scholarly journals Distinct roles of parvalbumin and somatostatin interneurons in the synchronization of spike-times in the neocortex

2019 ◽  
Author(s):  
Hyun Jae Jang ◽  
Hyowon Chung ◽  
James M. Rowland ◽  
Blake A. Richards ◽  
Michael M. Kohl ◽  
...  
Keyword(s):  
Barrel Cortex ◽  
Feedback Inhibition ◽  
Spike Timing ◽  
Timing Synchronization ◽  
Inhibitory Interneurons ◽  
Sensory Stimuli ◽  
Firing Rates ◽  
Single Unit Recordings ◽  
Spatio Temporal

AbstractSynchronization of precise spike-times across multiple neurons carries information about sensory stimuli. Inhibitory interneurons are suggested to promote this synchronization, but it is unclear whether distinct interneuron subtypes provide different contributions. To test this, we examined single-unit recordings from barrel cortex in vivo and used optogenetics to determine the contribution of two classes of inhibitory interneurons: parvalbumin (PV)- and somatostatin (SST)-positive interneurons to spike-timing synchronization across cortical layers. We found that PV interneurons preferentially promote the synchronization of spike-times when instantaneous firing-rates are low (<12 Hz), whereas SST interneurons preferentially promote the synchronization of spike-times when instantaneous firing-rates are high (>12 Hz). Furthermore, using a computational model, we demonstrate that these effects can be explained by PV and SST interneurons having preferential contribution to feedforward and feedback inhibition, respectively. Our findings demonstrate that distinct subtypes of inhibitory interneurons have frequency-selective roles in spatio-temporal synchronization of precise spike-times.

scholarly journals Distinct roles of parvalbumin and somatostatin interneurons in gating the synchronization of spike times in the neocortex

2020 ◽  
Vol 6 (17) ◽  
pp. eaay5333 ◽  
Author(s):  
Hyun Jae Jang ◽  
Hyowon Chung ◽  
James M. Rowland ◽  
Blake A. Richards ◽  
Michael M. Kohl ◽  
...  
Keyword(s):  
Computational Model ◽  
Single Unit ◽  
Barrel Cortex ◽  
Feedback Inhibition ◽  
Inhibitory Interneurons ◽  
Cortical Layers ◽  
Sensory Stimuli ◽  
Firing Rates ◽  
Single Unit Recordings

Synchronization of precise spike times across multiple neurons carries information about sensory stimuli. Inhibitory interneurons are suggested to promote this synchronization, but it is unclear whether distinct interneuron subtypes provide different contributions. To test this, we examined single-unit recordings from barrel cortex in vivo and used optogenetics to determine the contribution of parvalbumin (PV)– and somatostatin (SST)–positive interneurons to the synchronization of spike times across cortical layers. We found that PV interneurons preferentially promote the synchronization of spike times when instantaneous firing rates are low (<12 Hz), whereas SST interneurons preferentially promote the synchronization of spike times when instantaneous firing rates are high (>12 Hz). Furthermore, using a computational model, we demonstrate that these effects can be explained by PV and SST interneurons having preferential contributions to feedforward and feedback inhibition, respectively. Our findings demonstrate that distinct subtypes of inhibitory interneurons have frequency-selective roles in the spatiotemporal synchronization of precise spike times.

FosGFP expression does not capture a sensory learning-related engram in superficial layers of mouse barrel cortex

2021 ◽  
Vol 118 (52) ◽  
pp. e2112212118
Author(s):  
Jiseok Lee ◽  
Joanna Urban-Ciecko ◽  
Eunsol Park ◽  
Mo Zhu ◽  
Stephanie E. Myal ◽  
...  
Keyword(s):  
Pyramidal Neurons ◽  
Barrel Cortex ◽  
Sensory Information ◽  
Learning Task ◽  
Early Gene ◽  
Sensory Stimuli ◽  
Association Learning ◽  
Neural Ensembles ◽  
Dependent Learning

