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.

scholarly journals Synaptic Mechanisms for Bandwidth Tuning in Awake Mouse Primary Auditory Cortex

2018 ◽  
Vol 29 (7) ◽  
pp. 2998-3009 ◽  
Author(s):  
Haifu Li ◽  
Feixue Liang ◽  
Wen Zhong ◽  
Linqing Yan ◽  
Lucas Mesik ◽  
...  
Keyword(s):  
Auditory Cortex ◽  
Cortical Neurons ◽  
Primary Auditory Cortex ◽  
Cell Voltage ◽  
Inhibitory Neurons ◽  
Complex Sounds ◽  
Excitatory Neurons ◽  
Layer 4 ◽  
Bandwidth Tuning ◽  
Spatial Size

Abstract Spatial size tuning in the visual cortex has been considered as an important neuronal functional property for sensory perception. However, an analogous mechanism in the auditory system has remained controversial. In the present study, cell-attached recordings in the primary auditory cortex (A1) of awake mice revealed that excitatory neurons can be categorized into three types according to their bandwidth tuning profiles in response to band-passed noise (BPN) stimuli: nonmonotonic (NM), flat, and monotonic, with the latter two considered as non-tuned for bandwidth. The prevalence of bandwidth-tuned (i.e., NM) neurons increases significantly from layer 4 to layer 2/3. With sequential cell-attached and whole-cell voltage-clamp recordings from the same neurons, we found that the bandwidth preference of excitatory neurons is largely determined by the excitatory synaptic input they receive, and that the bandwidth selectivity is further enhanced by flatly tuned inhibition observed in all cells. The latter can be attributed at least partially to the flat tuning of parvalbumin inhibitory neurons. The tuning of auditory cortical neurons for bandwidth of BPN may contribute to the processing of complex sounds.

scholarly journals Spatiotemporal constraints on optogenetic inactivation in cortical circuits

eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Nuo Li ◽  
Susu Chen ◽  
Zengcai V Guo ◽  
Han Chen ◽  
Yan Huo ◽  
...  
Keyword(s):  
Cortical Neurons ◽  
Pyramidal Neurons ◽  
Inhibitory Neurons ◽  
Dependent Manner ◽  
Cortical Circuits ◽  
Neuronal Populations ◽  
Multiple Length Scales ◽  
Dose Dependent ◽  
Reduced Activity

Optogenetics allows manipulations of genetically and spatially defined neuronal populations with excellent temporal control. However, neurons are coupled with other neurons over multiple length scales, and the effects of localized manipulations thus spread beyond the targeted neurons. We benchmarked several optogenetic methods to inactivate small regions of neocortex. Optogenetic excitation of GABAergic neurons produced more effective inactivation than light-gated ion pumps. Transgenic mice expressing the light-dependent chloride channel GtACR1 produced the most potent inactivation. Generally, inactivation spread substantially beyond the photostimulation light, caused by strong coupling between cortical neurons. Over some range of light intensity, optogenetic excitation of inhibitory neurons reduced activity in these neurons, together with pyramidal neurons, a signature of inhibition-stabilized neural networks ('paradoxical effect'). The offset of optogenetic inactivation was followed by rebound excitation in a light dose-dependent manner, limiting temporal resolution. Our data offer guidance for the design of in vivo optogenetics experiments.

scholarly journals AIM: A Network Model of Attention in Auditory Cortex

2020 ◽  
Author(s):  
Kenny F. Chou ◽  
Kamal Sen
Keyword(s):  
Auditory Cortex ◽  
Network Model ◽  
Frequency Tuning ◽  
Primary Auditory Cortex ◽  
Inhibitory Neurons ◽  
Cortical Circuits ◽  
Cocktail Party ◽  
Theoretical Frameworks ◽  
Cocktail Party Problem ◽  
Underlying Mechanisms

