scholarly journals The generation of cortical novelty responses through inhibitory plasticity

2020 ◽  
Author(s):  
Auguste Schulz ◽  
Christoph Miehl ◽  
Michael J. Berry ◽  
Julijana Gjorgjieva
Keyword(s):  
Temporal Structure ◽  
Inhibitory Neurons ◽  
Specific Adaptation ◽  
Spiking Network ◽  
Reliable Detection ◽  
Plausible Mechanism ◽  
Novelty Response ◽  
Inhibitory Plasticity ◽  
Familiar Stimuli ◽  
Synaptic Mechanisms

AbstractAnimals depend on fast and reliable detection of novel stimuli in their environment. Indeed, 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 inhibitory synaptic plasticity readily 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. Generated novelty responses do not depend on the exact temporal structure 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 numerous experimentally testable predictions.

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 Circuit and synaptic organization of forebrain-to-midbrain pathways that promote and suppress vocalization

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Valerie Michael ◽  
Jack Goffinet ◽  
John Pearson ◽  
Fan Wang ◽  
Katherine Tschida ◽  
...  
Keyword(s):  
Preoptic Area ◽  
Brain Slices ◽  
Social Cues ◽  
Ultrasonic Vocalizations ◽  
Behavioral Effects ◽  
Inhibitory Neurons ◽  
Boundary Zone ◽  
Synaptic Organization ◽  
Two Populations ◽  
Synaptic Mechanisms

Animals vocalize only in certain behavioral contexts, but the circuits and synapses through which forebrain neurons trigger or suppress vocalization remain unknown. Here, we used transsynaptic tracing to identify two populations of inhibitory neurons that lie upstream of neurons in the periaqueductal gray (PAG) that gate the production of ultrasonic vocalizations (USVs) in mice (i.e. PAG-USV neurons). Activating PAG-projecting neurons in the preoptic area of the hypothalamus (POAPAG neurons) elicited USV production in the absence of social cues. In contrast, activating PAG-projecting neurons in the central-medial boundary zone of the amygdala (AmgC/M-PAG neurons) transiently suppressed USV production without disrupting non-vocal social behavior. Optogenetics-assisted circuit mapping in brain slices revealed that POAPAG neurons directly inhibit PAG interneurons, which in turn inhibit PAG-USV neurons, whereas AmgC/M-PAG neurons directly inhibit PAG-USV neurons. These experiments identify two major forebrain inputs to the PAG that trigger and suppress vocalization, respectively, while also establishing the synaptic mechanisms through which these neurons exert opposing behavioral effects.

scholarly journals Target Interneuron Preference in Thalamocortical Pathways Determines the Temporal Structure of Cortical Responses

2018 ◽  
Vol 29 (7) ◽  
pp. 2815-2831 ◽  
Author(s):  
Y Audrey Hay ◽  
Jérémie Naudé ◽  
Philippe Faure ◽  
Bertrand Lambolez
Keyword(s):  
Temporal Structure ◽  
Sensory Information ◽  
Response Duration ◽  
Cortical Response ◽  
Inhibitory Neurons ◽  
Thalamic Nuclei ◽  
Response Dynamics ◽  
Mean Field Model ◽  
Local Circuits ◽  
Feedforward Inhibition

Abstract Sensory processing relies on fast detection of changes in environment, as well as integration of contextual cues over time. The mechanisms by which local circuits of the cerebral cortex simultaneously perform these opposite processes remain obscure. Thalamic “specific” nuclei relay sensory information, whereas “nonspecific” nuclei convey information on the environmental and behavioral contexts. We expressed channelrhodopsin in the ventrobasal specific (sensory) or the rhomboid nonspecific (contextual) thalamic nuclei. By selectively activating each thalamic pathway, we found that nonspecific inputs powerfully activate adapting (slow-responding) interneurons but weakly connect fast-spiking interneurons, whereas specific inputs exhibit opposite interneuron preference. Specific inputs thereby induce rapid feedforward inhibition that limits response duration, whereas, in the same cortical area, nonspecific inputs elicit delayed feedforward inhibition that enables lasting recurrent excitation. Using a mean field model, we confirm that cortical response dynamics depends on the type of interneuron targeted by thalamocortical inputs and show that efficient recruitment of adapting interneurons prolongs the cortical response and allows the summation of sensory and contextual inputs. Hence, target choice between slow- and fast-responding inhibitory neurons endows cortical networks with a simple computational solution to perform both sensory detection and integration.

scholarly journals Thalamocortical Spectral Transmission Relies on Balanced Input Strengths

