scholarly journals Distinct Spiking Patterns of Excitatory and Inhibitory Neurons and LFP Oscillations in Prefrontal Cortex During Sensory Discrimination

2021 ◽  
Vol 12 ◽  
Author(s):  
Hua-an Tseng ◽  
Xue Han
Keyword(s):  
Prefrontal Cortex ◽  
Discrimination Task ◽  
Field Potential ◽  
Inhibitory Neurons ◽  
Sensory Stimuli ◽  
Sensory Discrimination ◽  
Related Information ◽  
Entire Duration ◽  
Excitatory Neurons ◽  
Spike Waveforms

Prefrontal cortex (PFC) are broadly linked to various aspects of behavior. During sensory discrimination, PFC neurons can encode a range of task related information, including the identity of sensory stimuli and related behavioral outcome. However, it remains largely unclear how different neuron subtypes and local field potential (LFP) oscillation features in the mouse PFC are modulated during sensory discrimination. To understand how excitatory and inhibitory PFC neurons are selectively engaged during sensory discrimination and how their activity relates to LFP oscillations, we used tetrode recordings to probe well-isolated individual neurons, and LFP oscillations, in mice performing a three-choice auditory discrimination task. We found that a majority of PFC neurons, 78% of the 711 recorded individual neurons, exhibited sensory discrimination related responses that are context and task dependent. Using spike waveforms, we classified these responsive neurons into putative excitatory neurons with broad waveforms or putative inhibitory neurons with narrow waveforms, and found that both neuron subtypes were transiently modulated, with individual neurons’ responses peaking throughout the entire duration of the trial. While the number of responsive excitatory neurons remain largely constant throughout the trial, an increasing fraction of inhibitory neurons were gradually recruited as the trial progressed. Further examination of the coherence between individual neurons and LFPs revealed that inhibitory neurons exhibit higher spike-field coherence with LFP oscillations than excitatory neurons during all aspects of the trial and across multiple frequency bands. Together, our results demonstrate that PFC excitatory neurons are continuously engaged during sensory discrimination, whereas PFC inhibitory neurons are increasingly recruited as the trial progresses and preferentially coordinated with LFP oscillations. These results demonstrate increasing involvement of inhibitory neurons in shaping the overall PFC dynamics toward the completion of the sensory discrimination task.

scholarly journals Distinct Spiking Patterns of Excitatory and Inhibitory Neurons and LFP Oscillations in Prefrontal Cortex during Sensory Discrimination

2019 ◽  
Author(s):  
Hua-an Tseng ◽  
Xue Han
Keyword(s):  
Prefrontal Cortex ◽  
Field Potential ◽  
Inhibitory Neurons ◽  
Task Completion ◽  
Sensory Stimuli ◽  
Sensory Discrimination ◽  
Excitatory Neurons ◽  
Gamma Frequencies ◽  
Oscillation Dynamics ◽  
Sensory Evoked

AbstractPrefrontal cortex (PFC) spike activity and local field potential (LFP) oscillation dynamics are broadly linked to various aspects of behavior. PFC neurons can encode the identity of sensory stimuli and related behavioral outcome in a range of sensory discrimination tasks. However, it remains largely unclear how different neuron subtypes and related LFP oscillation features are modulated in mice during sensory discrimination. To understand how excitatory and inhibitory neurons in PFC are selectively engaged during sensory discrimination and how they relate to LFPs oscillations, we used tetrode devices to probe well isolated individual PFC neurons, and LFP oscillations, in mice performing a three-choice auditory discrimination task. We found that a majority of the PFC neurons, 78% of a total of 711 individual neurons, exhibited sensory evoked responses that are context and task-progression dependent. Using spike waveforms, we classified these responsive neurons into excitatory and inhibitory neurons, and found that both neuron subtypes were transiently modulated, with individual neurons’ responses peaking throughout the entire task duration. While the number of responsive excitatory neurons remain largely constant throughout the task, an increasing fraction of inhibitory neurons were gradually recruited as trial progressed. Further examination of the coherences between individual neurons and LFPs revealed that inhibitory neurons in general exhibit higher spike-field coherence with LFP oscillations than excitatory neurons, first at higher gamma frequencies at the beginning of the task, and then at theta frequencies during the task, and finally across theta, beta and gamma frequencies at task completion. Together, our results demonstrate that while PFC excitatory neurons are continuously engaged during sensory discrimination, PFC inhibitory neurons are preferentially engaged as task progresses and selectively coordinated with distinct LFP oscillations. These results demonstrate increasing involvement of inhibitory neurons in shaping the overall PFC network dynamics as sensory discrimination progressed towards completion.

scholarly journals Functional selectivity and specific connectivity of inhibitory neurons in primary visual cortex

2018 ◽  
Author(s):  
Petr Znamenskiy ◽  
Mean-Hwan Kim ◽  
Dylan R. Muir ◽  
Maria Florencia Iacaruso ◽  
Sonja B. Hofer ◽  
...  
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Pyramidal Cells ◽  
Fine Tuning ◽  
Inhibitory Neurons ◽  
Local Network ◽  
Cortical Circuits ◽  
Sensory Stimuli ◽  
Excitatory Neurons ◽  
Strong Excitation

