Recurrent Synaptic Input and the Timing of Gamma-Frequency-Modulated Firing of Pyramidal Cells during Neocortical “UP” States

Morita, Kenji; Kalra, Rita; Aihara, Kazuyuki; Robinson, Hugh P. C.

doi:10.1523/jneurosci.3948-07.2008

Cited by 67 publications

(52 citation statements)

References 50 publications

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“…Gamma-band synchronization within a local group of neurons entails rhythmic inhibition through the local inhibitory interneuron network (Csicsvari et al, 2003;Hasenstaub et al, 2005;Vida et al, 2006;Buzsáki, 2006;Bartos et al, 2007;Morita et al, 2008). The gamma-rhythmic inhibition constitutes a gamma cycle that might impact neuronal processing .…”

Section: Introductionmentioning

confidence: 99%

Gamma-Phase Shifting in Awake Monkey Visual Cortex

Vinck¹,

Lima²,

Womelsdorf³

et al. 2010

J. Neurosci.

171

205

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Gamma-band synchronization is abundant in nervous systems. Typically, the strength or precision of gamma-band synchronization is studied. However, the precise phase with which individual neurons are synchronized to the gamma-band rhythm might have interesting consequences fortheirimpactonfurtherprocessingandforspiketiming-dependentplasticity.Therefore,weinvestigatedwhetherthespiketimesofindividual neurons shift systematically in the gamma cycle as a function of the neuronal activation strength. We found that stronger neuronal activation leads to spikes earlier in the gamma cycle, i.e., we observed gamma-phase shifting. Gamma-phase shifting occurred on very rapid timescales. It was particularly pronounced for periods in which gamma-band synchronization was relatively weak and for neurons that were only weakly coupled to the gamma rhythm. We suggest that gamma-phase shifting is brought about by an interplay between overall excitation and gammarhythmic synaptic input and has interesting consequences for neuronal coding, competition, and plasticity.

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Section: Introductionmentioning

confidence: 99%

Gamma-Phase Shifting in Awake Monkey Visual Cortex

Vinck¹,

Lima²,

Womelsdorf³

et al. 2010

J. Neurosci.

171

205

View full text Add to dashboard Cite

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“…They have an intrinsic resonance near these frequencies, which is evident in their minimum repetitive firing rate of 10 -30 spikes/s (Golomb et al 2007;Tateno et al 2004). Feedback excitation of cortical FS cells during persistent activity engages this resonance (Hausenstaub et al 2005;Morita et al 2008) to produce oscillatory inhibition in the cortex. Because of these properties, cortical FS cells are easily synchronized by noisy shared synaptic excitation and gap junctions (Galaretta and Hestrin 1999; Gibson et al 1999;Mancilla et al 2007;Tateno and Robinson 2009).…”

mentioning

confidence: 99%

The ionic mechanism of gamma resonance in rat striatal fast-spiking neurons

Sciamanna

Wilson

2011

Journal of Neurophysiology

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Sciamanna G, Wilson CJ. The ionic mechanism of gamma resonance in rat striatal fast-spiking neurons. J Neurophysiol 106: 2936-2949, 2011. First published August 31, 2011 doi:10.1152/jn.00280.2011.-Striatal fast-spiking (FS) cells in slices fire in the gamma frequency range and in vivo are often phase-locked to gamma oscillations in the field potential. We studied the firing patterns of these cells in slices from rats ages 16 -23 days to determine the mechanism of their gamma resonance. The resonance of striatal FS cells was manifested as a minimum frequency for repetitive firing. At rheobase, cells fired a doublet of action potentials or doublets separated by pauses, with an instantaneous firing rate averaging 44 spikes/s. The minimum rate for sustained firing was also responsible for the stuttering firing pattern. Firing rate adapted during each episode of firing, and bursts were terminated when firing was reduced to the minimum sustainable rate. Resonance and stuttering continued after blockade of Kv3 current using tetraethylammonium (0.1-1 mM). Both gamma resonance and stuttering were strongly dependent on Kv1 current. Blockade of Kv1 channels with dendrotoxin-I (100 nM) completely abolished the stuttering firing pattern, greatly lowered the minimum firing rate, abolished gamma-band subthreshold oscillations, and slowed spike frequency adaptation. The loss of resonance could be accounted for by a reduction in potassium current near spike threshold and the emergence of a fixed spike threshold. Inactivation of the Kv1 channel combined with the minimum firing rate could account for the stuttering firing pattern. The resonant properties conferred by this channel were shown to be adequate to account for their phase-locking to gamma-frequency inputs as seen in vivo. basal ganglia; interneurons; firing patterns; stuttering; spike frequency adaptation STRIATAL LOCAL FIELD POTENTIALS contain gamma-frequency (35-80 Hz) oscillations that are modulated during behavior (e.g

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“…One hundred and two hundred active excitatory synapses, each with a mean firing frequency of 3 Hz, were distributed among the basal and distal dendrites, respectively. The presynaptic spikes that generate oscillatory inhibition have a default fixed average frequency summed over the whole population of inhibitory synapses of 2,000/s and follow a Gaussian-like phase distribution resembling that during in vivo gamma oscillations (Hasenstaub et al 2005;Morita et al 2008):…”