2021 ◽  
Author(s):  
Matteo Saponati ◽  
Jordi Garcia-Ojalvo ◽  
Enrico Cataldo ◽  
Alberto Mazzoni
Keyword(s):  
Field Potential ◽  
Inhibitory Neurons ◽  
Feedforward Network ◽  
Sensory Transmission ◽  
Thalamocortical Connections ◽  
Primary Sensory Cortex ◽  
Spiking Network ◽  
Back Ground ◽  
Corticothalamic Feedback ◽  
The Brain

AbstractThe thalamus is a key element of sensory transmission in the brain, as it gates and selects sensory streams through a modulation of its internal activity. A preponderant role in these functions is played by its internal activity in the alpha range ([8–14] Hz), but the mechanism underlying this process is not completely understood. In particular, how do thalamocortical connections convey stimulus driven information selectively over the back-ground of thalamic internally generated activity? Here we investigate this issue with a spiking network model of feedforward connectivity between thalamus and primary sensory cortex reproducing the local field potential of both areas. We found that in a feedforward network, thalamic oscillations in the alpha range do not entrain cortical activity for two reasons: (i) alpha range oscillations are weaker in neurons projecting to the cortex, (ii) the gamma resonance dynamics of cortical networks hampers oscillations over the 10–20 Hz range thus weakening alpha range oscillations. This latter mechanism depends on the balance of the strength of thalamocortical connections toward excitatory and inhibitory neurons in the cortex. Our results highlight the relevance of corticothalamic feedback to sustain alpha range oscillations and pave the way toward an integrated understanding of the sensory streams traveling between the periphery and the cortex.

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 Excitatory and inhibitory receptors utilize distinct post- and trans-synaptic mechanisms in vivo

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Taisuke Miyazaki ◽  
Megumi Morimoto-Tomita ◽  
Coralie Berthoux ◽  
Kotaro Konno ◽  
Yoav Noam ◽  
...  
Keyword(s):  
Ampa Receptors ◽  
Ectopic Expression ◽  
Inhibitory Neurons ◽  
Mammalian Brain ◽  
Neurotransmitter Receptors ◽  
Presynaptic Terminals ◽  
Postsynaptic Receptors ◽  
A Cell ◽  
Synaptic Mechanisms

Ionotropic neurotransmitter receptors at postsynapses mediate fast synaptic transmission upon binding of the neurotransmitter. Post- and trans-synaptic mechanisms through cytosolic, membrane, and secreted proteins have been proposed to localize neurotransmitter receptors at postsynapses. However, it remains unknown which mechanism is crucial to maintain neurotransmitter receptors at postsynapses. In this study, we ablated excitatory or inhibitory neurons in adult mouse brains in a cell-autonomous manner. Unexpectedly, we found that excitatory AMPA receptors remain at the postsynaptic density upon ablation of excitatory presynaptic terminals. In contrast, inhibitory GABAA receptors required inhibitory presynaptic terminals for their postsynaptic localization. Consistent with this finding, ectopic expression at excitatory presynapses of neurexin 3alpha, a putative trans-synaptic interactor with the native GABAA receptor complex, could recruit GABAA receptors to contacted postsynaptic sites. These results establish distinct mechanisms for the maintenance of excitatory and inhibitory postsynaptic receptors in the mature mammalian brain.

scholarly journals Thalamocortical spectral transmission relies on balanced input strengths

2020 ◽  
Author(s):  
Matteo Saponati ◽  
Jordi Garcia-Ojalvo ◽  
Enrico Cataldo ◽  
Alberto Mazzoni
Keyword(s):  
Sensory Information ◽  
Field Potential ◽  
Sensory Cortex ◽  
Inhibitory Neurons ◽  
Spectral Transmission ◽  
Sensory Transmission ◽  
Thalamocortical Connections ◽  
Primary Sensory Cortex ◽  
Spiking Network ◽  
The Brain

AbstractThe thalamus is a key element of sensory transmission in the brain, as all sensory information is processed by the thalamus before reaching the cortex. The thalamus is known to gate and select sensory streams through a modulation of its internal activity in which spindle oscillations play a preponderant role, but the mechanism underlying this process is not completely understood. In particular, how do thalamocortical connections convey stimulus-driven information selectively over the background of thalamic internally generated activity (such as spindle oscillations)? Here we investigate this issue with a spiking network model of connectivity between thalamus and primary sensory cortex reproducing the local field potential of both areas. We found two features of the thalamocortical dynamics that filter out spindle oscillations: i) spindle oscillations are weaker in neurons projecting to the cortex, ii) the resonance dynamics of cortical networks selectively blocks frequency in the range encompassing spindle oscillations. This latter mechanism depends on the balance of the strength of thalamocortical connections toward excitatory and inhibitory neurons in the cortex. Our results pave the way toward an integrated understanding of the sensory streams traveling between the periphery and the cortex.

scholarly journals Counting on dis-inhibition: a circuit motif for interval counting and selectivity in the anuran auditory system

