Distinct classes of pyramidal cells exhibit mutually exclusive firing patterns in hippocampal area CA3b

Abstract

It is thought that CA3 pyramidal neurons communicate mainly through bursts of spikes rather than so-called trains of regular firing action potentials. Reports of both burst firing and nonburst firing CA3 cells suggest that they may fire with more than one output pattern. With the use of whole-cell recording methods we studied the firing properties of rat hippocampal pyramidal neurons in vitro within the CA3b subregion and found three distinct types of firing patterns. Approximately 37% of cells were regular firing where spikes generated by minimal current injection (rheobase) were elicited with a short latency and with stronger current intensities trains of spikes exhibited spike frequency adaptation (SFA). Another 46% of neurons exhibited a delayed onset at rheobase with a weakly-adapting firing pattern upon stronger stimulation. The remaining 17% of cells showed a burst-firing pattern, though only elicited in response to strong current injection and spontaneous bursts were never observed. Control experiments indicated that the distinct firing patterns were not due to our particular slicing methods or recording techniques. Finally, computer modeling was used to identify how relative differences in K+ conductances, specifically K(C), K(M), and K(D), between cells contribute to the different characteristics of the three types of firing patterns observed experimentally.

Spike-Time Precision and Network Synchrony Are Controlled by the Homeostatic Regulation of the D-Type Potassium Current

“…No change in resting membrane potential was induced by the drugs (Ϫ69.7 Ϯ 1.6 mV in control vs Ϫ69.7 Ϯ 1.5 mV; p ϭ 0.8). In contrast, the channel blocker tetraethylammonium (TEA; 5 mM) had no effect ( similar to an I D -like current (Storm, 1988;Luthi et al, 1996;Mitterdorfer and Bean, 2002;Hemond et al, 2008) present in CA3 pyramidal neurons in acute slices (supplemental Fig. S2, available at www.jneurosci.…”

“…A compartmental Hodgkin-Huxley model was implemented in NEURON (version 6.2, available at http:// www.neuron.yale.edu/neuron/) using the previously published CA3 model of Hemond et al (2008). Three different model morphologies were verified to exhibit the same qualitative behavior: (1) a fully reconstructed CA3 neuron, (2) a reduced reconstructed CA3 neuron, and (3) a ball-and-stick CA3 neuron.…”

“…Current densities were uniformly distributed in all compartments, and the model was tested to give similar results within a range of these current densities. Each current was specified as a firstorder differential equation following Hodgkin and Huxley formalisms and were identical to the equations in Hemond et al (2008). The Na ϩ channel density was increased 10-fold in the axon, and it was verified that APs were initiated in the axon.…”

“…The Na ϩ channel density was increased 10-fold in the axon, and it was verified that APs were initiated in the axon. The model was run at 35°C, the membrane capacitance was 1.41 uF/cm 2 , and the time step was 0.0125 ms. To introduce channel noise, a stochastic Na ϩ channel was implemented using the NEURON-extension NMODL (Hines and Carnevale, 2000) based on the deterministic Na ϩ channel (Hemond et al, 2008). The stochastic Na ϩ channel was implemented as an approximation to a full Markov model following the algorithm of Fox (1997).…”

Cannabinoid-mediated short-term plasticity in hippocampus

“…Further details about α ψ and β ψ (ψ = h E , n E , m E ) and the parameters of the model can be found in (Huguenard and Mccormick, 1994) and were obtained from ModelDB (accession number: 3808) (Hines et al, 2004). The Ca 2+ current I Ca,L through the L-type VGCC is described by a Goldman-Hodgkin-Katz (GHK) equation for Ca 2+ (Hemond et al, 2008;Zachariou et al, 2013). The equations describing concentration of Ca 2+ in the cytoplasm (c) can be found in subsection 4.5.1.…”