scholarly journals Network activity influences the subthreshold and spiking visual responses of pyramidal neurons in the three-layer turtle cortex

2017 ◽  
Vol 118 (4) ◽  
pp. 2142-2155 ◽  
Author(s):  
Nathaniel C. Wright ◽  
Ralf Wessel
Keyword(s):  
Membrane Potential ◽  
Cortical Neurons ◽  
Visual Stimulation ◽  
Cortical Activity ◽  
Network Activity ◽  
Visual Responses ◽  
Up States ◽  
Evoked Activity ◽  
Sensory Evoked

A primary goal of systems neuroscience is to understand cortical function, typically by studying spontaneous and stimulus-modulated cortical activity. Mounting evidence suggests a strong and complex relationship exists between the ongoing and stimulus-modulated cortical state. To date, most work in this area has been based on spiking in populations of neurons. While advantageous in many respects, this approach is limited in scope: it records the activity of a minority of neurons and gives no direct indication of the underlying subthreshold dynamics. Membrane potential recordings can fill these gaps in our understanding, but stable recordings are difficult to obtain in vivo. Here, we recorded subthreshold cortical visual responses in the ex vivo turtle eye-attached whole brain preparation, which is ideally suited for such a study. We found that, in the absence of visual stimulation, the network was “synchronous”; neurons displayed network-mediated transitions between hyperpolarized (Down) and depolarized (Up) membrane potential states. The prevalence of these slow-wave transitions varied across turtles and recording sessions. Visual stimulation evoked similar Up states, which were on average larger and less reliable when the ongoing state was more synchronous. Responses were muted when immediately preceded by large, spontaneous Up states. Evoked spiking was sparse, highly variable across trials, and mediated by concerted synaptic inputs that were, in general, only very weakly correlated with inputs to nearby neurons. Together, these results highlight the multiplexed influence of the cortical network on the spontaneous and sensory-evoked activity of individual cortical neurons. NEW & NOTEWORTHY Most studies of cortical activity focus on spikes. Subthreshold membrane potential recordings can provide complementary insight, but stable recordings are difficult to obtain in vivo. Here, we recorded the membrane potentials of cortical neurons during ongoing and visually evoked activity. We observed a strong relationship between network and single-neuron evoked activity spanning multiple temporal scales. The membrane potential perspective of cortical dynamics thus highlights the influence of intrinsic network properties on visual processing.

scholarly journals Network activity influences the subthreshold and spiking visual responses of pyramidal neurons in a three-layer cortex

2016 ◽  
Author(s):  
Nathaniel C. Wright ◽  
Ralf Wessel
Keyword(s):  
Membrane Potential ◽  
Cortical Neurons ◽  
Visual Stimulation ◽  
Ex Vivo ◽  
Network Activity ◽  
Visual Responses ◽  
Cortical Function ◽  
Sensory Evoked ◽  
High Conductance

A primary goal of systems neuroscience is to understand cortical function, which typically involves studying spontaneous and sensory-evoked cortical activity. Mounting evidence suggests a strong and complex relationship between the ongoing and evoked state. To date, most work in this area has been based on spiking in populations of neurons. While advantageous in many respects, this approach is limited in scope; it records the activities of a minority of neurons, and gives no direct indication of the underlying subthreshold dynamics. Membrane potential recordings can fill these gaps in our understanding, but are difficult to obtain in vivo. Here, we record subthreshold cortical visual responses in the ex vivo turtle eye-attached whole-brain preparation, which is ideally-suited to such a study. In the absence of visual stimulation, the network is “synchronous”; neurons display network-mediated transitions between low- and high-conductance membrane potential states. The prevalence of these slow-wave transitions varies across turtles and recording sessions. Visual stimulation evokes similar high-conductance states, which are on average larger and less reliable when the ongoing state is more synchronous. Responses are muted when immediately preceded by large, spontaneous high-conductance events. Evoked spiking is sparse, highly variable across trials, and mediated by concerted synaptic inputs that are in general only very weakly correlated with inputs to nearby neurons. Together, these results highlight the multiplexed influence of the cortical network on the spontaneous and sensory-evoked activity of individual cortical neurons.

