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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.


Related in: MedlinePlus

Rate modulations related to stimulus inputs are not associated with SSSs. Comparison of SSSs and rate modulations between high tone (red) and low tone (blue) trials was selected in this example. Results of U-tests of 5 s of tone presentation in the preceding trial, 5 s of delay, and 2 s of tone presentation in the next trial are shown. (A) Firing rates of neuron 13 in high tone (red) and low tone (blue) trials. (B,C) Raster plots of spikes of neuron 13 in high tone (red) and low tone (blue) trials. (D) P-values of neuron 13 for a difference between rates on high tone trials and on low tone trials. (E) Firing rates of neuron 14. (F,G) Raster plots of neuron 14. (H) P-values of neuron 14. (I) Rates of the SSS between neurons 13 and 14. (J–M) In copies of raster plots from (B), (C), (F), and (G) (black dots), SSSs are shown as green dots. (N) P-values of the SSS between neurons 13 and 14. Significant firing rate modulations of neurons 13 and 14 were not associated with SSSs. Additional details are presented in Figure 5 and described in Section ‘Materials and Methods’.
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Figure 11: Rate modulations related to stimulus inputs are not associated with SSSs. Comparison of SSSs and rate modulations between high tone (red) and low tone (blue) trials was selected in this example. Results of U-tests of 5 s of tone presentation in the preceding trial, 5 s of delay, and 2 s of tone presentation in the next trial are shown. (A) Firing rates of neuron 13 in high tone (red) and low tone (blue) trials. (B,C) Raster plots of spikes of neuron 13 in high tone (red) and low tone (blue) trials. (D) P-values of neuron 13 for a difference between rates on high tone trials and on low tone trials. (E) Firing rates of neuron 14. (F,G) Raster plots of neuron 14. (H) P-values of neuron 14. (I) Rates of the SSS between neurons 13 and 14. (J–M) In copies of raster plots from (B), (C), (F), and (G) (black dots), SSSs are shown as green dots. (N) P-values of the SSS between neurons 13 and 14. Significant firing rate modulations of neurons 13 and 14 were not associated with SSSs. Additional details are presented in Figure 5 and described in Section ‘Materials and Methods’.

Mentions: Even if SSSs play an important role in biological and computational processes, the rate modulation of individual neurons can play other roles; SSSs and rate modulations might contain independent information (Riehle et al., 1997). We tested this hypothesis for all detected groups. Results showed that SSSs were observed with or without modulations of the firing rates of participating neurons. A summary of the analysis is shown in Figure 9. Figures 5–8 show that SSS occurred at the probability of 79% if at least one participating neuron show significant firing rate modulations in relation to both internal (retention and comparison) and external (stimulus input and motor output) events. This consistent relation among SSS, rate modulation, and behavioral events implies the functional significance of both SSS and rate modulation. Of six groups related to stimulus inputs, half (3/6) showed that SSS was not associated with modulations of the firing rates of participating neurons, as portrayed in Figure 10. In each behavioral event, at least one group showed that SSSs were not related to behavioral events, even when the firing rate of participating neurons was modulated, as presented in Figure 11. Moreover, the analysis used to identify the statistical significance of the SSS incorporates the expected rate of coincidence caused by the firing rate modulation of participating neurons. Therefore, we conclude that SSSs are not simply a consequence of the rate modulations of participating neurons.


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)

Rate modulations related to stimulus inputs are not associated with SSSs. Comparison of SSSs and rate modulations between high tone (red) and low tone (blue) trials was selected in this example. Results of U-tests of 5 s of tone presentation in the preceding trial, 5 s of delay, and 2 s of tone presentation in the next trial are shown. (A) Firing rates of neuron 13 in high tone (red) and low tone (blue) trials. (B,C) Raster plots of spikes of neuron 13 in high tone (red) and low tone (blue) trials. (D) P-values of neuron 13 for a difference between rates on high tone trials and on low tone trials. (E) Firing rates of neuron 14. (F,G) Raster plots of neuron 14. (H) P-values of neuron 14. (I) Rates of the SSS between neurons 13 and 14. (J–M) In copies of raster plots from (B), (C), (F), and (G) (black dots), SSSs are shown as green dots. (N) P-values of the SSS between neurons 13 and 14. Significant firing rate modulations of neurons 13 and 14 were not associated with SSSs. Additional details are presented in Figure 5 and described in Section ‘Materials and Methods’.
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Related In: Results  -  Collection

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Figure 11: Rate modulations related to stimulus inputs are not associated with SSSs. Comparison of SSSs and rate modulations between high tone (red) and low tone (blue) trials was selected in this example. Results of U-tests of 5 s of tone presentation in the preceding trial, 5 s of delay, and 2 s of tone presentation in the next trial are shown. (A) Firing rates of neuron 13 in high tone (red) and low tone (blue) trials. (B,C) Raster plots of spikes of neuron 13 in high tone (red) and low tone (blue) trials. (D) P-values of neuron 13 for a difference between rates on high tone trials and on low tone trials. (E) Firing rates of neuron 14. (F,G) Raster plots of neuron 14. (H) P-values of neuron 14. (I) Rates of the SSS between neurons 13 and 14. (J–M) In copies of raster plots from (B), (C), (F), and (G) (black dots), SSSs are shown as green dots. (N) P-values of the SSS between neurons 13 and 14. Significant firing rate modulations of neurons 13 and 14 were not associated with SSSs. Additional details are presented in Figure 5 and described in Section ‘Materials and Methods’.
Mentions: Even if SSSs play an important role in biological and computational processes, the rate modulation of individual neurons can play other roles; SSSs and rate modulations might contain independent information (Riehle et al., 1997). We tested this hypothesis for all detected groups. Results showed that SSSs were observed with or without modulations of the firing rates of participating neurons. A summary of the analysis is shown in Figure 9. Figures 5–8 show that SSS occurred at the probability of 79% if at least one participating neuron show significant firing rate modulations in relation to both internal (retention and comparison) and external (stimulus input and motor output) events. This consistent relation among SSS, rate modulation, and behavioral events implies the functional significance of both SSS and rate modulation. Of six groups related to stimulus inputs, half (3/6) showed that SSS was not associated with modulations of the firing rates of participating neurons, as portrayed in Figure 10. In each behavioral event, at least one group showed that SSSs were not related to behavioral events, even when the firing rate of participating neurons was modulated, as presented in Figure 11. Moreover, the analysis used to identify the statistical significance of the SSS incorporates the expected rate of coincidence caused by the firing rate modulation of participating neurons. Therefore, we conclude that SSSs are not simply a consequence of the rate modulations of participating neurons.

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.


Related in: MedlinePlus