Abstract
Firing synchrony among neurons is thought to play functional roles in several brain regions. In theoretical analyses, firing synchrony among neurons within sub-millisecond precision is feasible to convey information. However, little is known about the occurrence and the functional significance of the sub-millisecond synchrony among closely neighboring neurons in the brain of behaving animals because of a technical issue: spikes simultaneously generated from closely neighboring neurons are overlapped in the extracellular space and are not easily separated. As described herein, using a unique spike sorting technique based on independent component analysis together with extracellular 12-channel multi-electrodes (dodecatrodes), we separated such overlapping spikes and investigated the firing synchrony among closely neighboring pyramidal neurons in the hippocampal CA1 of rats during a delayed non-matching to sample task. Results showed that closely neighboring pyramidal neurons in the hippocampal CA1 can co-fire with sub-millisecond precision. The synchrony generally co-occurred with the firing rate modulation in relation to both internal (retention and comparison) and external (stimulus input and motor output) events during the task. However, the synchrony occasionally occurred in relation to stimulus inputs even when rate modulation was clearly absent, suggesting that the synchrony is not simply accompanied with firing rate modulation and that the synchrony and the rate modulation might code similar information independently. We therefore conclude that the sub-millisecond firing synchrony in the hippocampus is an effective carrier for propagating information – as represented by the firing rate modulations – to downstream neurons.
Highlights
In several brain regions, strongly modulated firing rates of neurons can provide accurate information about external stimuli (Hubel and Wiesel, 1977) and behaviors (Georgopoulos et al, 1986), as well as internal cognitive processes (Funahashi et al, 1989)
We identified 63 neurons as pyramidal neurons based on their wide spike shape, low average firing rate, and a sign of bursts
Taken together, our findings demonstrate that robust sub-millisecond synchronized spikes (SSSs) exist between two closely neighboring pyramidal neurons in the hippocampal CA1 of behaving rats
Summary
Strongly modulated firing rates of neurons can provide accurate information about external stimuli (Hubel and Wiesel, 1977) and behaviors (Georgopoulos et al, 1986), as well as internal cognitive processes (Funahashi et al, 1989) These rate changes of neurons in relation to internal or external events have yielded extremely valuable insights into the functioning of the brain. 100 μm) because, when two or more neurons recorded from one electrode co-fire with sub-millisecond precision, the waveforms overlap and are not separated This is designated as ‘the spike overlapping problem’ (Gray et al, 1989; Henze et al, 2000; Takahashi et al, 2003a,b; Buzsaki, 2004; Takahashi and Sakurai, 2005). Our previous studies (Takahashi et al, 2003a,b; Takahashi and Sakurai, 2005, 2007; Sakurai and Takahashi, 2006)
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