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Sub-Millisecond Firing Synchrony of Closely Neighboring Pyramidal Neurons in Hippocampal CA1 of Rats During Delayed Non-Matching to Sample Task.

Takahashi S, Sakurai Y - Front Neural Circuits (2009)

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Khoyama Center for Neuroscience, Faculty of Computer Science and Engineering, Kyoto Sangyo University Kyoto, Japan.

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.

No MeSH data available.


Sub-millisecond synchronizations among closely neighboring neurons. (A) Spike rasters of four pyramidal neurons recorded from one dodecatrode for a 1-s data segment. Possible coincidences within a 1-ms range are color-coded (Black, no coincident spike; Red, pairwise coincident spike; Green, triplet coincident spike; Blue, quadruplet coincident spike). (B) Cross-correlograms between pyramidal neurons, showing sharp peaks at around zero delay. The bin size is 50 μs.
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Figure 3: Sub-millisecond synchronizations among closely neighboring neurons. (A) Spike rasters of four pyramidal neurons recorded from one dodecatrode for a 1-s data segment. Possible coincidences within a 1-ms range are color-coded (Black, no coincident spike; Red, pairwise coincident spike; Green, triplet coincident spike; Blue, quadruplet coincident spike). (B) Cross-correlograms between pyramidal neurons, showing sharp peaks at around zero delay. The bin size is 50 μs.

Mentions: In fact, ICSort was important for this study because conventional spike sorting cannot detect sub-millisecond synchronization of spikes of different neurons on one electrode because of the overlapped spike waveform (Gray et al., 1995; Buzsaki, 2004). The spike overlaps occurred when two or more neighboring single-neurons co-fire with sub-millisecond precision. Figures 1A,B present typical examples of dodecatrode recordings in the start and end periods of the task. The overall distribution of spike amplitudes across channels does not change during the task. Figure 1C shows that spike waveforms of neurons 1 and 2, which are reconstructed from each IC estimated using ICSort, are similar and that the distribution of spike amplitudes across 12 channels is constant. Noise components were identified and eliminated during thresholding in ICSort. To determine whether spikes from different neurons are intermingled (Type I error; false positive), we calculated auto-correlograms of all single neurons sorted in this study. Each auto-correlogram shows clear refractory periods (1–2 ms; Figure 1D). To determine whether spikes from a single neuron are sorted to different neurons (Type II error; false negative), we calculated cross-correlograms of all pairs of single neurons sorted in this study. No cross-correlogram shows a refractory period (Figures 1D and 3B). Figure 1E presents typical examples of overlapped (black) and separated waveforms (green and red) from two neurons co-firing with long (0.40 ms, left, see the gap separating red and green dashed vertical lines) and short (0.15 ms, right, see the gap separating red and green dashed vertical lines) jitters of delay. Red and green dashed vertical lines respectively depict the detected spike timing of neurons 1 and 2. In our entire dataset (n = 36 units), the correlation coefficients R between averaged waveforms of identical neurons detected from overlapping and non-overlapping spikes are >0.86. (neuron 1, R = 0.99; neuron 2, R = 0.98 in Figures 1C,E).


Sub-Millisecond Firing Synchrony of Closely Neighboring Pyramidal Neurons in Hippocampal CA1 of Rats During Delayed Non-Matching to Sample Task.

Takahashi S, Sakurai Y - Front Neural Circuits (2009)

Sub-millisecond synchronizations among closely neighboring neurons. (A) Spike rasters of four pyramidal neurons recorded from one dodecatrode for a 1-s data segment. Possible coincidences within a 1-ms range are color-coded (Black, no coincident spike; Red, pairwise coincident spike; Green, triplet coincident spike; Blue, quadruplet coincident spike). (B) Cross-correlograms between pyramidal neurons, showing sharp peaks at around zero delay. The bin size is 50 μs.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2742662&req=5

Figure 3: Sub-millisecond synchronizations among closely neighboring neurons. (A) Spike rasters of four pyramidal neurons recorded from one dodecatrode for a 1-s data segment. Possible coincidences within a 1-ms range are color-coded (Black, no coincident spike; Red, pairwise coincident spike; Green, triplet coincident spike; Blue, quadruplet coincident spike). (B) Cross-correlograms between pyramidal neurons, showing sharp peaks at around zero delay. The bin size is 50 μs.
Mentions: In fact, ICSort was important for this study because conventional spike sorting cannot detect sub-millisecond synchronization of spikes of different neurons on one electrode because of the overlapped spike waveform (Gray et al., 1995; Buzsaki, 2004). The spike overlaps occurred when two or more neighboring single-neurons co-fire with sub-millisecond precision. Figures 1A,B present typical examples of dodecatrode recordings in the start and end periods of the task. The overall distribution of spike amplitudes across channels does not change during the task. Figure 1C shows that spike waveforms of neurons 1 and 2, which are reconstructed from each IC estimated using ICSort, are similar and that the distribution of spike amplitudes across 12 channels is constant. Noise components were identified and eliminated during thresholding in ICSort. To determine whether spikes from different neurons are intermingled (Type I error; false positive), we calculated auto-correlograms of all single neurons sorted in this study. Each auto-correlogram shows clear refractory periods (1–2 ms; Figure 1D). To determine whether spikes from a single neuron are sorted to different neurons (Type II error; false negative), we calculated cross-correlograms of all pairs of single neurons sorted in this study. No cross-correlogram shows a refractory period (Figures 1D and 3B). Figure 1E presents typical examples of overlapped (black) and separated waveforms (green and red) from two neurons co-firing with long (0.40 ms, left, see the gap separating red and green dashed vertical lines) and short (0.15 ms, right, see the gap separating red and green dashed vertical lines) jitters of delay. Red and green dashed vertical lines respectively depict the detected spike timing of neurons 1 and 2. In our entire dataset (n = 36 units), the correlation coefficients R between averaged waveforms of identical neurons detected from overlapping and non-overlapping spikes are >0.86. (neuron 1, R = 0.99; neuron 2, R = 0.98 in Figures 1C,E).

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Khoyama Center for Neuroscience, Faculty of Computer Science and Engineering, Kyoto Sangyo University Kyoto, Japan.

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.

No MeSH data available.