Conditional Bursting Enhances Resonant Firing in Neocortical Layer 2–3 Pyramidal Neurons

Higgs, Matthew H.; Spain, William J.

doi:10.1523/jneurosci.3728-08.2009

Cited by 97 publications

(165 citation statements)

References 82 publications

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“…Therefore, although the fAHP amplitude is strongly correlated to f STA , its presence alone is not sufficient to confer spectral selectivity upon spike initiation dynamics. Albeit being a correlative inference from our results, future studies could use ion channels involved in spike repolarization and fAHP differences between pyramidal and interneurons as instruments with which to understand the relationship between spike repolarization and initiation dynamics from a neural coding perspective (Higgs and Spain, 2009;Famulare and Fairhall, 2010;Kispersky et al, 2012;Mease et al, 2013). Finally, our study also highlights the utility of spectral and spectrotemporal analyses in understanding the physiological roles of ion channels and their interactions.…”

Section: Biophysics Of Frequency Selectivity In Neuronal Spike Initiamentioning

confidence: 58%

Active Dendrites Regulate Spectral Selectivity in Location-Dependent Spike Initiation Dynamics of Hippocampal Model Neurons

2014

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How does the presence of plastic active dendrites in a pyramidal neuron alter its spike initiation dynamics? To answer this question, we measured the spike-triggered average (STA) from experimentally constrained, conductance-based hippocampal neuronal models of various morphological complexities. We transformed the STA computed from these models to the spectral and the spectrotemporal domains and found that the spike initiation dynamics exhibited temporally localized selectivity to a characteristic frequency. In the presence of the hyperpolarization-activated cyclic nucleotide-gated (HCN) channels, the STA characteristic frequency strongly correlated with the subthreshold resonance frequency in the theta frequency range. Increases in HCN channel density or in input variance increased the STA characteristic frequency and its selectivity strength. In the absence of HCN channels, the STA exhibited weak delta frequency selectivity and the characteristic frequency was related to the repolarization dynamics of the action potentials and the recovery kinetics of sodium channels from inactivation. Comparison of STA obtained with inputs at various dendritic locations revealed that nonspiking and spiking dendrites increased and reduced the spectrotemporal integration window of the STA with increasing distance from the soma as direct consequences of passive filtering and dendritic spike initiation, respectively. Finally, the presence of HCN channels set the STA characteristic frequency in the theta range across the somatodendritic arbor and specific STA measurements were strongly related to equivalent transfer-impedance-related measurements. Our results identify explicit roles for plastic active dendrites in neural coding and strongly recommend a dynamically reconfigurable multi-STA model to characterize location-dependent input feature selectivity in pyramidal neurons.

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Section: Biophysics Of Frequency Selectivity In Neuronal Spike Initiamentioning

confidence: 58%

Active Dendrites Regulate Spectral Selectivity in Location-Dependent Spike Initiation Dynamics of Hippocampal Model Neurons

2014

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“…The first interval is plotted on the vertical axis and the subsequent interval is plotted on the horizontal axis. If spike doublets occurred with greater frequency (Traub et al, 1996;Higgs and Spain, 2009), we should find short intervals preceding longer intervals, as well as longer intervals preceding short intervals. A high occurrence of doublets would appear as vertical and horizontal bands on the 2D histogram (Fig.…”

Section: Interspike Interval Distributionsmentioning

confidence: 98%

Natural Movies Evoke Spike Trains with Low Spike Time Variability in Cat Primary Visual Cortex

Herikstad¹,

Baker²,

Lachaux³

et al. 2011

J. Neurosci.

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Neuronal responses in primary visual cortex have been found to be highly variable. This has led to the widespread notion that neuronal responses have to be averaged over large numbers of neurons to obtain suitably invariant responses that can be used to reliably encode or represent external stimuli. However, it is possible that the high variability of neuronal responses may result from the use of simple, artificial stimuli and that the visual cortex may respond differently to dynamic, naturalistic images. To investigate this question, we recorded the responses of primary visual cortical neurons in the anesthetized cat under stimulation with time-varying natural movies. We found that cortical neurons on the whole exhibited a high degree of spike count variability, but a surprisingly low degree of spike time variability. The spike count variability was further reduced when all but the first spike in a burst were removed. We also found that responses exhibiting low spike time variability exhibited low spike count variability, suggesting that rate coding and temporal coding might be more compatible than previously thought. In addition, we found the spike time variability to be significantly lower when stimulated by natural movies as compared with stimulation using drifting gratings. Our results indicate that response variability in primary visual cortex is stimulus dependent and significantly lower than previous measurements have indicated.

