Burst generation in rat pyramidal neurones by regenerative potentials elicited in a restricted part of the basilar dendritic tree

Abstract

The common preconception about central nervous system neurones is that thousands of small postsynaptic potentials sum across the entire dendritic tree to generate substantial firing rates, previously observed in in vivo experiments. We present evidence that local inputs confined to a single basal dendrite can profoundly influence the neuronal output of layer V pyramidal neurones in the rat prefrontal cortical slices. In our experiments, brief glutamatergic stimulation delivered in a restricted part of the basilar dendritic tree invariably produced sustained plateau depolarizations of the cell body, accompanied by bursts of action potentials. Because of their small diameters, basolateral dendrites are not routinely accessible for glass electrode measurements, and very little is known about their electrical properties and their role in information processing. Voltage-sensitive dye recordings were used to follow membrane potential transients in distal segments of basal branches during sub-and suprathreshold glutamate and synaptic stimulations. Recordings were obtained simultaneously from multiple dendrites and multiple points along individual dendrites, thus showing in a direct way how regenerative potentials initiate at the postsynaptic site and propagate decrementally toward the cell body. The glutamate-evoked dendritic plateau depolarizations described here are likely to occur in conjunction with strong excitatory drive during so-called 'UP states', previously observed in in vivo recordings from mammalian cortices. Several lines of evidence suggest that basal dendrites play a very important role in cortical information processing. Studies that combine physiological and histological techniques have shown that connections between layer V large pyramidal cells are mediated by synaptic junctions placed mainly on the basal dendrites (Deuchars et al. 1994;Markram et al. 1997). Local excitatory contacts are essential in a process known as 'recurrent excitation' , which is thought to be the cellular substrate of persistent neuronal activity (Goldman-Rakic, 1995;Compte et al. 2000;Goldman et al. 2003). Basal and proximal oblique dendrites are ideally suited to participate in recurrent excitation in that they comprise approximately twothirds of the total membrane area of a neurone. Based on dendritic spine counts, it has been estimated that This paper is dedicated to the memory of Patricia Goldman-Rakic, our dear friend and colleague.within the boundaries of layer V, basal and oblique branches receive approximately 65% of the total number of excitatory synaptic contacts (Larkman, 1991). Interestingly, Lucifer yellow injections showed that those cortical pyramidal neurones, which exhibit UP and DOWN states in vivo, have noticeably rich basal dendritic arbors (Steriade et al. 1993a). In vitro models of cortical rhythmic recurrent activity unequivocally showed that synaptic inputs arriving on basal and proximal oblique dendrites within the boundaries of layers V and VI are the major source of excitatory drive during the UP s...

Initiation of Sodium Spikelets in Basal Dendrites of Neocortical Pyramidal Neurons

“…Intracellular voltage-sensitive dyes cannot be used to determine the absolute amplitude (in mV) of the electrical transients in distal dendritic segments (Antic, Major & Zecevic, 1999). However, voltage-sensitive dyes can be used to detect a relative amplitude change between signals obtained from the same dendritic segment in consecutive recording trials (Milojkovic et al, 2004). Since the concentration and partition of the voltage-sensitive dye in a given dendritic segment is unlikely to change significantly within a 2-3 min period, the sensitivity of voltage-sensitive dye measurements obtained from the same dendritic segment remains constant between successive recordings.…”

“…Quite the opposite is true for glutamate-evoked dendritic plateau potentials. Dendritic plateau potentials, which originate in the same section of the basal dendrite as fast spikes, provide a very reliable drive for bursts of action potentials (Milojkovic et al, 2004). The second piece of evidence against basal spikes acting as precise temporal encoders consists of in vivo recordings of fast prepotentials.…”

“…5B,ROI 1). Both the fast spikelet and the plateau potential propagate centripetally towards the cell body, in a decremental fashion (Milojkovic et al, 2004). The low-pass filtering of the dendrite-soma junction severely reduces the amplitude of the fast spikelet, and the spikelet fails to invade the soma (to trigger an action potential, Fig.…”

“…The dendritic plateau potentials were shown to play the critical role in the in vitro model of the cortical pyramidal neuron UP state (Milojkovic et al, 2004;.…”

Imaging membrane potential in dendrites and axons of single neurons

“…By directly comparing the amplitude of excitatory postsynaptic potentials (EPSPs) with the back-propagating action potential at different dendritic locations, it was concluded that EPSPs undergo only slight attenuation as they propagate from their site of origin in the glomerular tuft to the soma. Internal application of voltage-sensitive dyes has also been used to study regenerative plateau potentials [38,39] and local dendritic sodium spikes [40] in basal dendrites in cortical pyramidal neurons. A recent study also used internally Fig.…”