In the cerebral cortex, the interaction of excitatory and inhibitory synaptic inputs shapes the responses of neurons to sensory stimuli, stabilizes network dynamics1 and improves the efficiency and robustness of the neural code2–4. Excitatory neurons receive inhibitory inputs that track excitation5–8. However, how this co-tuning of excitation and inhibition is achieved by cortical circuits is unclear, since inhibitory interneurons are thought to pool the inputs of nearby excitatory cells and provide them with non-specific inhibition proportional to the activity of the local network9–13. Here we show that although parvalbumin-expressing (PV) inhibitory cells in mouse primary visual cortex make connections with the majority of nearby pyramidal cells, the strength of their synaptic connections is structured according to the similarity of the cells’ responses. Individual PV cells strongly inhibit those pyramidal cells that provide them with strong excitation and share their visual selectivity. This fine-tuning of synaptic weights supports co-tuning of inhibitory and excitatory inputs onto individual pyramidal cells despite dense connectivity between inhibitory and excitatory neurons. Our results indicate that individual PV cells are preferentially integrated into subnetworks of inter-connected, co-tuned pyramidal cells, stabilising their recurrent dynamics. Conversely, weak but dense inhibitory connectivity between subnetworks is sufficient to support competition between them, de-correlating their output. We suggest that the history and structure of correlated firing adjusts the weights of both inhibitory and excitatory connections, supporting stable amplification and selective recruitment of cortical subnetworks.

scholarly journals A Disinhibitory Circuit for Contextual Modulation in Primary Visual Cortex

2020 ◽  
Author(s):  
Andreas J. Keller ◽  
Mario Dipoppa ◽  
Morgane M. Roth ◽  
Matthew S. Caudill ◽  
Alessandro Ingrosso ◽  
...  
Keyword(s):  
Visual Cortex ◽  
Vasoactive Intestinal Peptide ◽  
Primary Visual Cortex ◽  
Computational Modelling ◽  
Visual Scene ◽  
Inhibitory Neurons ◽  
Contextual Modulation ◽  
Sensory Stimuli ◽  
Excitatory Neurons ◽  
Mouse Visual Cortex

Context guides perception by influencing the saliency of sensory stimuli. Accordingly, in visual cortex, responses to a stimulus are modulated by context, the visual scene surrounding the stimulus. Responses are suppressed when stimulus and surround are similar but not when they differ. The mechanisms that remove suppression when stimulus and surround differ remain unclear. Here we use optical recordings, manipulations, and computational modelling to show that a disinhibitory circuit consisting of vasoactive-intestinal-peptide-expressing (VIP) and somatostatin-expressing (SOM) inhibitory neurons modulates responses in mouse visual cortex depending on the similarity between stimulus and surround. When the stimulus and the surround are similar, VIP neurons are inactive and SOM neurons suppress excitatory neurons. However, when the stimulus and the surround differ, VIP neurons are active, thereby inhibiting SOM neurons and relieving excitatory neurons from suppression. We have identified a canonical cortical disinhibitory circuit which contributes to contextual modulation and may regulate perceptual saliency.

scholarly journals Analysing neuronal correlates of the comparison of two sequentially presented sensory stimuli

2002 ◽  
Vol 357 (1428) ◽  
pp. 1843-1850 ◽  
Author(s):  
Carlos D. Brody ◽  
Adrián Hernández ◽  
Antonio Zainos ◽  
Luis Lemus ◽  
Ranulfo Romo
Keyword(s):  
Macaca Mulatta ◽  
Cortical Area ◽  
Discrimination Task ◽  
Memory Trace ◽  
Sensory Stimulus ◽  
Neuronal Responses ◽  
Sensory Stimuli ◽  
Sensory Discrimination ◽  
Cortical Areas ◽  
Highly Correlated

In a typical sequential sensory discrimination task, subjects are required to make a decision based on comparing a sensory stimulus against the memory trace left by a previous stimulus. What is the neuronal substrate for such comparisons and the resulting decisions? This question was studied by recording neuronal responses in a variety of cortical areas of awake monkeys ( Macaca mulatta ), trained to carry out a vibrotactile sequential discrimination task. We describe methods to analyse responses obtained during the comparison and decision phases of the task, and describe the resulting findings from recordings in secondary somatosensory cortical area (S2). A subset of neurons in S2 become highly correlated with the monkey's decision in the task.

scholarly journals Cell type specific information transfer for sparse coding

2020 ◽  
Author(s):  
Fleur Zeldenrust ◽  
Niccolò Calcini ◽  
Xuan Yan ◽  
Ate Bijlsma ◽  
Tansu Celikel
Keyword(s):  
Sparse Coding ◽  
Information Transfer ◽  
Spike Trains ◽  
Inhibitory Neurons ◽  
Specific Information ◽  
Cell Type ◽  
Sensory Stimuli ◽  
Firing Rates ◽  
Excitatory Neurons ◽  
Cell Type Specific

