory areas respond more strongly to novel in comparison to familiar stimuli. Yet, it remains unclear which circuit, cellular, and synaptic mechanisms underlie those responses. Here, we show that spike-timing-dependent plasticity of inhibitory-to-excitatory synapses generates novelty responses in a recurrent spiking network model. Inhibitory plasticity increases the inhibition onto excitatory neurons tuned to familiar stimuli, while inhibition for novel stimuli remains low, leading to a network novelty response. The generation of novelty responses does not depend on the periodicity but rather on the distribution of presented stimuli. By including tuning of inhibitory neurons, the network further captures stimulus-specific adaptation. Finally, we suggest that disinhibition can control the amplification of novelty responses. Therefore, inhibitory plasticity provides a flexible, biologically plausible mechanism to detect the novelty of bottom-up stimuli, enabling us to make experimentally testable predictions.

scholarly journals Interneuron-specific plasticity at parvalbumin and somatostatin inhibitory synapses onto CA1 pyramidal neurons shapes hippocampal output

2019 ◽  
Author(s):  
Matt Udakis ◽  
Victor Pedrosa ◽  
Sophie E.L. Chamberlain ◽  
Claudia Clopath ◽  
Jack R Mellor
Keyword(s):  
Pyramidal Neurons ◽  
Physiological Activity ◽  
Activity Patterns ◽  
Pyramidal Cells ◽  
Network Activity ◽  
Inhibitory Synapses ◽  
Ca1 Pyramidal Cells ◽  
Hippocampal Cell ◽  
Hippocampal Network

SummaryThe formation and maintenance of spatial representations within hippocampal cell assemblies is strongly dictated by patterns of inhibition from diverse interneuron populations. Although it is known that inhibitory synaptic strength is malleable, induction of long-term plasticity at distinct inhibitory synapses and its regulation of hippocampal network activity is not well understood. Here, we show that inhibitory synapses from parvalbumin and somatostatin expressing interneurons undergo long-term depression and potentiation respectively (PV-iLTD and SST-iLTP) during physiological activity patterns. Both forms of plasticity rely on T-type calcium channel activation to confer synapse specificity but otherwise employ distinct mechanisms. Since parvalbumin and somatostatin interneurons preferentially target perisomatic and distal dendritic regions respectively of CA1 pyramidal cells, PV-iLTD and SST-iLTP coordinate a reprioritisation of excitatory inputs from entorhinal cortex and CA3. Furthermore, circuit-level modelling reveals that PV-iLTD and SST-iLTP cooperate to stabilise place cells while facilitating representation of multiple unique environments within the hippocampal network.

Modulation of Cellular and Synaptic Variability in the Lamprey Spinal Cord

2007 ◽  
Vol 97 (1) ◽  
pp. 44-56 ◽  
Author(s):  
David Parker ◽  
Sarah Bevan
Keyword(s):  
Spinal Cord ◽  
Substance P ◽  
Motor Neurons ◽  
Network Activity ◽  
Inhibitory Interneurons ◽  
Additional Source ◽  
Mean Values ◽  
Different Types ◽  
Network Properties ◽  
Synaptic Variability

Variability is increasingly recognized as a characteristic feature of cellular, synaptic, and network properties. While studies have traditionally focused on mean values, significant effects can result from changes in variance. This study has examined cellular and synaptic variability in the lamprey spinal cord and its modulation by the neuropeptide substance P. Cellular and synaptic variability differed in different types of cell and synapse. Substance P reduced the variability of subthreshold locomotor-related depolarizations and spiking in motor neurons during network activity. These effects were associated with a reduction in the variability of spiking in glutamatergic excitatory network interneurons and with a reduction in the variance of excitatory interneuron-evoked excitatory postsynaptic potentials (EPSPs). Substance P also reduced the variance of postsynpatic potentials (PSPs) from crossing inhibitory and excitatory interneurons, but it increased the variance of inhibitory postsynpatic potentials (IPSPs) from ipsilateral inhibitory interneurons. The effects on the variance of different PSPs could occur with or without changes in the PSP amplitude. The reduction in the variance of excitatory interneuron-evoked EPSPs was protein kinase A, calcium, and N-methyl-d-aspartate (NMDA) dependent. The NMDA dependence suggested that substance P was acting postsynaptically. This was supported by the reduced variability of postsynaptic responses to glutamate by substance P. However, ultrastructural analyses suggested that there may also be a presynaptic component to the modulation, because substance P reduced the variability of synaptic vesicle diameters in putative glutamatergic terminals. These results suggest that cellular and synaptic variability can be targeted for modulation, making it an additional source of spinal cord plasticity.

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