AbstractAttentional modulation of cortical networks is critical for the cognitive flexibility required to process complex scenes. Current theoretical frameworks for attention are based almost exclusively on studies in visual cortex, where attentional effects are typically modest and excitatory. In contrast, attentional effects in auditory cortex can be large and suppressive. A theoretical framework for explaining attentional effects in auditory cortex is lacking, preventing a broader understanding of cortical mechanisms underlying attention. Here, we present a cortical network model of attention in primary auditory cortex (A1). A key mechanism in our network is attentional inhibitory modulation (AIM) of cortical inhibitory neurons. In this mechanism, top-down inhibitory neurons disinhibit bottom-up cortical circuits, a prominent circuit motif observed in sensory cortex. Our results reveal that the same underlying mechanisms in the AIM network can explain diverse attentional effects on both spatial and frequency tuning in A1. We find that a dominant effect of disinhibition on cortical tuning is suppressive, consistent with experimental observations. Functionally, the AIM network may play a key role in solving the cocktail party problem. We demonstrate how attention can guide the AIM network to monitor an acoustic scene, select a specific target, or switch to a different target, providing flexible outputs for solving the cocktail party problem.

scholarly journals AIM: A network model of attention in auditory cortex

2021 ◽  
Vol 17 (8) ◽  
pp. e1009356
Author(s):  
Kenny F. Chou ◽  
Kamal Sen
Keyword(s):  
Auditory Cortex ◽  
Network Model ◽  
Frequency Tuning ◽  
Primary Auditory Cortex ◽  
Inhibitory Neurons ◽  
Cortical Circuits ◽  
Cocktail Party ◽  
Theoretical Frameworks ◽  
Cocktail Party Problem ◽  
Underlying Mechanisms

Attentional modulation of cortical networks is critical for the cognitive flexibility required to process complex scenes. Current theoretical frameworks for attention are based almost exclusively on studies in visual cortex, where attentional effects are typically modest and excitatory. In contrast, attentional effects in auditory cortex can be large and suppressive. A theoretical framework for explaining attentional effects in auditory cortex is lacking, preventing a broader understanding of cortical mechanisms underlying attention. Here, we present a cortical network model of attention in primary auditory cortex (A1). A key mechanism in our network is attentional inhibitory modulation (AIM) of cortical inhibitory neurons. In this mechanism, top-down inhibitory neurons disinhibit bottom-up cortical circuits, a prominent circuit motif observed in sensory cortex. Our results reveal that the same underlying mechanisms in the AIM network can explain diverse attentional effects on both spatial and frequency tuning in A1. We find that a dominant effect of disinhibition on cortical tuning is suppressive, consistent with experimental observations. Functionally, the AIM network may play a key role in solving the cocktail party problem. We demonstrate how attention can guide the AIM network to monitor an acoustic scene, select a specific target, or switch to a different target, providing flexible outputs for solving the cocktail party problem.

scholarly journals Equations governing dynamics of excitation and inhibition in the mouse corticothalamic network

2020 ◽  
Author(s):  
I-Chun Lin ◽  
Michael Okun ◽  
Matteo Carandini ◽  
Kenneth D. Harris
Keyword(s):  
Cortical Neurons ◽  
Mean Field ◽  
Inhibitory Neurons ◽  
Cortical Circuits ◽  
Mean Field Model ◽  
Population Activity ◽  
Cortical Dynamics ◽  
Mean Field Models ◽  
Cortical Responses ◽  
Mouse Visual Cortex

Although cortical circuits are complex and interconnected with the rest of the brain, their macroscopic dynamics are often approximated by modeling the averaged activities of excitatory and inhibitory cortical neurons, without interactions with other brain circuits. To verify the validity of such mean-field models, we optogenetically stimulated populations of excitatory and parvalbumin-expressing inhibitory neurons in awake mouse visual cortex, while recording population activity in cortex and in its thalamic correspondent, the lateral geniculate nucleus. The cortical responses to brief test pulses could not be explained by a mean-field model including only cortical excitatory and inhibitory populations. However, these responses could be predicted by extending the model to include thalamic interactions that cause net cortical suppression following activation of cortical excitatory neurons. We conclude that mean-field models can accurately summarize cortical dynamics, but only when the cortex is considered as part of a dynamic corticothalamic network.

scholarly journals Cortical interneurons ensure maintenance of frequency tuning following adaptation

2017 ◽  
Author(s):  
Ryan G. Natan ◽  
Winnie Rao ◽  
Maria N. Geffen
Keyword(s):  
Frequency Response ◽  
Response Function ◽  
Cortical Neurons ◽  
Frequency Response Function ◽  
Frequency Tuning ◽  
Inhibitory Neurons ◽  
Sensory Stimuli ◽  
Cortical Interneurons ◽  
Excitatory Neurons ◽  
Shape Tuning

