Abstract
It is becoming clear that the detection and integration of synaptic input and its conversion into an output signal in cortical neurons are strongly influenced by background synaptic activity or “noise.” The majority of this noise results from the spontaneous release of synaptic transmitters, interacting with ligand-gated ion channels in the postsynaptic neuron [Berretta N, Jones RSG (1996); A comparison of spontaneous synaptic EPSCs in layer V and layer II neurones in the rat entorhinal cortex in vitro. J Neurophysiol 76:1089–1110; Jones RSG, Woodhall GL (2005) Background synaptic activity in rat entorhinal cortical neurons: differential control of transmitter release by presynaptic receptors. J Physiol 562:107–120; LoTurco JJ, Mody I, Kriegstein AR (1990) Differential activation of glutamate receptors by spontaneously released transmitter in slices of neocortex. Neurosci Lett 114:265–271; Otis TS, Staley KJ, Mody I (1991) Perpetual inhibitory activity in mammalian brain slices generated by spontaneous GABA release. Brain Res 545:142–150; Ropert N, Miles R, Korn H (1990) Characteristics of miniature inhibitory postsynaptic currents in CA1 pyramidal neurones of rat hippocampus. J Physiol 428:707–722; Salin PA, Prince DA (1996) Spontaneous GABAA receptor-mediated inhibitory currents in adult rat somatosensory cortex. J Neurophysiol 75:1573–1588; Staley KJ (1999) Quantal GABA release: noise or not? Nat Neurosci 2:494–495; Woodhall GL, Bailey SJ, Thompson SE, Evans DIP, Stacey AE, Jones RSG (2005) Fundamental differences in spontaneous synaptic inhibition between deep and superficial layers of the rat entorhinal cortex. Hippocampus 15:232–245]. The function of synaptic noise has been the subject of debate for some years, but there is increasing evidence that it modifies or controls neuronal excitability and, thus, the integrative properties of cortical neurons. In the present study we have investigated a novel approach [Rudolph M, Piwkowska Z, Badoual M, Bal T, Destexhe A (2004) A method to estimate synaptic conductances from membrane potential fluctuations. J Neurophysiol 91:2884–2896] to simultaneously quantify synaptic inhibitory and excitatory synaptic noise, together with postsynaptic excitability, in rat entorhinal cortical neurons in vitro. The results suggest that this is a viable and useful approach to the study of the function of synaptic noise in cortical networks.
Highlights
Destexhe A (2004) A method to estimate synaptic conductances from membrane potential fluctuations
The analytic expression of mean and standard deviation of membrane potential distribution permits simultaneous estimation of the global background excitation mediated by glutamate acting at AMPA receptors (EBg) and background inhibition (IBg, due to GABA acting via GABAA receptors)
The VmD method is applicable to GABAA- and AMPA-mediated conductances, and does not take into account GABAB- or NMDA receptor–mediated activity
Summary
Cortical neurons are embedded in a dense, complex network and are the target of tens of thousands of individual synapses Both excitatory (glutamate) and inhibitory (GABA) synapses continuously release transmitter as a result of action potentials within network interconnections, and in the form of mono-quantal, activity-independent release (miniature events). We have been studying spontaneous release of both glutamate and GABA onto neurons in the entorhinal cortex (EC) using whole cell patch clamp recording of spontaneous synaptic currents in vitro (see Jones and Woodhall, 2005). This approach does not lend itself well to relating the level of background activity to cellular excitability.
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