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

Abstract

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...

Spike Firing and IPSPs in Layer V Pyramidal Neurons during Beta Oscillations in Rat Primary Motor Cortex (M1) In Vitro

“…One such candidate is the low-threshold spiking (LTS) cell [37], [38], [39] which preferentially targets distal apical dendrites [35], [38] and which have been shown to undergo oscillatory activity in the beta range by a number of groups [44], [45], [46]. In a recent computational modelling study [47], distal dendrite targeting ‘Martinotti’ cells have been proposed to control layer V neocortical pyramidal cell spiking in the 5–30 Hz range through oscillatory inhibition, which serves to allow distal dendritic excitation to drive somatic spiking. By contrast, asynchronous distal dendritic inhibition may facilitate more irregular burst firing.…”

A developmental cell-type switch in cortical interneurons leads to a selective defect in cortical oscillations

“…On the basis of modelling studies, the lack of fast signalling properties of the PV+ interneurons, including synaptic kinetics, rapid action potentials and high intrinsic resonance frequency, is likely to play a critical role in the observed oscillatory phenotype131443. In addition, the SST+ interneurons, which innervate distal dendrites of cortical pyramidal neurons, have also been shown to synchronize even though at lower (<30 Hz) frequencies44. Therefore, the genetic deletion of SST+ interneurons may also contribute to the oscillatory phenotype observed in the Nkx2-1 E12.5LOF cortex.…”

Burst Firing Synchronizes Prefrontal and Anterior Cingulate Cortex during Attentional Control

“…prepared the manuscript. [12], which may be facilitated when the dendritic membranes undergo rhythmic inhibition at the 10-20 Hz frequency to which distal dendrites resonate [37]. Such a putative rhythmic gate of bursts is expected to be activated during intermediate levels of depolarization.…”