AbstractNeurons throughout the sensory pathway are tuned to specific aspects of stimuli. This selectivity is shaped by feedforward and recurrent excitatory-inhibitory interactions. In the auditory cortex (AC), two large classes of interneurons, parvalbumin- (PVs) and somatostatin- positive (SOMs) interneurons, differentially modulate frequency-dependent responses across the frequency response function of excitatory neurons. At the same time, the responsiveness of neurons in AC to sounds is dependent on the temporal context, with the majority of neurons exhibiting adaptation to repeated sounds. Here, we asked whether and how inhibitory neurons shape the frequency response function of excitatory neurons as a function of adaptation to temporal repetition of tones. The effects of suppressing both SOMs and PVs diverged for responses to preferred versus non-preferred frequencies following adaptation. Prior to adaptation, suppressing either SOM or PV inhibition drove both increases and decreases in spiking activity among cortical neurons. After adaptation, suppressing SOM activity caused predominantly disinhibitory effects, whereas suppressing PV activity still evoked bi-directional changes. SOM, but not PV-driven inhibition dynamically modulated frequency tuning as a function of adaptation. Additionally, testing across frequency tuning revealed that, unlike PVs, SOM-driven inhibition exhibited gain-like increases reflective of adaptation. Our findings suggest that distinct cortical interneurons differentially shape tuning to sensory stimuli across the neuronal receptive field, maintaining frequency selectivity of excitatory neurons during adaptation.

scholarly journals Role of somatostatin-positive cortical interneurons in the generation of sleep slow waves

2017 ◽  
Author(s):  
Chadd M. Funk ◽  
Kayla Peelman ◽  
Michele Bellesi ◽  
William Marshall ◽  
Chiara Cirelli ◽  
...  
Keyword(s):  
Slow Wave ◽  
Cortical Neurons ◽  
Nrem Sleep ◽  
Slow Waves ◽  
Inhibitory Neurons ◽  
Excitatory Transmission ◽  
Cortical Interneurons ◽  
Somatic Inhibition ◽  
Apical Dendrites

SUMMARYCortical slow waves – the hallmark of NREM sleep - reflect near-synchronous OFF periods in cortical neurons. However, the mechanisms triggering such OFF periods are unclear, as there is little evidence for somatic inhibition. We studied cortical inhibitory interneurons that express somatostatin (SOM), because ∼70% of them are Martinotti cells that target diffusely layer 1 and can block excitatory transmission presynaptically, at glutamatergic terminals, and postsynaptically, at apical dendrites, without inhibiting the soma. In freely moving mice, we show that SOM+ cells can fire immediately before slow waves and their optogenetic stimulation triggers neuronal OFF periods during sleep. Next, we show that chemogenetic activation of SOM+ cells increases slow wave activity (SWA), the slope of individual slow waves, and the duration of NREM sleep; whereas their chemogenetic inhibition decreases SWA and slow wave incidence without changing time spent asleep. By contrast, activation of parvalbumin+ (PV+) cells, the most numerous population of cortical inhibitory neurons, greatly decreases SWA and cortical firing. These results indicate that SOM+ cells, but not PV+ cells, are involved in the generation of sleep slow waves. Whether Martinotti cells are solely responsible for this effect, or are complemented by other classes of inhibitory neurons, remains to be investigated.

scholarly journals Subcortical circuits mediate communication between primary sensory cortical areas in mice

2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Michael Lohse ◽  
Johannes C. Dahmen ◽  
Victoria M. Bajo ◽  
Andrew J. King
Keyword(s):  
Cortical Neurons ◽  
Common Property ◽  
Primary Auditory Cortex ◽  
Facilitatory Effect ◽  
Thalamic Nuclei ◽  
Auditory Midbrain ◽  
Cortical Areas ◽  
Auditory Responses ◽  
Evoked Activity

AbstractIntegration of information across the senses is critical for perception and is a common property of neurons in the cerebral cortex, where it is thought to arise primarily from corticocortical connections. Much less is known about the role of subcortical circuits in shaping the multisensory properties of cortical neurons. We show that stimulation of the whiskers causes widespread suppression of sound-evoked activity in mouse primary auditory cortex (A1). This suppression depends on the primary somatosensory cortex (S1), and is implemented through a descending circuit that links S1, via the auditory midbrain, with thalamic neurons that project to A1. Furthermore, a direct pathway from S1 has a facilitatory effect on auditory responses in higher-order thalamic nuclei that project to other brain areas. Crossmodal corticofugal projections to the auditory midbrain and thalamus therefore play a pivotal role in integrating multisensory signals and in enabling communication between different sensory cortical areas.