Bulk Dye Loading for In Vivo Calcium Imaging of Visual Responses in Populations of Xenopus Tectal Neurons

2021 ◽  
Vol 2022 (1) ◽  
pp. pdb.prot106831
Author(s):  
Peter W. Hogg ◽  
Kurt Haas
Keyword(s):  
Optic Tectum ◽  
Image Plane ◽  
Time Lapse ◽  
Visual Responses ◽  
Easy Method ◽  
Tectal Neurons ◽  
Evoked Activity ◽  
Sensory Evoked ◽  
Time Lapse Imaging

Bulk loading of neurons with fluorescent calcium indicators in transparent albino Xenopus tadpoles offers a rapid and easy method for tracking sensory-evoked activity in large numbers of neurons within an awake developing brain circuit. In vivo two-photon time-lapse imaging of an image plane through the optic tectum allows defining receptive field properties from visual-evoked responses for studies of single-neuron and network-level encoding and plasticity. Here, we describe loading the Xenopus tadpole optic tectum with the membrane-permeable AM ester of Oregon Green 488 BAPTA-1 (OGB-1 AM) for in vivo imaging experiments.

scholarly journals Optogenetic Modulation of a Minor Fraction of Parvalbumin-Positive Interneurons Specifically Affects Spatiotemporal Dynamics of Spontaneous and Sensory-Evoked Activity in Mouse Somatosensory Cortex in Vivo

2017 ◽  
Vol 27 (12) ◽  
pp. 5784-5803 ◽  
Author(s):  
Jenq-Wei Yang ◽  
Pierre-Hugues Prouvot ◽  
Vicente Reyes-Puerta ◽  
Maik C Stüttgen ◽  
Albrecht Stroh ◽  
...  
Keyword(s):  
Somatosensory Cortex ◽  
Spatiotemporal Dynamics ◽  
Minor Fraction ◽  
Evoked Activity ◽  
Sensory Evoked ◽  
A Minor

scholarly journals A Method to Estimate Synaptic Conductances From Membrane Potential Fluctuations

2004 ◽  
Vol 91 (6) ◽  
pp. 2884-2896 ◽  
Author(s):  
Michael Rudolph ◽  
Zuzanna Piwkowska ◽  
Mathilde Badoual ◽  
Thierry Bal ◽  
Alain Destexhe
Keyword(s):  
Membrane Potential ◽  
Computational Models ◽  
Network Activity ◽  
Intracellular Recordings ◽  
Neocortical Neurons ◽  
Underlying Network ◽  
Analytic Expression ◽  
Synaptic Conductances

In neocortical neurons, network activity can activate a large number of synaptic inputs, resulting in highly irregular subthreshold membrane potential ( Vm) fluctuations, commonly called “synaptic noise.” This activity contains information about the underlying network dynamics, but it is not easy to extract network properties from such complex and irregular activity. Here, we propose a method to estimate properties of network activity from intracellular recordings and test this method using theoretical and experimental approaches. The method is based on the analytic expression of the subthreshold Vm distribution at steady state in conductance-based models. Fitting this analytic expression to Vm distributions obtained from intracellular recordings provides estimates of the mean and variance of excitatory and inhibitory conductances. We test the accuracy of these estimates against computational models of increasing complexity. We also test the method using dynamic-clamp recordings of neocortical neurons in vitro. By using an on-line analysis procedure, we show that the measured conductances from spontaneous network activity can be used to re-create artificial states equivalent to real network activity. This approach should be applicable to intracellular recordings during different network states in vivo, providing a characterization of the global properties of synaptic conductances and possible insight into the underlying network mechanisms.