Section: Resultsmentioning

confidence: 99%

“…LTS cells have been shown to form an electrically coupled network via specific gap junctions (Gibson et al 1999), which is distinct from the network of fast spiking (FS) cells, another class of GABAergic interneurons, which, in contrast, selectively targets pyramidal somata and proximal dendrites. Several studies (Fanselow and Connors 2010;Fanselow et al 2008;Mancilla et al 2007;Vierling-Claassen et al 2010) have suggested that LTS cells can fire in synchrony at relatively slow frequencies (5ϳ30 Hz, around the -to ␤-frequency ranges), presumably by virtue of electrical coupling, again in contrast to the FS cells, which typically show synchronized firing in the ␥-frequency range (30ϳ80 Hz) (Buszsaki 2006;Fries 2009;Gouwens et al 2010;Hasenstaub et al 2005;Kopell and Ermentrout 2004;Morita et al 2008;Tateno et al 2004;Tiesinga and Sejnowski 2009;Wang and Buzsaki 1996;Whittington and Traub 2003). Cholinergic agonists induce beta oscillations in superficial layers of prefrontal cortical slices, which are independent of rhythms in the deeper layers (van Aerde et al 2009).…”

mentioning

confidence: 99%

“…Experimentally controlling a large number of synaptic inputs to a single pyramidal cell is effectively impossible, and thus compartmental modeling (Mel 1993;Rall 1964;Segev et al 1989) has been used extensively to study synaptic integration. However, to our knowledge, no computational study has so far focused on the effects of distal, distributed oscillating inhibition, except in morphologically simplified models (Vierling-Claassen et al 2010), or where inhibition was uniformly spread over the whole dendritic tree, and oscillation frequency was fixed in the ␥-range (Morita et al 2008). In this work, we used detailed compartmental models of layer 5 pyramidal cells to examine how inhibitory inputs distributed specifically over the apical tuft dendrites regulate neuronal output, depending on the degree and frequency of common rhythmic modulation of these inputs.…”

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confidence: 99%

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Control of layer 5 pyramidal cell spiking by oscillatory inhibition in the distal apical dendrites: a computational modeling study

Morita

Robinson

et al. 2013

Journal of Neurophysiology

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Li X, Morita K, Robinson HP, Small M. Control of layer 5 pyramidal cell spiking by oscillatory inhibition in the distal apical dendrites: a computational modeling study. J Neurophysiol 109: 2739-2756, 2013. First published March 13, 2013 doi:10.1152/jn.00397.2012.-The distal apical dendrites of layer 5 pyramidal neurons receive cortico-cortical and thalamocortical top-down and feedback inputs, as well as local recurrent inputs. A prominent source of recurrent inhibition in the neocortical circuit is somatostatin-positive Martinotti cells, which preferentially target distal apical dendrites of pyramidal cells. These electrically coupled cells can fire synchronously at various frequencies, including over a relatively slow range (5ϳ30 Hz), thereby imposing oscillatory inhibition on the pyramidal apical tuft dendrites. We examined how such distal oscillatory inhibition influences the firing of a biophysically detailed layer 5 pyramidal neuron model, which reproduced the spatiotemporal properties of sodium, calcium, and N-methyl-D-aspartate receptor spikes found experimentally. We found that oscillatory synchronization strongly influences the impact of distal inhibition on the pyramidal cell firing. Whereas asynchronous inhibition largely cancels out the facilitatory effects of distal excitatory inputs, inhibition oscillating synchronously at around 10ϳ20 Hz allows distal excitation to drive axosomatic firing, as if distal inhibition were absent. Underlying this is a switch from relatively infrequent burst firing to single spike firing at every period of the inhibitory oscillation. This phenomenon depends on hyperpolarization-activated cation current-dependent membrane potential resonance in the dendrite, but also, in a novel manner, on a cooperative amplification of this resonance by N-methyl-D-aspartate-receptor-driven dendritic action potentials. Our results point to a surprising dependence of the effect of recurrent inhibition by Martinotti cells on their oscillatory synchronization, which may control not only the local circuit activity, but also how it is transmitted to and decoded by downstream circuits. resonance; beta oscillation; NMDA receptor; I h NEOCORTICAL LAYER 5 PYRAMIDAL neurons are characterized by extensively branched apical tuft dendrites in cortical layer 1, which are known to receive top-down and feedback inputs from cortical and thalamic regions (Cauller 1995;Larkum et al. 2009;Oda et al. 2004; Thomson and Bannister 2003). Besides these excitatory inputs, recent studies (Kapfer et al. 2007;Murayama et al. 2009;Silberberg and Markram 2007) Whittington and Traub 2003). Cholinergic agonists induce beta oscillations in superficial layers of prefrontal cortical slices, which are independent of rhythms in the deeper layers (van Aerde et al. 2009). It is, therefore, quite likely that LTS cell-mediated recurrent inhibition onto the pyramidal apical tuft dendrites is modulated at frequencies in the -to ␤-range in certain conditions in vivo. To understand the operation of recurrent inhibition in the neoco...

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Recurrent Synaptic Input and the Timing of Gamma-Frequency-Modulated Firing of Pyramidal Cells during Neocortical “UP” States

Cited by 67 publications

References 50 publications

Gamma-Phase Shifting in Awake Monkey Visual Cortex

Gamma-Phase Shifting in Awake Monkey Visual Cortex

The ionic mechanism of gamma resonance in rat striatal fast-spiking neurons

Control of layer 5 pyramidal cell spiking by oscillatory inhibition in the distal apical dendrites: a computational modeling study

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