Apical dendrites of the neocortex: correlation between sodium- and calcium-dependent spiking and pyramidal cell morphology

Abstract

Apical dendrites and somata of layer V pyramidal neurons were recorded with tight-seal patch electrodes in a slice preparation of rat somatosensory cortex. Recording sites were confirmed by measurements of the electrode location and by staining with biocytin. Dendritic recordings were made along the main trunk of the apical dendrite, usually within layer IV, at distances from 100 to 500 microns from the soma. Most cells recorded through the dendrite had a distinct enlargement of the apical trunk around the presumed recording site. The electrical properties of apical dendrites were readily distinguishable from those of somata. Dendrites generated two types of response when injected with depolarizing current. Group I responses were relatively small and broad Na(+)-dependent action potentials whose amplitude and rate-of-rise were negatively correlated with recording distance from the soma. Group II responses were complex, clustered firing patterns of Na(+)-dependent spikes together with higher-threshold slow spikes or plateaus; in these dendrites spike parameters were not correlated with distance from the soma. These two response groups were correlated with dendritic morphology: group I had significantly fewer oblique branches on the apical dendrite (5.5 vs 12.0) and a thinner apical trunk (2.0 vs 2.5 microns) than group II. TTX (1-2 microM) selectively blocked fast dendritic spikes, but not slow spikes and plateaus. Blocking Ca2+ currents reduced complex firing patterns and suppressed high-threshold slow spikes. Physiological and pharmacological studies imply that slow spikes and plateau potentials were primarily generated by high-threshold Ca2+ channels in the apical dendrite. Stimulating axons of layer I elicited EPSPs on distal apical dendrites of layer V cells. Recordings from both groups of apical dendrites revealed that EPSPs triggered a variety of distally generated, all-or-nothing depolarizations. The results show that voltage-dependent Na+ and Ca2+ currents are present in distal apical dendrites, in variable densities. These currents significantly modify distal synaptic events. The prevalence and character of active dendritic spiking (and presumably of Na+ and Ca2+ channel densities) correlate with the morphology of the apical dendritic tree.

Inhibitory control of somatodendritic interactions underlying action potentials in neocortical pyramidal neurons in vivo: An intracellular and computational study

“…14C). This is in agreement with previous intracellular studies of neocortical pyramidal cells in vivo and in vitro 5,9,30,52 where it was observed that synaptic stimuli can elicit dendritic spikes (reviewed in Ref. 66).…”

“…In inferior olivary cells, this shoulder is mediated by high-threshold dendritic Ca 2+ currents. 35,36 Since pyramidal cells possess similar dendritic conductances, 30,67 and pyramidal neurons generate dendritic Ca 2+ plateaus in the presence of K + channel blockers, 53,67 a similar mechanism probably contributed to the spike shoulder observed here. In computer simulations of Cs + recordings, it was determined that Na + currents generated by the proximal 300 µm of the dendrites contributed to the falling phase of the somatic APs.…”

“…However, the applicability of this model to other cell types was questioned when the first intradendritic recordings revealed that dendrites can sustain active electrogenesis. 33,34,63 In neocortical and hippocampal pyramidal neurons for instance, intracellular recordings revealed that dendritic spikes can be elicited by synaptic inputs 5,9,30,52 and that they can amplify synaptic inputs electrotonically distant from the soma to initiate APs. 5 Moreover, the proximal apical dendrites of pyramidal neurons were found to contain voltage-gated Ca 2+ and Na + conductances capable of generating current densities similar to those observed at the soma.…”

Diversity of Gain Modulation by Noise in Neocortical Neurons: Regulation by the Slow Afterhyperpolarization Conductance

“…Spatial factors may affect the gain increase and its modulation by G sAHP . Na ϩ and Ca 2ϩ spikes generated in apical dendrites (Kim and Connors, 1993;Reuveni et al, 1993;Yuste et al, 1994;Schiller et al, 1997;Stuart et al, 1997;Schwindt and Crill, 1999;Larkum et al, 1999) might cause noise to increase gain in some pyramidal neurons. Noisy current injected into the distal apical dendrite of layer 5 pyramidal cells increases gain for 4 stimulus fluctuation to fire, and its gain increases with noise amplitude.…”

Spatial Heterogeneity of Cortical Receptive Fields and Its Impact on Multisensory Interactions

“…on physiological data from excitatory synapses, where g was set to 1 ms and d to 20 ms (Kim and Connors 1993;Mason et al 1991;Sato and Schall 2001;Sayer et al 1990). Baselines for each SDF were calculated as the mean firing rate during the 1,500 ms immediately preceding stimulus onset.…”