scholarly journals Aberrant development of excitatory circuits to inhibitory neurons in the primary visual cortex after neonatal binocular enucleation

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Rongkang Deng ◽  
Joseph P. Y. Kao ◽  
Patrick O. Kanold
Keyword(s):  
Visual Cortex ◽  
Nmda Receptors ◽  
Laser Scanning ◽  
Inhibitory Neurons ◽  
Gabaergic Interneurons ◽  
Cortical Circuits ◽  
Retinal Input ◽  
Layer 4 ◽  
Ampa And Nmda Receptors ◽  
Laser Scanning Photostimulation

AbstractThe development of GABAergic interneurons is important for the functional maturation of cortical circuits. After migrating into the cortex, GABAergic interneurons start to receive glutamatergic connections from cortical excitatory neurons and thus gradually become integrated into cortical circuits. These glutamatergic connections are mediated by glutamate receptors including AMPA and NMDA receptors and the ratio of AMPA to NMDA receptors decreases during development. Since previous studies have shown that retinal input can regulate the early development of connections along the visual pathway, we investigated if the maturation of glutamatergic inputs to GABAergic interneurons in the visual cortex requires retinal input. We mapped the spatial pattern of glutamatergic connections to layer 4 (L4) GABAergic interneurons in mouse visual cortex at around postnatal day (P) 16 by laser-scanning photostimulation and investigated the effect of binocular enucleations at P1/P2 on these patterns. Gad2-positive interneurons in enucleated animals showed an increased fraction of AMPAR-mediated input from L2/3 and a decreased fraction of input from L5/6. Parvalbumin-expressing (PV) interneurons showed similar changes in relative connectivity. NMDAR-only input was largely unchanged by enucleation. Our results show that retinal input sculpts the integration of interneurons into V1 circuits and suggest that the development of AMPAR- and NMDAR-only connections might be regulated differently.

Representation of Spectral and Temporal Envelope of Twitter Vocalizations in Common Marmoset Primary Auditory Cortex

2002 ◽  
Vol 87 (4) ◽  
pp. 1723-1737 ◽  
Author(s):  
Srikantan S. Nagarajan ◽  
Steven W. Cheung ◽  
Purvis Bedenbaugh ◽  
Ralph E. Beitel ◽  
Christoph E. Schreiner ◽  
...  
Keyword(s):  
Cortical Neurons ◽  
Social Contact ◽  
Primary Auditory Cortex ◽  
Common Marmoset ◽  
Spectral Envelope ◽  
Response Patterns ◽  
Temporal Envelope ◽  
Degraded Speech ◽  
Neurophysiological Data ◽  
Narrowband Channels

Cortical sensitivity in representations of behaviorally relevant complex input signals was examined in recordings from primary auditory cortical neurons (AI) in adult, barbiturate-anesthetized common marmoset monkeys ( Callithrix jacchus). We studied the robustness of distributed responses to natural and degraded forms of twitter calls, social contact vocalizations comprising several quasi-periodic phrases of frequency and AM. We recorded neuronal responses to a monkey's own twitter call (MOC), degraded forms of their twitter call, and sinusoidal amplitude modulated (SAM) tones with modulation rates similar to those of twitter calls. In spectral envelope degradation, calls with narrowband channels of varying bandwidths had the same temporal envelope as a natural call. However, the carrier phase was randomized within each narrowband channel. In temporal envelope degradation, the temporal envelope within narrowband channels was filtered while the carrier frequencies and phases remained unchanged. In a third form of degradation, noise was added to the natural calls. Spatiotemporal discharge patterns in AI both within and across frequency bands encoded spectrotemporal acoustic features in the call although the encoded response is an abstract version of the call. The average temporal response pattern in AI, however, was significantly correlated with the average temporal envelope for each phrase of a call. Response entrainment to MOC was significantly correlated with entrainment to SAM stimuli at comparable modulation frequencies. Sensitivity of the response patterns to MOC was substantially greater for temporal envelope than for spectral envelope degradations. The distributed responses in AI were robust to additive continuous noise at signal-to-noise ratios ≥10 dB. Neurophysiological data reflecting response sensitivity in AI to these forms of degradation closely parallel human psychophysical results on the intelligibility of degraded speech in quiet and noisy conditions.

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