The unimodal distribution of sub-threshold, ongoing activity in cortical networks.

The characterization of the subthreshold, ongoing activity in cortical neurons has been the focus of numerous studies. This activity, described as spontaneous slow waves in membrane potential, has been observed in a span of species in diverse cortical and subcortical areas. We here characterized membrane potential fluctuations in motor and the frontal association cortices cortical neurons of ketamine-xylazine anesthetized rats. We recorded from 95 neurons from a range of cortical depths to unravel the network and cellular mechanisms that shape the subthreshold ongoing spontaneous activity of these neurons. We define a unitary event that generates the subthreshold ongoing activity: giant synaptic potentials (GSPs). These events have a duration of 87 ± 50 ms and an amplitude of 19 ± 6.4 mV. They occur at a frequency of 3.7 ± 0.8 Hz and involve an increase in conductance change of 22 ± 21%. GSPs are mainly due to excitatory activity that occurs throughout all cortical layers, unaffected by the intrinsic properties of the cells. Indeed, blocking the GABAA receptors, a procedure that had a profound effect on cortical activity, did not alter these unitary events. We propose that this unitary event is composed of individual, excitatory synaptic potentials that appear at different levels of synchrony and that the level of synchrony determines the shape of the subthreshold activity.

A paradoxical isopotentiality: a spatially uniform noise spectrum in neocortical pyramidal cells.

Membrane ion channels and synapses are among the most important computational elements of nerve cells. Both have stochastic components that are reflected in random fluctuations of the membrane potential. We measured the spectral characteristics of membrane voltage noise in vitro at the soma and the apical dendrite of layer 4/5 (L4/5) neocortical neurons of rats near the resting potential. We found a remarkable similarity between the voltage noise power spectra at the soma and the dendrites, despite a marked difference in their respective input impedances. At both sites, the noise levels and the input impedance are voltage dependent; in the soma, the noise level increased from sigma = 0.33 +/- 0.28 mV at 10 mV hyperpolarization from the resting potential to sigma = 0.59 +/- 0.3 at a depolarization of 10 mV. At the dendrite, the noise increased from sigma = 0.34 +/- 0.28 to sigma = 0.56 +/- 0.30 mV, respectively. TTX reduced both the input impedance and the voltage noise, and eliminated their voltage dependence at both locations. We describe a detailed compartmental model of a L4/5 neuron with simplified electrical properties that successfully reproduces the difference in input impedance between dendrites and soma and demonstrates that spatially uniform conductance-base noise sources leads to an apparent isopotential structure which exhibits a uniform power spectra of voltage noise at all locations. We speculate that a homogeneous distribution of noise sources insures that variability in synaptic amplitude as well as timing of action potentials is location invariant.

Subthreshold voltage noise of rat neocortical pyramidal neurones.

Neurones are noisy elements. Noise arises from both intrinsic and extrinsic sources, and manifests itself as fluctuations in the membrane potential. These fluctuations limit the accuracy of a neurone's output but have also been suggested to play a computational role. We present a detailed study of the amplitude and spectrum of voltage noise recorded at the soma of layer IV-V pyramidal neurones in slices taken from rat neocortex. The dependence of the noise on holding potential, synaptic activity and Na+ conductance is systematically analysed. We demonstrate that voltage noise increases non-linearly as the cell depolarizes (from a standard deviation (s.d.) of 0.19 mV at -75 mV to an s.d. of 0.54 mV at -55 mV). The increase in voltage noise is accompanied by an increase in the cell impedance, due to voltage dependence of Na+ conductance. The impedance increase accounts for the majority (70%) of the voltage noise increase. The increase in voltage noise and impedance is restricted to the low-frequency range (0.2-2 Hz). At the high frequency range (5-100 Hz) the voltage noise is dominated by synaptic activity. In our slice preparation, synaptic noise has little effect on the cell impedance. A minimal model reproduces qualitatively these data. Our results imply that ion channel noise contributes significantly to membrane voltage fluctuations at the subthreshold voltage range, and that Na+ conductance plays a key role in determining the amplitude of this noise by acting as a voltage-dependent amplifier of low-frequency transients.