Rapid ReportA possible role of ectopic action potentials in the in vitro hippocampal sharp wave–ripple complexes
Section snippets
Slice preparation
Hippocampal slices were prepared from 17 young adult (4–6 weeks old) male Wistar rats. All measures were taken to minimize animal suffering and to reduce the number of the animals used, according to the European Communities Council Directive Guidelines (86/609/EEC) for the care and use of laboratory animals. Furthermore, animal treatment was approved by the local ethics committee. Animals were deeply anesthetized with diethyl-ether, were decapitated and the brains were removed and placed in
Results
Intracellular recordings from 35 neurons and simultaneous extracellular recordings were made from the stratum pyramidale of the CA1b field. All recorded cells were situated at least 150 μm deep from the surface of the slices and were putative principal neurons as concluded on the basis of their accommodating firing mode in response to depolarizing DC current injection (300–500 ms, 0.1–0.5 nA), their resting membrane potential (−62.35±0.98 mV) and input resistance (54.5±4.2 MΩ). In line with
Discussion
The present findings show that two relatively distinct populations of CA1 pyramidal cells fire at different temporal windows with respect to SPW-R activity. Furthermore, firing in the two populations is apparently triggered by distinct mechanisms. In one subset of pyramidal cells depolarization-induced o-APs most frequently occur before the onset of SPW-Rs while the cells in a second group fire maximally during the peaking phase of the ripple oscillation coinciding with the hyperpolarization of
Acknowledgments
This study was supported by a “Karatheodori” grant (# C 176) of the Research Committee of the University of Patras. The author thanks Dr. G. Kostopoulos as well as Dr. P. Giannopoulos, E. Koniaris and D. Kotzadimitriou for valuable discussions.
References (46)
- et al.
The effects of cooling and rewarming on the neuronal activity of pyramidal neurons in guinea pig hippocampal slices
Brain Res
(2001) Hippocampal sharp waves: their origin and significance
Brain Res
(1986)- et al.
Spontaneous GABA(A)-dependent synchronous periodic activity in adult rat ventral hippocampal slices
Neurosci Lett
(2002) Antidromic firing occurs spontaneously on thalamic relay neurons: triggering of ectopic action potentials by somatic intrinsic burst discharges
Neuroscience
(1990)Backpropagation of action potentials generated at ectopic axonal loci: hypothesis that axon terminals integrate local environmental signals
Brain Res Brain Res Rev
(1995)- et al.
Antidromic firing occurs spontaneously on thalamic relay neurons: triggering of somatic intrinsic burst discharges by ectopic action potentials
Neuroscience
(1989) - et al.
A new type of specific interneuron in the monkey hippocampus forming synapses exclusively with the axon initial segments of pyramidal cells
Brain Res
(1983) - et al.
Action potential initiation and backpropagation in neurons of the mammalian CNS
Trends Neurosci
(1997) - et al.
Memory trace reactivation in hippocampal and neocortical neuronal ensembles
Curr Opin Neurobiol
(2000) - et al.
Spontaneous EEG spikes in the normal hippocampusI. Behavioral correlates, laminar profiles and bilateral synchrony
Electroencephalogr Clin Neurophysiol
(1987)
Contribution of nitric oxide to the depression of neuronal activity induced by temperature increase in the rat hippocampal CA1 area
Neurosci Lett
Hippocampal electrical activity and voluntary movement in the rat
Electroencephalogr Clin Neurophysiol
GABA-dependent generation of ectopic action potentials in the rat hippocampus
Eur J Neurosci
Physiological properties of anatomically identified axo-axonic cells in the rat hippocampus
J Neurophysiol
The hippocampo-neocortical dialogue
Cereb Cortex
High-frequency network oscillation in the hippocampus
Science
Selective activation of deep layer (V-VI) retrohippocampal cortical neurons during hippocampal sharp waves in the behaving rat
J Neurosci
High-frequency oscillations in the output networks of the hippocampal-entorhinal axis of the freely behaving rat
J Neurosci
Gamma and ripple oscillations: functional indices of hippocampal-entorhinal interactions
Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons
Nature
Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat
J Neurosci
Thalamocortical relay neurons: antidromic invasion of spikes from a cortical epileptogenic focus
Science
Electrophysiology of hippocampal neuronsI. Sequential invasion and synaptic organization
J Neurophysiol
Cited by (32)
Gap Junctions Between Pyramidal Cells Account for a Variety of Very Fast Network Oscillations (>80 Hz) in Cortical Structures
2017, Network Functions and Plasticity: Perspectives from Studying Neuronal Electrical Coupling in MicrocircuitsBDNF mRNA abundance regulated by antidromic action potentials and AP-LTD in hippocampus
2016, Neuroscience LettersThe axon as a unique computational unit in neurons
2013, Neuroscience ResearchCitation Excerpt :These peculiar APs are distinguishable at the soma by their stereotypical kinetics; the voltage trajectory of ectopic APs increases sharply from the resting potential in the absence of depolarization prior to the AP. The existence of ectopic APs was initially confirmed under pathological circumstances (Pinault, 1995), but more recently, several studies have demonstrated that ectopic APs can occur during active states even in normal cortical networks (Papatheodoropoulos, 2008; Bahner et al., 2011; Sheffield et al., 2011). In a subset of hippocampal and neocortical interneurons, repetitive spikes at the soma are integrated at the distal axonal region and eventually trigger persistent autonomous firing originating from the axonal segment (Sheffield et al., 2011).
Cannabinoid receptor activation disrupts the internal structure of hippocampal sharp wave-ripple complexes
2012, Journal of Pharmacological Sciencesα5GABA<inf>A</inf> receptors regulate hippocampal sharp wave-ripple activity in vitro
2011, NeuropharmacologyCitation Excerpt :The abrupt suppressive effect of etomidate on the likelihood of SWRs’ initiation (episodes/min) between 1 and 5 μM may involve an additional increase in the decay time of the phasic GABAAR-mediated events (Dai et al., 2009; Proctor et al., 1986). This is corroborated by the prominent prolongation of the slow component of SWR events by 5 μM etomidate taking into account that this component reflects GABAAR-mediated hyperpolarization in CA1 pyramidal cells (Papatheodoropoulos, 2008, 2010). A proposed mechanism for the generation of secondary SWRs in clusters includes post-inhibitory rebound depolarization (Papatheodoropoulos, 2010).