Action Potentials in Basal and Oblique Dendrites of Rat Neocortical Pyramidal Neurons

Abstract

Basal and oblique dendrites comprise ~2/3 of the total excitable membrane in the mammalian cerebral cortex, yet they have never been probed with glass electrodes, and therefore their electrical properties and overall impact on synaptic processing are unknown. In the present study, fast multisite voltage-sensitive dye imaging combined with somatic recording was used to provide a detailed description of the membrane potential transients in basal and oblique dendrites of pyramidal neurons during single and trains of action potentials (APs). The optical method allowed simultaneous measurements from several dendrites in the visual field up to 200 mm from the soma, thus providing a unique report on how an AP invades the entire dendritic tree. In contrast to apical dendrites, basal and oblique branches: (1) impose very little amplitude and time course modulation on backpropagating APs; (2) are strongly invaded by the somatic spike even when somatic firing rates reach 40 Hz (activity-independent backpropagation); and (3) do not exhibit signs of a 'calcium shoulder' on the falling phase of the AP. A compartmental model incorporating AP peak latencies and half-widths obtained from the apical, oblique and basal dendrites indicates that the specific intracellular resistance (R i ) is less than 100 V cm. The combined experimental and modelling results also provide evidence that all synaptic locations along basal and oblique dendrites, situated within 200 mm from the soma, experience strong and near-simultaneous (latency < 1 ms) voltage transients during somatic firing. The cell body, axon hillock and basal dendritic compartments achieve unique synchronization during each AP. Therefore, with respect to a retrograde signal (AP), basal and proximal oblique dendrites should be considered as an integral part of the axo-somatic compartment. Journal of PhysiologyIn order to understand how fine neocortical dendrites process electrical signals, it is necessary to experimentally characterize the actual membrane potential transients in basal and oblique dendrites just as they were characterized in the apical dendrite (Stuart & Sakmann, 1994;Larkum et al. 2001). The objective of this study was to implement a new technique for optical imaging of membrane potential transients in distal segments of basal and oblique dendrites, and estimate dendritic electrical properties by comparing the actual experimental measurements with traces generated in computer simulations. METHODS Intracellular application of the dyesSprague-Dawley rats (postnatal day (P)21-35) were deeply anaesthetized with halothane and decapitated according to an animal protocol approved by the Yale University Animal Care and Use Committee. Coronal brain slices (300 mm thick) were harvested from the somatosensory area in gassed (95 % O 2 and 5 % CO 2 ), ice-cold artificial cerebrospinal fluid (ACSF, mM): 125 NaCl, 26 NaHCO 3 , 10 glucose, 2.3 KCl, 1.26 KH 2 PO 4 , 2 CaCl 2 and 1 MgSO 4 (pH 7.4, osmolarity 300-310 mosmol l _1 ). The slices were incubated for 30 min at 35°C and...

The Properties and Implications of NMDA Spikes in Neocortical Pyramidal Cells

“…1 B), according to previous work modeling this cell (Rhodes and Gray, 1994;Rhodes, 1999;Rhodes and Llinás, 2001), in which details of current kinetics may be found. The distribution of dendritic ionic conductances included Na ϩ conductance density (12 mS/cm 2 ) in the basal dendrites consistent with the measurements of Antic (2003), along with high-threshold Ca 2ϩ densities of 6 -12 mS/cm 2 , adequate to drive the bursts characteristic of this cell type (McCormick et al, 1985;Rhodes and Gray, 1994). The distribution of ionic conductance densities specified in Table 1 was used for all that were simulated, unless specifically noted otherwise.…”

Initiation of Sodium Spikelets in Basal Dendrites of Neocortical Pyramidal Neurons

“…Backpropagating APs have the advantage of being generated in the soma. They start with impressive amplitudes (~ 100 mV), and even in the absence of dendritic sodium conductance they can backpropagate passively and cause substantial voltage transients in basal dendrites, as revealed in the detailed multicompartmental models of the pyramidal layer V neuron (Rapp et al, 1996;Vetter, Roth & Hausser, 2001;Antic, 2003). Locally triggered basal spikelets on the other hand, not only lack the passive boost of the somatic AP, but even worse, their generator current is sucked up by an enormous nearby current sink -the cell body.…”

“…Basal spikelets could perhaps be just a side product of sodium channel proteins that were originally placed there to support action potential backpropagation in thin dendrites (Antic, 2003). These and other hypotheses concerning the functional significance of basal spikes, and their potential role in cortical signal processing, are currently under active investigation.…”

Imaging membrane potential in dendrites and axons of single neurons

“…Using this method to compare the first and third action potential signal in a burst, a recent study concluded that action potentials are significantly attenuated as they propagate into distal The increasing delay between the signal from the somatic region and proximal dendritic segments reflects the time taken for the propagation of the action potential to dendritic locations. Taken from [2] basal dendrites of pyramidal neurons [26], in contrast to the conclusions of Antic [5].…”

“…2) [2]. A follow-up study examined action potential back-propagation into basal dendrites in cortical pyramidal neurons in more detail [5], concluding that action potentials backpropagate up to 200 μm from the soma with little amplitude and shape modulation.…”