Characterization of Synaptic Conductances and Integrative Properties During Electrically Induced EEG-Activated States in Neocortical Neurons In Vivo

2005 ◽  
Vol 94 (4) ◽  
pp. 2805-2821 ◽  
Author(s):  
Michael Rudolph ◽  
Joe Guillaume Pelletier ◽  
Denis Paré ◽  
Alain Destexhe
Keyword(s):  
Cortical Neurons ◽  
Computational Models ◽  
Input Resistance ◽  
Synaptic Activity ◽  
Intracellular Recordings ◽  
Neocortical Neurons ◽  
Up States ◽  
Conductance State ◽  
Stimulation Of

The activation of the electroencephalogram (EEG) is paralleled with an increase in the firing rate of cortical neurons, but little is known concerning the conductance state of their membrane and its impact on their integrative properties. Here, we combined in vivo intracellular recordings with computational models to investigate EEG-activated states induced by stimulation of the brain stem ascending arousal system. Electrical stimulation of the pedonculopontine tegmental (PPT) nucleus produced long-lasting (≈20 s) periods of desynchronized EEG activity similar to the EEG of awake animals. Intracellularly, PPT stimulation locked the membrane into a depolarized state, similar to the up-states seen during deep anesthesia. During these EEG-activated states, however, the input resistance was higher than that during up-states. Conductance measurements were performed using different methods, which all indicate that EEG-activated states were associated with a synaptic activity dominated by inhibitory conductances. These results were confirmed by computational models of reconstructed pyramidal neurons constrained by the corresponding intracellular recordings. These models indicate that, during EEG-activated states, neocortical neurons are in a high-conductance state consistent with a stochastic integrative mode. The amplitude and timing of somatic excitatory postsynaptic potentials were nearly independent of the position of the synapses in dendrites, suggesting that EEG-activated states are compatible with coding paradigms involving the precise timing of synaptic events.

scholarly journals Behavioral-state modulation of inhibition is context-dependent and cell type specific in mouse visual cortex

eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Janelle MP Pakan ◽  
Scott C Lowe ◽  
Evelyn Dylda ◽  
Sander W Keemink ◽  
Stephen P Currie ◽  
...  
Keyword(s):  
Visual Cortex ◽  
Pyramidal Neurons ◽  
Visual Stimulation ◽  
Inhibitory Neurons ◽  
Behavioral State ◽  
Visual Responses ◽  
Cell Type ◽  
Sensory Stimuli ◽  
Context Dependent

Cortical responses to sensory stimuli are modulated by behavioral state. In the primary visual cortex (V1), visual responses of pyramidal neurons increase during locomotion. This response gain was suggested to be mediated through inhibitory neurons, resulting in the disinhibition of pyramidal neurons. Using in vivo two-photon calcium imaging in layers 2/3 and 4 in mouse V1, we reveal that locomotion increases the activity of vasoactive intestinal peptide (VIP), somatostatin (SST) and parvalbumin (PV)-positive interneurons during visual stimulation, challenging the disinhibition model. In darkness, while most VIP and PV neurons remained locomotion responsive, SST and excitatory neurons were largely non-responsive. Context-dependent locomotion responses were found in each cell type, with the highest proportion among SST neurons. These findings establish that modulation of neuronal activity by locomotion is context-dependent and contest the generality of a disinhibitory circuit for gain control of sensory responses by behavioral state.

scholarly journals Calculating Event-Triggered Average Synaptic Conductances From the Membrane Potential

2007 ◽  
Vol 97 (3) ◽  
pp. 2544-2552 ◽  
Author(s):  
Martin Pospischil ◽  
Zuzanna Piwkowska ◽  
Michelle Rudolph ◽  
Thierry Bal ◽  
Alain Destexhe
Keyword(s):  
Membrane Potential ◽  
Cortical Neurons ◽  
Time Course ◽  
Spike Generation ◽  
Nonlinear Contribution ◽  
Central Neurons ◽  
Time Courses ◽  
Model Subject ◽  
Synaptic Conductances

The optimal patterns of synaptic conductances for spike generation in central neurons is a subject of considerable interest. Ideally such conductance time courses should be extracted from membrane potential ( Vm) activity, but this is difficult because the nonlinear contribution of conductances to the Vm renders their estimation from the membrane equation extremely sensitive. We outline here a solution to this problem based on a discretization of the time axis. This procedure can extract the time course of excitatory and inhibitory conductances solely from the analysis of Vm activity. We test this method by calculating spike-triggered averages of synaptic conductances using numerical simulations of the integrate-and-fire model subject to colored conductance noise. The procedure was also tested successfully in biological cortical neurons using conductance noise injected with dynamic clamp. This method should allow the extraction of synaptic conductances from Vm recordings in vivo.

