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Modulation of Purkinje cell complex spike waveform by synchrony levels in the olivocerebellar system.

Lang EJ, Tang T, Suh CY, Xiao J, Kotsurovskyy Y, Blenkinsop TA, Marshall SP, Sugihara I - Front Syst Neurosci (2014)

Bottom Line: Control experiments showed that changes in variance with synchrony were primarily due to changes in the CS waveform, as opposed to changes in the strength of field potentials from surrounding cells.Direct counts of spikelets showed that their number increased with synchronization of CS activity.In sum, these results provide evidence of a causal link between two of the distinguishing characteristics of the olivocerebellar system, its ability to generate synchronous activity and the waveform of the CS.

View Article: PubMed Central - PubMed

Affiliation: Department of Neuroscience and Physiology, New York University School of Medicine New York, NY, USA.

ABSTRACT
Purkinje cells (PCs) generate complex spikes (CSs) when activated by the olivocerebellar system. Unlike most spikes, the CS waveform is highly variable, with the number, amplitude, and timing of the spikelets that comprise it varying with each occurrence. This variability suggests that CS waveform could be an important control parameter of olivocerebellar activity. The origin of this variation is not well known. Thus, we obtained extracellular recordings of CSs to investigate the possibility that the electrical coupling state of the inferior olive (IO) affects the CS waveform. Using multielectrode recordings from arrays of PCs we showed that the variance in the recording signal during the period when the spikelets occur is correlated with CS synchrony levels in local groups of PCs. The correlation was demonstrated under both ketamine and urethane, indicating that it is robust. Moreover, climbing fiber reflex evoked CSs showed an analogous positive correlation between spikelet-related variance and the number of cells that responded to a stimulus. Intra-IO injections of GABA-A receptor antagonists or the gap junction blocker carbenoxolone produced correlated changes in the variance and synchrony levels, indicating the presence of a causal relationship. Control experiments showed that changes in variance with synchrony were primarily due to changes in the CS waveform, as opposed to changes in the strength of field potentials from surrounding cells. Direct counts of spikelets showed that their number increased with synchronization of CS activity. In sum, these results provide evidence of a causal link between two of the distinguishing characteristics of the olivocerebellar system, its ability to generate synchronous activity and the waveform of the CS.

No MeSH data available.


Related in: MedlinePlus

Comparison of contributions of spikelets and fields from neighboring neurons to the correlation of synchrony and spikelet-related variance. (A1) Segments of an extracellular recording from a PC all aligned to the times of the CSs in other PCs in a group of PCs whose CSs are synchronized. (A2) Example of one trace that was removed from set shown in (A1) because of simple spikes being present just before and during the analysis period (A3) The set of traces selected from those in (A1) in which no CSs or simple spikes were present during the time windows indicated (SS = simple spikes). (B) Plot of variance vs. CS synchrony among PCs in the group. Variance measurements during the 0–10 ms period in the traces with no spikes indicated by black circles. T window variance for the CSs for the PC whose traces were analyzed for fields indicated by red circles. (C) Replotting of regression lines shown in (B) after vertically aligning their left-most points. (D,E) Same as (B,C) respectively, but for a second experiment. Data markers in (B,D) are slightly offset along the x-axis for clarity.
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Figure 8: Comparison of contributions of spikelets and fields from neighboring neurons to the correlation of synchrony and spikelet-related variance. (A1) Segments of an extracellular recording from a PC all aligned to the times of the CSs in other PCs in a group of PCs whose CSs are synchronized. (A2) Example of one trace that was removed from set shown in (A1) because of simple spikes being present just before and during the analysis period (A3) The set of traces selected from those in (A1) in which no CSs or simple spikes were present during the time windows indicated (SS = simple spikes). (B) Plot of variance vs. CS synchrony among PCs in the group. Variance measurements during the 0–10 ms period in the traces with no spikes indicated by black circles. T window variance for the CSs for the PC whose traces were analyzed for fields indicated by red circles. (C) Replotting of regression lines shown in (B) after vertically aligning their left-most points. (D,E) Same as (B,C) respectively, but for a second experiment. Data markers in (B,D) are slightly offset along the x-axis for clarity.

