H-current modulation of cortical Up and Down states
Abstract: Understanding the link between cellular processes and brain function remains a key challenge in neuroscience. One crucial aspect is the interplay between specific ion channels and network dynamics. This work reveals a role for h-current, a hyperpolarization-activated cationic current, in shaping cortical slow oscillations. Cortical slow oscillations exhibit rhythmic periods of activity (Up states) alternating with silent periods (Down states). By progressively reducing h-current in both cortical slices and in … Show more
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Cited by 2 publications
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Interleaved single and bursting spiking resonance in neurons
Underin vivoconditions, CA1 pyramidal cells from the hippocampus display transitions from single spikes to bursts. It is believed that subthreshold hyperpolarization and depolarization, also known as down and up-states, play a pivotal role in these transitions. Nevertheless, a central impediment to correlating suprathreshold (spiking) and subthreshold activity has been the technical difficulties of this type of recordings, even with widely used calcium imaging or multielectrode recordings. Recent work using voltage imaging with genetically encoded voltage indicators has been able to correlate spiking patterns with subthreshold activity in a variety of CA1 neurons, and recent computational models have been able to capture these transitions. In this work, we used a computational model of a CA1 pyramidal cell to investigate the role of intrinsic conductances and oscillatory patterns in generating down and up-states and their modulation in the transition from single spiking to bursting. Specifically, the emergence of distinct spiking resonances between these two spiking modes that share the same voltage traces in the presence of theta or gamma oscillatory inputs, a phenomenon we call interleaved single and bursting spiking resonance. We noticed that these resonances do not necessarily overlap in frequency or amplitude, underscoring their relevance for providing flexibility to neural processing. We studied the conductance values of three current types that are thought to be critical for the bursting behavior: persistent sodium current (INaP) and its conductanceGNaP, delayed rectifier potassium (IKDR) and its conductanceGKDR, and hyperpolarization-activated current (Ih) and its conductanceGh. We conclude that the intricate interplay of ionic currents significantly influences the neuronal firing patterns, transitioning from single to burst firing during sustained depolarization. Specifically, the intermediate levels ofGNaPandGKDRfacilitate spiking resonance at gamma frequency inputs. The resonance characteristics vary between single and burst firing modes, each displaying distinct amplitudes and resonant frequencies. Furthermore, lowGNaPand highGKDRvalues lock bursting to theta frequencies, while highGNaPand lowGKDRvalues lock single spiking to gamma frequencies. Lastly, the duration of quiet intervals plays a crucial role in determining the likelihood of transitioning to either bursting or single spiking modes. We confirmed that the same features were present in previously recorded in vivo voltage-imaging data. Understanding these dynamics provides valuable insights into the fundamental mechanisms underlying neuronal excitability underin vivoconditions.Author summarySince discovering that neurons in the hippocampus can encode spatial position through phase precession, many experiments have explored how specific theta and gamma oscillations influence location specificity in the brain. However, the individual neuronal properties and dynamics behind these behaviors are still being uncovered. Previously, we found that stereotypical bursting and single-spike firing in pyramidal neurons are linked to these oscillations and further associated with an animal entering or leaving a place field. Advances in voltage-imaging techniques have enabled us to assess these properties more precisely. Our study shows that different frequencies can independently trigger these stereotypical spikes, demonstrating a complex pattern where the same cell can be double-coded: a phenomenon we called interleaved resonance. Additionally, we found that this coding can be modulated by persistent sodium and delayed-rectifier potassium currents. Moreover, these neurons are more likely to burst following long periods of silence. These findings provide new insights into the mechanisms underlying neural coding in the hippocampus and how it relates to behavior.