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“…Repetitive firing behavior also changes with age Christophe et al 2005;Kasper et al 1994aKasper et al , 1994bLorenzon and Foehring 1993;Maravall et al 2004aMaravall et al , 2004bMcCormick and Prince 1987;Metherate and Aramkis 1999;Oswald and Reyes 2008;van Brederode et al 2000;Zhang 2004). In mature pyramidal neurons, voltage-gated K ϩ channels contribute to the filtering and integration of synaptic inputs, as well as shaping firing rates and pattern (Guan et al 2007a;Higgs and Spain 2009;Schwindt et al 1988). Developmental changes in these channels should therefore play significant roles in the maturation of pyramidal cell function.…”

mentioning

confidence: 99%

Postnatal development of A-type and Kv1- and Kv2-mediated potassium channel currents in neocortical pyramidal neurons

Guan

Horton

Armstrong

et al. 2011

Journal of Neurophysiology

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Guan D, Horton LR, Armstrong WE, Foehring RC. Postnatal development of A-type and Kv1-and Kv2-mediated potassium channel currents in neocortical pyramidal neurons. J Neurophysiol 105: 2976-2988, 2011. First published March 30, 2011 doi:10.1152/jn.00758.2010.-Potassium channels regulate numerous aspects of neuronal excitability, and several voltage-gated K ϩ channel subunits have been identified in pyramidal neurons of rat neocortex. Previous studies have either considered the development of outward current as a whole or divided currents into transient, A-type and persistent, delayed rectifier components but did not differentiate between current components defined by ␣-subunit type. To facilitate comparisons of studies reporting K ϩ currents from animals of different ages and to understand the functional roles of specific current components, we characterized the postnatal development of identified Kv channel-mediated currents in pyramidal neurons from layers II/III from rat somatosensory cortex. Both the persistent/slowly inactivating and transient components of the total K ϩ current increased in density with postnatal age. We used specific pharmacological agents to test the relative contributions of putative Kv1-and Kv2-mediated currents (100 nM ␣-dendrotoxin and 600 nM stromatoxin, respectively). A combination of voltage protocol, pharmacology, and curve fitting was used to isolate the rapidly inactivating A-type current. We found that the density of all identified current components increased with postnatal age, approaching a plateau at 3-5 wk. We found no significant changes in the relative proportions or kinetics of any component between postnatal weeks 1 and 5, except that the activation time constant for A-type current was longer at 1 wk. The putative Kv2-mediated component was the largest at all ages. Immunocytochemistry indicated that protein expression for Kv4.2, Kv4.3, Kv1.4, and Kv2.1 increased between 1 wk and 4 -5 wk of age. Kv channel; somatosensory cortex; voltage clamp; A current; delayed rectifier AT BIRTH, the rodent somatosensory system is immature, and somatosensory cortex undergoes dramatic changes over the first postnatal month. Neocortical pyramidal cells are generated prenatally in an "inside-out" laminar pattern (Caviness 1982; Caviness et al.

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Conditional Bursting Enhances Resonant Firing in Neocortical Layer 2–3 Pyramidal Neurons

Cited by 97 publications

References 82 publications

Active Dendrites Regulate Spectral Selectivity in Location-Dependent Spike Initiation Dynamics of Hippocampal Model Neurons

Active Dendrites Regulate Spectral Selectivity in Location-Dependent Spike Initiation Dynamics of Hippocampal Model Neurons

Natural Movies Evoke Spike Trains with Low Spike Time Variability in Cat Primary Visual Cortex

Postnatal development of A-type and Kv1- and Kv2-mediated potassium channel currents in neocortical pyramidal neurons

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