Immediate-early gene (IEG) expression has been used to identify small neural ensembles linked to a particular experience, based on the principle that a selective subset of activated neurons will encode specific memories or behavioral responses. The majority of these studies have focused on “engrams” in higher-order brain areas where more abstract or convergent sensory information is represented, such as the hippocampus, prefrontal cortex, or amygdala. In primary sensory cortex, IEG expression can label neurons that are responsive to specific sensory stimuli, but experience-dependent shaping of neural ensembles marked by IEG expression has not been demonstrated. Here, we use a fosGFP transgenic mouse to longitudinally monitor in vivo expression of the activity-dependent gene c-fos in superficial layers (L2/3) of primary somatosensory cortex (S1) during a whisker-dependent learning task. We find that sensory association training does not detectably alter fosGFP expression in L2/3 neurons. Although training broadly enhances thalamocortical synaptic strength in pyramidal neurons, we find that synapses onto fosGFP+ neurons are not selectively increased by training; rather, synaptic strengthening is concentrated in fosGFP− neurons. Taken together, these data indicate that expression of the IEG reporter fosGFP does not facilitate identification of a learning-specific engram in L2/3 in barrel cortex during whisker-dependent sensory association learning.

scholarly journals Reconciling the STDP and BCM Models of Synaptic Plasticity in a Spiking Recurrent Neural Network

2010 ◽  
Vol 22 (8) ◽  
pp. 2059-2085 ◽  
Author(s):  
Daniel Bush ◽  
Andrew Philippides ◽  
Phil Husbands ◽  
Michael O'Shea
Keyword(s):  
Neural Network ◽  
Synaptic Plasticity ◽  
Recurrent Neural Network ◽  
Hebbian Learning ◽  
Spike Timing ◽  
Synaptic Competition ◽  
Firing Rates ◽  
Plasticity Rule ◽  
Asymmetric Learning

Rate-coded Hebbian learning, as characterized by the BCM formulation, is an established computational model of synaptic plasticity. Recently it has been demonstrated that changes in the strength of synapses in vivo can also depend explicitly on the relative timing of pre- and postsynaptic firing. Computational modeling of this spike-timing-dependent plasticity (STDP) has demonstrated that it can provide inherent stability or competition based on local synaptic variables. However, it has also been demonstrated that these properties rely on synaptic weights being either depressed or unchanged by an increase in mean stochastic firing rates, which directly contradicts empirical data. Several analytical studies have addressed this apparent dichotomy and identified conditions under which distinct and disparate STDP rules can be reconciled with rate-coded Hebbian learning. The aim of this research is to verify, unify, and expand on these previous findings by manipulating each element of a standard computational STDP model in turn. This allows us to identify the conditions under which this plasticity rule can replicate experimental data obtained using both rate and temporal stimulation protocols in a spiking recurrent neural network. Our results describe how the relative scale of mean synaptic weights and their dependence on stochastic pre- or postsynaptic firing rates can be manipulated by adjusting the exact profile of the asymmetric learning window and temporal restrictions on spike pair interactions respectively. These findings imply that previously disparate models of rate-coded autoassociative learning and temporally coded heteroassociative learning, mediated by symmetric and asymmetric connections respectively, can be implemented in a single network using a single plasticity rule. However, we also demonstrate that forms of STDP that can be reconciled with rate-coded Hebbian learning do not generate inherent synaptic competition, and thus some additional mechanism is required to guarantee long-term input-output selectivity.

scholarly journals Texture coarseness responsive neurons and their mapping in layer 2–3 of the rat barrel cortex in vivo

eLife ◽  
2014 ◽  
Vol 3 ◽  
Author(s):  
Liora Garion ◽  
Uri Dubin ◽  
Yoav Rubin ◽  
Mohamed Khateb ◽  
Yitzhak Schiller ◽  
...  
Keyword(s):  
Calcium Imaging ◽  
Barrel Cortex ◽  
Fundamental Function ◽  
Tactile Information ◽  
Hierarchical Processing ◽  
Two Photon ◽  
Columnar Organization ◽  
Layer 2 ◽  
Single Unit Recordings