AbstractSensory neurons reconstruct the world from action potentials (spikes) impinging on them. Recent work argues that the formation of sensory representations are cell-type specific, as excitatory and inhibitory neurons use complementary information available in spike trains to represent sensory stimuli. Here, by measuring the mutual information between synaptic input and spike trains, we show that inhibitory and excitatory neurons in the barrel cortex transfer information differently: excitatory neurons show strong threshold adaptation and a reduction of intracellular information transfer with increasing firing rates. Inhibitory neurons, on the other hand, show threshold behaviour that facilitates broadband information transfer. We propose that cell-type specific intracellular information transfer is the rate-limiting step for neuronal communication across synaptically coupled networks. Ultimately, at high firing rates, the reduction of information transfer by excitatory neurons and its facilitation by inhibitory neurons together provides a mechanism for sparse coding and information compression in cortical networks.

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 Distributed representations of temporal stimulus associations across regular-firing and fast-spiking neurons in rat medial prefrontal cortex

2020 ◽  
Vol 123 (1) ◽  
pp. 439-450
Author(s):  
Bohan Xing ◽  
Mark D. Morrissey ◽  
Kaori Takehara-Nishiuchi
Keyword(s):  
Prefrontal Cortex ◽  
Medial Prefrontal Cortex ◽  
Functional Organization ◽  
Spiking Neurons ◽  
Burst Firing ◽  
Inhibitory Neurons ◽  
Firing Patterns ◽  
Excitatory Neurons ◽  
Fast Spiking ◽  
The Difference

The prefrontal cortex has been implicated in various cognitive processes, including working memory, executive control, decision making, and relational learning. One core computational requirement underlying all these processes is the integration of information across time. When rodents and rabbits associate two temporally discontiguous stimuli, some neurons in the medial prefrontal cortex (mPFC) change firing rates in response to the preceding stimulus and sustain the firing rate during the subsequent temporal interval. These firing patterns are thought to serve as a mechanism to buffer the previously presented stimuli and signal the upcoming stimuli; however, how these critical properties are distributed across different neuron types remains unknown. We investigated the firing selectivity of regular-firing, burst-firing, and fast-spiking neurons in the prelimbic region of the mPFC while rats associated two neutral conditioned stimuli (CS) with one aversive stimulus (US). Analyses of firing patterns of individual neurons and neuron ensembles revealed that regular-firing neurons maintained rich information about CS identity and CS-US contingency during intervals separating the CS and US. Moreover, they further strengthened the latter selectivity with repeated conditioning sessions over a month. The selectivity of burst-firing neurons for both stimulus features was weaker than that of regular-firing neurons, indicating the difference in task engagement between two subpopulations of putative excitatory neurons. In contrast, putative inhibitory, fast-spiking neurons showed a stronger selectivity for CS identity than for CS-US contingency, suggesting their potential role in sensory discrimination. These results reveal a fine-scaled functional organization in the prefrontal network supporting the formation of temporal stimulus associations. NEW & NOTEWORTHY To associate stimuli that occurred separately in time, the brain needs to bridge the temporal gap by maintaining what was presented and predicting what would follow. We show that in rat medial prefrontal cortex, the former function is associated with a subpopulation of putative inhibitory neurons, whereas the latter is supported by a subpopulation of putative excitatory neurons. Our results reveal a distinct contribution of these microcircuit components to neural representations of temporal stimulus associations.

scholarly journals Neuron-specific spinal cord translatomes reveal a neuropeptide code for mouse dorsal horn excitatory neurons

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Rebecca Rani Das Gupta ◽  
Louis Scheurer ◽  
Pawel Pelczar ◽  
Hendrik Wildner ◽  
Hanns Ulrich Zeilhofer
Keyword(s):  
Spinal Cord ◽  
Dorsal Horn ◽  
Functional Organization ◽  
Affinity Purification ◽  
Expression Patterns ◽  
Inhibitory Neurons ◽  
Dorsal Horn Neurons ◽  
Expression Of Genes ◽  
Excitatory Neurons ◽  
Genes Encoding

AbstractThe spinal dorsal horn harbors a sophisticated and heterogeneous network of excitatory and inhibitory neurons that process peripheral signals encoding different sensory modalities. Although it has long been recognized that this network is crucial both for the separation and the integration of sensory signals of different modalities, a systematic unbiased approach to the use of specific neuromodulatory systems is still missing. Here, we have used the translating ribosome affinity purification (TRAP) technique to map the translatomes of excitatory glutamatergic (vGluT2+) and inhibitory GABA and/or glycinergic (vGAT+ or Gad67+) neurons of the mouse spinal cord. Our analyses demonstrate that inhibitory and excitatory neurons are not only set apart, as expected, by the expression of genes related to the production, release or re-uptake of their principal neurotransmitters and by genes encoding for transcription factors, but also by a differential engagement of neuromodulator, especially neuropeptide, signaling pathways. Subsequent multiplex in situ hybridization revealed eleven neuropeptide genes that are strongly enriched in excitatory dorsal horn neurons and display largely non-overlapping expression patterns closely adhering to the laminar and presumably also functional organization of the spinal cord grey matter.

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