High frequency action potential bursts (≥ 100 Hz) in L2/3 and L5B thick tufted neurons in anaesthetized and awake rat primary somatosensory cortex

Abstract

High frequency (>or= 100 Hz) bursts of action potentials (APs) generated by neocortical neurons are thought to increase information content and, through back-propagation, to influence synaptic integration and efficacy in distal dendritic compartments. It was recently shown in acute slice experiments that intrinsic bursting properties differ between neocortical L2/3 and L5B (thick tufted) neurons. In L2/3 neurons for instance, dendritic APs were brief and generated only one additional AP after the initial somatic AP. In L5B neurons, dendritic plateau potentials facilitated the generation of trains of three or more APs. We recently showed in vivo that spiking frequencies are very different for L2/3 and L5B thick tufted neurons under anaesthesia. Here, we addressed the question whether in vivo the bursting properties are different for these two cell types. We recorded from L2/3 and L5B thick tufted neurons of rat primary somatosensory (barrel) cortex under anaesthetized and awake conditions and found that AP activity is dominated by single APs. In addition, we found that in the anaesthetized animal also bursts of two APs were observed in L2/3 neurons but the relative occurrence of these bursts was low. In L5B thick tufted neurons, bursts consisting of up to six APs were recorded and their relative occurrence was significantly higher. Frequencies within bursts were also significantly higher in L5B thick tufted neurons than in L2/3 neurons. In awake (head-restrained) animals, average spike frequencies of L2/3 and L5B thick tufted neurons were surprisingly similar to spike rates under anaesthesia. However, bursting behaviour in L2/3 neurons was comparable to L5B thick tufted neurons. Thus, the distribution of interspike intervals was changed in L2/3 neurons without affecting the average spiking rate. We observed bursts consisting of up to five APs in both cell types and both probability of bursts and AP frequency within bursts were similar for L2/3 and L5B thick tufted neurons. Our analysis shows that most cortical APs occur as single APs, although a minor fraction of APs in L2/3 and L5B thick tufted neurons are part of high frequency bursts (15%). This AP bursting is dependent on the behavioural state of the animal in a cell-type dependent manner.