Texture discrimination is a fundamental function of somatosensory systems, yet the manner by which texture is coded and spatially represented in the barrel cortex are largely unknown. Using in vivo two-photon calcium imaging in the rat barrel cortex during artificial whisking against different surface coarseness or controlled passive whisker vibrations simulating different coarseness, we show that layer 2–3 neurons within barrel boundaries differentially respond to specific texture coarsenesses, while only a minority of neurons responded monotonically with increased or decreased surface coarseness. Neurons with similar preferred texture coarseness were spatially clustered. Multi-contact single unit recordings showed a vertical columnar organization of texture coarseness preference in layer 2–3. These findings indicate that layer 2–3 neurons perform high hierarchical processing of tactile information, with surface coarseness embodied by distinct neuronal subpopulations that are spatially mapped onto the barrel cortex.

scholarly journals Identification of a developmental switch in information transfer between whisker S1 and S2 cortex in mice

2021 ◽  
Author(s):  
Theofanis Karayannis ◽  
Linbi Cai ◽  
Jenq-Wei Yang ◽  
Shen-Ju Chou ◽  
Chia-Fang Wang ◽  
...  
Keyword(s):  
Information Transfer ◽  
Barrel Cortex ◽  
Wide Field ◽  
Sensory Stimuli ◽  
Knock Out ◽  
Electrophysiological Recordings ◽  
Primary Sensory Cortex ◽  
Animal Navigation ◽  
Knock Out Mice

The whiskers of rodents are a key sensory organ that provides critical tactile information for animal navigation and object exploration throughout life. Previous work has explored the developmental sensory-driven activation of the primary sensory cortex processing whisker information (wS1), also called barrel cortex. This body of work has shown that the barrel cortex is already activated by sensory stimuli during the first post-natal week. However, it is currently unknown when over the course of development these stimuli begin being processed by higher order cortical areas, such as secondary whisker somatosensory area (wS2). Here we investigate for the first time the developmental engagement of wS2 by sensory stimuli and the emergence of cortico-cortical communication from wS1 to wS2. Using in vivo wide-field imaging and electrophysiological recordings in control and conditional knock-out mice we find that wS1 and wS2 are able to process bottom-up information coming from the thalamus already right after birth. We identify that it is only at the end of the first post-natal week that wS1 begins to provide excitation into wS2, a connection which begins to acquire feed-forward inhibition characteristics after the second post-natal week. Therefore, we have uncovered a developmental window during which excitatory versus inhibitory functional connectivity between wS1 and wS2 takes place.

Phasic Stimuli Evoke Precisely Timed Spikes in Intermittently Discharging Mitral Cells

2004 ◽  
Vol 92 (2) ◽  
pp. 743-753 ◽  
Author(s):  
Ramani Balu ◽  
Phillip Larimer ◽  
Ben W. Strowbridge
Keyword(s):  
Olfactory Bulb ◽  
Action Potentials ◽  
Sensory Stimulation ◽  
Spike Timing ◽  
Mitral Cells ◽  
Potential Oscillations ◽  
Sensory Stimuli ◽  
Subthreshold Oscillations ◽  
Simple Step