2015 ◽  
Vol 114 (5) ◽  
pp. 2804-2815 ◽  
Author(s):  
Richard Naud ◽  
Dave Houtman ◽  
Gary J. Rose ◽  
André Longtin
Keyword(s):  
Auditory System ◽  
Temporal Structure ◽  
Selective Inhibition ◽  
Inhibitory Neurons ◽  
Pulse Excitation ◽  
General Importance ◽  
Simple Connectivity ◽  
Parsimonious Model ◽  
Millisecond Range ◽  
Species Specific

Information can be encoded in the temporal patterning of spikes. How the brain reads these patterns is of general importance and represents one of the greatest challenges in neuroscience. We addressed this issue in relation to temporal pattern recognition in the anuran auditory system. Many species of anurans perform mating decisions based on the temporal structure of advertisement calls. One important temporal feature is the number of sound pulses that occur with a species-specific interpulse interval. Neurons representing this pulse count have been recorded in the anuran inferior colliculus, but the mechanisms underlying their temporal selectivity are incompletely understood. Here, we construct a parsimonious model that can explain the key dynamical features of these cells with biologically plausible elements. We demonstrate that interval counting arises naturally when combining interval-selective inhibition with pulse-per-pulse excitation having both fast- and slow-conductance synapses. Interval-dependent inhibition is modeled here by a simple architecture based on known physiology of afferent nuclei. Finally, we consider simple implementations of previously proposed mechanistic explanations for these counting neurons and show that they do not account for all experimental observations. Our results demonstrate that tens of millisecond-range temporal selectivities can arise from simple connectivity motifs of inhibitory neurons, without recourse to internal clocks, spike-frequency adaptation, or appreciable short-term plasticity.

scholarly journals Sensory coding and contrast invariance emerge from the control of plastic inhibition over emergent selectivity

2021 ◽  
Vol 17 (11) ◽  
pp. e1009566
Author(s):  
René Larisch ◽  
Lorenz Gönner ◽  
Michael Teichmann ◽  
Fred H. Hamker
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Gain Control ◽  
Metabolic Efficiency ◽  
Tuning Curves ◽  
Coding Efficiency ◽  
Spiking Network ◽  
Inhibitory Feedback ◽  
Efficient Code ◽  
Inhibitory Plasticity

Visual stimuli are represented by a highly efficient code in the primary visual cortex, but the development of this code is still unclear. Two distinct factors control coding efficiency: Representational efficiency, which is determined by neuronal tuning diversity, and metabolic efficiency, which is influenced by neuronal gain. How these determinants of coding efficiency are shaped during development, supported by excitatory and inhibitory plasticity, is only partially understood. We investigate a fully plastic spiking network of the primary visual cortex, building on phenomenological plasticity rules. Our results suggest that inhibitory plasticity is key to the emergence of tuning diversity and accurate input encoding. We show that inhibitory feedback (random and specific) increases the metabolic efficiency by implementing a gain control mechanism. Interestingly, this led to the spontaneous emergence of contrast-invariant tuning curves. Our findings highlight that (1) interneuron plasticity is key to the development of tuning diversity and (2) that efficient sensory representations are an emergent property of the resulting network.

scholarly journals Complementary control of sensory adaptation by two types of cortical interneurons

eLife ◽  
2015 ◽  
Vol 4 ◽  
Author(s):  
Ryan G Natan ◽  
John J Briguglio ◽  
Laetitia Mwilambwe-Tshilobo ◽  
Sara I Jones ◽  
Mark Aizenberg ◽  
...  
Keyword(s):  
Cortical Neurons ◽  
Primary Auditory Cortex ◽  
Inhibitory Neurons ◽  
Specific Inhibition ◽  
Sensory Adaptation ◽  
Cortical Circuits ◽  
Unexpected Events ◽  
Specific Adaptation ◽  
Cortical Interneurons ◽  
Excitatory Responses

Reliably detecting unexpected sounds is important for environmental awareness and survival. By selectively reducing responses to frequently, but not rarely, occurring sounds, auditory cortical neurons are thought to enhance the brain's ability to detect unexpected events through stimulus-specific adaptation (SSA). The majority of neurons in the primary auditory cortex exhibit SSA, yet little is known about the underlying cortical circuits. We found that two types of cortical interneurons differentially amplify SSA in putative excitatory neurons. Parvalbumin-positive interneurons (PVs) amplify SSA by providing non-specific inhibition: optogenetic suppression of PVs led to an equal increase in responses to frequent and rare tones. In contrast, somatostatin-positive interneurons (SOMs) selectively reduce excitatory responses to frequent tones: suppression of SOMs led to an increase in responses to frequent, but not to rare tones. A mutually coupled excitatory-inhibitory network model accounts for distinct mechanisms by which cortical inhibitory neurons enhance the brain's sensitivity to unexpected sounds.

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