Characteristic Membrane Potential Trajectories in Primate Sensorimotor Cortex Neurons Recorded In Vivo

2005 ◽  
Vol 94 (4) ◽  
pp. 2713-2725 ◽  
Author(s):  
Daofen Chen ◽  
Eberhard E. Fetz
Keyword(s):  
Membrane Potential ◽  
Sensorimotor Cortex ◽  
High Frequency ◽  
Cortical Neurons ◽  
Type I ◽  
Type Ii ◽  
Interspike Intervals ◽  
Cortical Oscillations ◽  
Firing Properties

We examined the membrane potentials and firing properties of motor cortical neurons recorded intracellularly in awake, behaving primates. Three classes of neuron were distinguished by 1) the width of their spikes, 2) the shape of the afterhyperpolarization (AHP), and 3) the distribution of interspike intervals. Type I neurons had wide spikes, exhibited scoop-shaped AHPs, and fired irregularly. Type II neurons had narrower spikes, showed brief postspike afterdepolarizations before the AHP, and sometimes fired high-frequency doublets. Type III neurons had the narrowest spikes, showed a distinct post-AHP depolarization, or “rebound AHP” (rAHP), lasting nearly 30 ms, and tended to fire at 25–35 Hz. The evidence suggests that an intrinsic rAHP may confer on these neurons a tendency to fire at a preferred frequency governed by the duration of the rAHP and may contribute to a “pacemaking” role in generating cortical oscillations.

Two-State Membrane Potential Fluctuations Driven by Weak Pairwise Correlations

2004 ◽  
Vol 16 (11) ◽  
pp. 2351-2378 ◽  
Author(s):  
Andrea Benucci ◽  
Paul F.M.J. Verschure ◽  
Peter König
Keyword(s):  
Membrane Potential ◽  
Single Cell ◽  
Cortical Neurons ◽  
Bimodal Distribution ◽  
Quantitative Agreement ◽  
Neuronal Model ◽  
Dendritic Morphology ◽  
Cell Dynamics ◽  
Up States ◽  
Pairwise Correlations

Physiological experiments demonstrate the existence of weak pairwise correlations of neuronal activity in mammalian cortex (Singer, 1993). The functional implications of this correlated activity are hotly debated (Roskiesetal., 1999).Nevertheless, it is generally considered a wide spread feature of cortical dynamics. In recent years, another line of research has attracted great interest: the observation of a bimodal distribution of the membrane potential defining up states and down states at the single cell level (Wilson & Kawaguchi, 1996; Steriade, Contreras, & Amzica, 1994; Contreras & Steriade, 1995; Steriade, 2001). Here we use a theoretical approach to demonstrate that the latter phenomenon is a natural consequence of the former. In particular, we show that weak pairwise correlations of the inputs to a compartmental model of a layer V pyramidal cell can induce bimodality in its membrane potential. We show how this relationship can account for the observed increase of the power in the γ frequency band during up states, as well as the increase in the standard deviation and fraction of time spent in the depolarized state (Anderson, Lampl, Reichova, Carandini, & Ferster, 2000). In order to quantify the relationship between the correlation properties of a cortical network and the bistable dynamics of single neurons, we introduce a number of new indices. Subsequently, we demonstrate that a quantitative agreement with the experimental data can be achieved, introducing voltage-dependent mechanisms in our neuronal model such as Ca2+- and Ca2+-dependent K+ channels. In addition, we show that the up states and down states of the membrane potential are dependent on the dendritic morphology of cortical neurons. Furthermore, bringing together network and single cell dynamics under a unified view allows the direct transfer of results obtained in one context to the other and suggests a new experimental paradigm: the use of specific intracellular analysis as a powerful tool to reveal the properties of the correlation structure present in the network dynamics.

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