Mitral cells, the principal cells of the olfactory bulb, respond to sensory stimulation with precisely timed patterns of action potentials. By contrast, the same neurons generate intermittent spike clusters with variable timing in response to simple step depolarizations. We made whole cell recordings from mitral cells in rat olfactory bulb slices to examine the mechanisms by which normal sensory stimuli could generate precisely timed spike clusters. We found that individual mitral cells fired clusters of action potentials at 20-40 Hz, interspersed with periods of subthreshold membrane potential oscillations in response to depolarizing current steps. TTX (1 μM) blocked a sustained depolarizing current and fast subthreshold oscillations in mitral cells. Phasic stimuli that mimic trains of slow excitatory postsynaptic potentials (EPSPs) that occur during sniffing evoked precisely timed spike clusters in repeated trials. The amplitude of the first simulated EPSP in a train gated the generation of spikes on subsequent EPSPs. 4-aminopyridine (4-AP)–sensitive K+ channels are critical to the generation of spike clusters and reproducible spike timing in response to phasic stimuli. Based on these results, we propose that spike clustering is a process that depends on the interaction between a 4-AP–sensitive K+ current and a subthreshold TTX-sensitive Na+ current; interactions between these currents may allow mitral cells to respond selectively to stimuli in the theta frequency range. These intrinsic properties of mitral cells may be important for precisely timing spikes evoked by phasic stimuli that occur in response to odor presentation in vivo.

scholarly journals NMDA receptor–BK channel coupling regulates synaptic plasticity in the barrel cortex

2021 ◽  
Vol 118 (35) ◽  
pp. e2107026118 ◽  
Author(s):  
Ricardo Gómez ◽  
Laura E. Maglio ◽  
Alberto J. Gonzalez-Hernandez ◽  
Belinda Rivero-Pérez ◽  
David Bartolomé-Martín ◽  
...  
Keyword(s):  
Synaptic Plasticity ◽  
Pyramidal Neurons ◽  
Barrel Cortex ◽  
Feedback Inhibition ◽  
Bk Channels ◽  
Bk Channel ◽  
Spike Timing ◽  
Ability To Act ◽  
Nmdar Activation ◽  
Molecular Context

Postsynaptic N-methyl-D-aspartate receptors (NMDARs) are crucial mediators of synaptic plasticity due to their ability to act as coincidence detectors of presynaptic and postsynaptic neuronal activity. However, NMDARs exist within the molecular context of a variety of postsynaptic signaling proteins, which can fine-tune their function. Here, we describe a form of NMDAR suppression by large-conductance Ca2+- and voltage-gated K+ (BK) channels in the basal dendrites of a subset of barrel cortex layer 5 pyramidal neurons. We show that NMDAR activation increases intracellular Ca2+ in the vicinity of BK channels, thus activating K+ efflux and strong negative feedback inhibition. We further show that neurons exhibiting such NMDAR–BK coupling serve as high-pass filters for incoming synaptic inputs, precluding the induction of spike timing–dependent plasticity. Together, these data suggest that NMDAR-localized BK channels regulate synaptic integration and provide input-specific synaptic diversity to a thalamocortical circuit.

scholarly journals Corticothalamic gating of population auditory thalamocortical transmission in mouse

2019 ◽  
Author(s):  
Baher A. Ibrahim ◽  
Caitlin Murphy ◽  
Guido Muscioni ◽  
Aynaz Taheri ◽  
Georgiy Yudintsev ◽  
...  
Keyword(s):  
Receptive Field ◽  
Auditory Cortex ◽  
Cortical Neurons ◽  
Feedback Inhibition ◽  
Thalamic Reticular Nucleus ◽  
Reticular Nucleus ◽  
Linear Filter ◽  
Sensory Stimuli

AbstractSince the discovery of the receptive field, scientists have tracked receptive field structure to gain insights about mechanisms of sensory processing. At the level of the thalamus and cortex, this linear filter approach has been challenged by findings that populations of cortical neurons respond in a stereotyped fashion to sensory stimuli. Here, we elucidate a possible mechanism by which gating of cortical representations occurs. All-or-none population responses (here called “ON” and “OFF” responses) were observed in vivo and in vitro in the mouse auditory cortex at near-threshold acoustic or electrical stimulation. ON-responses were associated with previously-described UP states in the auditory cortex. OFF-responses in the cortex were only eliminated by blocking GABAergic inhibition in the thalamus. Opto- and chemogenetic silencing of NTSR-positive corticothalamic layer 6 (CTL6) neurons as well as the pharmacological blocking of the thalamic reticular nucleus (TRN) retrieved the missing cortical responses, suggesting that the corticothalamic feedback inhibition via TRN controls the gating of thalamocortical activity. Moreover, the oscillation of the pre-stimulus activity of corticothalamic cells predicted the cortical ON vs. OFF responses, suggesting that underlying cortical oscillation controls thalamocortical gating. These data suggest that the thalamus may recruit cortical ensembles rather than linearly encoding ascending stimuli and that corticothalamic projections play a key role in selecting cortical ensembles for activation.