Interleaved single and bursting spiking resonance in neurons
Underin vivoconditions, CA1 pyramidal cells from the hippocampus display transitions from single spikes to bursts. It is believed that subthreshold hyperpolarization and depolarization, also known as down and up-states, play a pivotal role in these transitions. Nevertheless, a central impediment to correlating suprathreshold (spiking) and subthreshold activity has been the technical difficulties of this type of recordings, even with widely used calcium imaging or multielectrode recordings. Recent work using voltage imaging with genetically encoded voltage indicators has been able to correlate spiking patterns with subthreshold activity in a variety of CA1 neurons, and recent computational models have been able to capture these transitions. In this work, we used a computational model of a CA1 pyramidal cell to investigate the role of intrinsic conductances and oscillatory patterns in generating down and up-states and their modulation in the transition from single spiking to bursting. Specifically, the emergence of distinct spiking resonances between these two spiking modes that share the same voltage traces in the presence of theta or gamma oscillatory inputs, a phenomenon we call interleaved single and bursting spiking resonance. We noticed that these resonances do not necessarily overlap in frequency or amplitude, underscoring their relevance for providing flexibility to neural processing. We studied the conductance values of three current types that are thought to be critical for the bursting behavior: persistent sodium current (INaP) and its conductanceGNaP, delayed rectifier potassium (IKDR) and its conductanceGKDR, and hyperpolarization-activated current (Ih) and its conductanceGh. We conclude that the intricate interplay of ionic currents significantly influences the neuronal firing patterns, transitioning from single to burst firing during sustained depolarization. Specifically, the intermediate levels ofGNaPandGKDRfacilitate spiking resonance at gamma frequency inputs. The resonance characteristics vary between single and burst firing modes, each displaying distinct amplitudes and resonant frequencies. Furthermore, lowGNaPand highGKDRvalues lock bursting to theta frequencies, while highGNaPand lowGKDRvalues lock single spiking to gamma frequencies. Lastly, the duration of quiet intervals plays a crucial role in determining the likelihood of transitioning to either bursting or single spiking modes. We confirmed that the same features were present in previously recorded in vivo voltage-imaging data. Understanding these dynamics provides valuable insights into the fundamental mechanisms underlying neuronal excitability underin vivoconditions.Author summarySince discovering that neurons in the hippocampus can encode spatial position through phase precession, many experiments have explored how specific theta and gamma oscillations influence location specificity in the brain. However, the individual neuronal properties and dynamics behind these behaviors are still being uncovered. Previously, we found that stereotypical bursting and single-spike firing in pyramidal neurons are linked to these oscillations and further associated with an animal entering or leaving a place field. Advances in voltage-imaging techniques have enabled us to assess these properties more precisely. Our study shows that different frequencies can independently trigger these stereotypical spikes, demonstrating a complex pattern where the same cell can be double-coded: a phenomenon we called interleaved resonance. Additionally, we found that this coding can be modulated by persistent sodium and delayed-rectifier potassium currents. Moreover, these neurons are more likely to burst following long periods of silence. These findings provide new insights into the mechanisms underlying neural coding in the hippocampus and how it relates to behavior.
Global and local nature of cortical slow waves
Explaining the macroscopic activity of a recorded neuronal population from its known microscopic properties still poses a great challenge, not just because of the many local agents that shape the output of a circuit, but due to the impact of long-range connections from other brain regions. Here we use a computational model to explore how local and global components of a network shape the Slow Wave Activity (SWA). We performed a sensitivity analysis of multiple cellular and synaptic features in models of isolated and connected networks. This allowed us to explore how the interaction of local properties and long-range connections shape the SWA of a population and its neighbors, as well as how the sequential propagation of active Up states lead to the emergence of preferred modes of propagation. We described relevant features of cortical Up states that are modulated by stiff combinations of parameters of the local circuit as opposed to other that are sensitive to the level of excitability of the whole network and the input coming from neighbor populations. We found that while manipulations in the synaptic excitatory/inhibitory balance can create local changes, cellular components that modulate the excitability or adaptation of a population have a long-range effect that leads to changes in neighbor populations too. Additionally, our simulations guided in vivo experiments that showed how heterogeneities in excitability between cortical areas can determine the directionality of travelling waves during SWA. We expect these results to motivate future research exploring and comparing cortical circuits through the analysis of their Up states.
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