Single-axon action potentials in the rat hippocampal cortex

Abstract

Whether all action potentials propagate faithfully throughout axon arbors in the mammalian CNS has long been debated, and remains an important issue because many synapses occur far from the soma along extremely thin, unmyelinated, varicosity-laden branches of axon arbors. We detected unitary action potentials along individual axon branches of adult hippocampal CA3 pyramidal cells using extracellular electrodes, and analysed their conduction across long distances (mean, 2.1 mm) at 22 and 37 degrees C. Axons nearly always transmitted low-frequency impulses. At higher frequencies, most axons also transmitted impulses with striking fidelity. However, at paired-pulse frequencies in the hundreds of kilohertz range, axons exhibited variability: refractory periods ranged from 2.5 to 10 ms at 37 degrees C and from 5 to 40 ms at 22 degrees C. Although the basis for the refractory period variability could not be determined, these limits overlap with CA3 spike frequencies observed in vivo, raising the possibility that some axonal branches act as filters for the higher-order spikes in bursts, in contrast to the observed first-spike reliability. These results extend the observations of propagation reliability to a much longer distance and higher frequency domain than previously reported, and suggest a high safety factor for action potential propagation along thin, varicose axons.

Information processing in the axon

“…But it will also be extremely important to use other probes that do not perturb the rather fragile equilibrium that underlies propagation. Non-invasive recording techniques such as extracellular recording from single axons will be extremely helpful 39,81,100,131 .…”

“…Propagation failures have been induced in only 30% of cases 66 , showing that propagation is generally reliable in hippocampal axons [98][99][100] . I A -dependent conduction failures occur at some axon collaterals but not at others 66 .…”

Potassium diffusive coupling in neural networks

“…Historically, studies have emphasized the effect of electrical stimulation on activity at the cell body, with suppression of somatic activity during stimulation predominating (figure 7a,b;D'Ambrosio et al 1998;Beurrier et al 2001;Bikson et al 2001;Garcia et al 2003;Lee et al 2003;Richardson et al 2003;D'Ambrosio 2004). Recent studies have shown that electrical stimulation also generates changes in axonal activity (Raastad & Shepherd 2003;Soleng et al 2004;Meeks et al 2005;Iremonger et al 2006;De Col et al 2008) including a depression of excitatory synaptic currents (Iremonger et al 2006;Schiller & Bankirer 2007), and conduction blockade in the PNS (Kilgore & Bhadra 2006;Ragnarsson 2007;Tai et al 2007) and in the CNS (figure 7c; Jensen & Durand 2007). Thus, changes in neural activity induced by electrical stimulation provide a means to modulate abnormal communication at several levels within the target network.…”

Effects of Axonal Topology on the Somatic Modulation of Synaptic Outputs

“…Although eAPs recorded from local field potentials (LFPs) are thought to reflect the derivative of intracellularly recorded APs (iAPs), the origin of eAPs monitored by cell-attached recording is controversial (Raastad and Shepherd, 2003;Khaliq and Raman, 2006;Perkins, 2006). Therefore, we simultaneously recorded and compared the waveforms of iAPs (whole cell) and eAPs (cell attached) from cell bodies of CA3 pyramidal cells and eAPs recorded in LFPs (Fig.…”