scholarly journals Prediction-error neurons in circuits with multiple neuron types: Formation, refinement and functional implications

2021 ◽  
Author(s):  
Loreen Hertäg ◽  
Claudia Clopath
Keyword(s):  
Network Model ◽  
Prediction Error ◽  
Recurrent Network ◽  
Inhibitory Interneurons ◽  
Sensory Stimuli ◽  
Firing Rates ◽  
Sensory Inputs ◽  
Functional Implications ◽  
Inhibitory Plasticity ◽  
Biased Perception

AbstractPredictable sensory stimuli do not evoke significant responses in a subset of cortical excitatory neurons. Some of those neurons, however, change their activity upon mismatches between actual and predicted stimuli. Different variants of these prediction-error neurons exist and they differ in their responses to unexpected sensory stimuli. However, it is unclear how these variants can develop and co-exist in the same recurrent network, and how they are simultaneously shaped by the astonishing diversity of inhibitory interneurons. Here, we study these questions in a computational network model with three types of inhibitory interneurons. We find that balancing excitation and inhibition in multiple pathways gives rise to heterogeneous prediction-error circuits. Dependent on the network’s initial connectivity and distribution of actual and predicted sensory inputs, these circuits can form different variants of prediction-error neurons that are robust to network perturbations and generalize to stimuli not seen during learning. These variants can be learned simultaneously via homeostatic inhibitory plasticity with low baseline firing rates. Finally, we demonstrate that prediction-error neurons can support biased perception, we illustrate a number of functional implications, and we discuss testable predictions.

scholarly journals Chemical synaptic transmission onto superficial stellate cells of the mouse dorsal cochlear nucleus

2014 ◽  
Vol 111 (9) ◽  
pp. 1812-1822 ◽  
Author(s):  
Pierre F. Apostolides ◽  
Laurence O. Trussell
Keyword(s):  
Cochlear Nucleus ◽  
Stellate Cell ◽  
Stellate Cells ◽  
Dorsal Cochlear Nucleus ◽  
Fine Tuning ◽  
In Vivo Studies ◽  
Inhibitory Synapses ◽  
Inhibitory Interneurons ◽  
Sensory Stimuli

The dorsal cochlear nucleus (DCN) is a cerebellum-like auditory brain stem region whose functions include sound localization and multisensory integration. Although previous in vivo studies have shown that glycinergic and GABAergic inhibition regulate the activity of several DCN cell types in response to sensory stimuli, data regarding the synaptic inputs onto DCN inhibitory interneurons remain limited. Using acute DCN slices from mice, we examined the properties of excitatory and inhibitory synapses onto the superficial stellate cell, a poorly understood cell type that provides inhibition to DCN output neurons (fusiform cells) as well as to local inhibitory interneurons (cartwheel cells). Excitatory synapses onto stellate cells activated both NMDA receptors and fast-gating, Ca2+-permeable AMPA receptors. Inhibition onto superficial stellate cells was mediated by glycine and GABAA receptors with different temporal kinetics. Paired recordings revealed that superficial stellate cells make reciprocal synapses and autapses, with a connection probability of ∼18–20%. Unexpectedly, superficial stellate cells co-released both glycine and GABA, suggesting that co-transmission may play a role in fine-tuning the duration of inhibitory transmission.

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