Abstract
Hippocampal neurons are known to fire as a function of frequency and phase of spontaneous network rhythms, associated with the animal's behaviour. This dependence is believed to give rise to precise rate and temporal codes. However, it is not well understood how these periodic membrane potential fluctuations affect the integration of synaptic inputs. Here we used sinusoidal current injection to the soma of CA1 pyramidal neurons in the rat brain slice to simulate background oscillations in the physiologically relevant theta and gamma frequency range. We used a detailed compartmental model to show that somatic current injection gave comparable results to more physiological synaptically driven theta rhythms incorporating excitatory input in the dendrites, and inhibitory input near the soma. We systematically varied the phase of synaptic inputs with respect to this background, and recorded changes in response and summation properties of CA1 neurons using whole-cell patch recordings. The response of the cell was dependent on both the phase of synaptic inputs and frequency of the background input. The probability of the cell spiking for a given synaptic input was up to 40% greater during the depolarized phases between 30–135 degrees of theta frequency current injection. Summation gain on the other hand, was not affected either by the background frequency or the phasic afferent inputs. This flat summation gain, coupled with the enhanced spiking probability during depolarized phases of the theta cycle, resulted in enhanced transmission of summed inputs during the same phase window of 30–135 degrees. Overall, our study suggests that although oscillations provide windows of opportunity to selectively boost transmission and EPSP size, summation of synaptic inputs remains unaffected during membrane oscillations.
Highlights
Oscillations in the brain have been suggested to provide single neurons with a temporal reference to network activity
We investigated the role played by rhythmic hippocampal activity represented by sinusoidal current injection, in tuning responses and summation properties of hippocampal neurons to synaptic inputs
The sinusoidal current injection at 4 Hz, 40 Hz and 100 Hz were designed to simulate the fluctuations in membrane voltage during theta and gamma spontaneous network activity typically seen in CA1 neurons in vivo [28,29,30]
Summary
Oscillations in the brain have been suggested to provide single neurons with a temporal reference to network activity. Hippocampal rhythms are typically in the theta (4–12 Hz) and gamma (30–100 Hz) frequencies. Both theta and gamma oscillations have been shown to be emergent properties intrinsic to the hippocampal network [7,8,9]. Lower frequency network oscillations are used for high level temporal interactions with distant regions whereas higher frequency gamma rhythms are implicated in more local computations [17,18]. These rhythms are not exclusive, and gamma activity is frequently nested within theta waves [19,20,21]
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