Mentions: We did this in two multielectrode experiments (one group from each experiment, n = 9 PCs/group) using urethane anesthesia. As was described above, the CSs for each cell in the group were classified according to the synchrony level at the time of their occurrence (5-ms window). Then one focal PC (the one with the highest signal-to-noise ratio) was selected for analysis. Next, segments of this PC's recording corresponding to the times of the CSs (from 10 ms prior to 10 ms after the onset) in each of the other cells in the group were made. Thus, for each synchrony level, a set of traces of the focal PC's activity were obtained, all aligned on the CSs of the other PCs (time t = 0 ms in Figure 8A). One such set is shown in Figure 8A1. In most traces the selected PC had spike activity (Figure 8A2), as shown by the denseness of the spikes when the traces are overlapped. To exclude spike-related activity from the selected PC, all traces with simple spikes between t = −5 and 10 ms or CSs between t = −10 and 10 ms were removed (the differing times reflects an attempt to preserve as many traces as possible for analysis while also avoiding contamination of the 0–10 ms period with spike-related activity). The remaining traces were then analyzed for their variance between t = 0 and 10 ms (Figure 8A3). The spikelet-related variance was also measured for the focal PC using a T window in order to compare it with that from the field only traces.


Modulation of Purkinje cell complex spike waveform by synchrony levels in the olivocerebellar system.

Lang EJ, Tang T, Suh CY, Xiao J, Kotsurovskyy Y, Blenkinsop TA, Marshall SP, Sugihara I - Front Syst Neurosci (2014)

Comparison of contributions of spikelets and fields from neighboring neurons to the correlation of synchrony and spikelet-related variance. (A1) Segments of an extracellular recording from a PC all aligned to the times of the CSs in other PCs in a group of PCs whose CSs are synchronized. (A2) Example of one trace that was removed from set shown in (A1) because of simple spikes being present just before and during the analysis period (A3) The set of traces selected from those in (A1) in which no CSs or simple spikes were present during the time windows indicated (SS = simple spikes). (B) Plot of variance vs. CS synchrony among PCs in the group. Variance measurements during the 0–10 ms period in the traces with no spikes indicated by black circles. T window variance for the CSs for the PC whose traces were analyzed for fields indicated by red circles. (C) Replotting of regression lines shown in (B) after vertically aligning their left-most points. (D,E) Same as (B,C) respectively, but for a second experiment. Data markers in (B,D) are slightly offset along the x-axis for clarity.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4214199&req=5

Figure 8: Comparison of contributions of spikelets and fields from neighboring neurons to the correlation of synchrony and spikelet-related variance. (A1) Segments of an extracellular recording from a PC all aligned to the times of the CSs in other PCs in a group of PCs whose CSs are synchronized. (A2) Example of one trace that was removed from set shown in (A1) because of simple spikes being present just before and during the analysis period (A3) The set of traces selected from those in (A1) in which no CSs or simple spikes were present during the time windows indicated (SS = simple spikes). (B) Plot of variance vs. CS synchrony among PCs in the group. Variance measurements during the 0–10 ms period in the traces with no spikes indicated by black circles. T window variance for the CSs for the PC whose traces were analyzed for fields indicated by red circles. (C) Replotting of regression lines shown in (B) after vertically aligning their left-most points. (D,E) Same as (B,C) respectively, but for a second experiment. Data markers in (B,D) are slightly offset along the x-axis for clarity.
Mentions: We did this in two multielectrode experiments (one group from each experiment, n = 9 PCs/group) using urethane anesthesia. As was described above, the CSs for each cell in the group were classified according to the synchrony level at the time of their occurrence (5-ms window). Then one focal PC (the one with the highest signal-to-noise ratio) was selected for analysis. Next, segments of this PC's recording corresponding to the times of the CSs (from 10 ms prior to 10 ms after the onset) in each of the other cells in the group were made. Thus, for each synchrony level, a set of traces of the focal PC's activity were obtained, all aligned on the CSs of the other PCs (time t = 0 ms in Figure 8A). One such set is shown in Figure 8A1. In most traces the selected PC had spike activity (Figure 8A2), as shown by the denseness of the spikes when the traces are overlapped. To exclude spike-related activity from the selected PC, all traces with simple spikes between t = −5 and 10 ms or CSs between t = −10 and 10 ms were removed (the differing times reflects an attempt to preserve as many traces as possible for analysis while also avoiding contamination of the 0–10 ms period with spike-related activity). The remaining traces were then analyzed for their variance between t = 0 and 10 ms (Figure 8A3). The spikelet-related variance was also measured for the focal PC using a T window in order to compare it with that from the field only traces.

Bottom Line: Control experiments showed that changes in variance with synchrony were primarily due to changes in the CS waveform, as opposed to changes in the strength of field potentials from surrounding cells.Direct counts of spikelets showed that their number increased with synchronization of CS activity.In sum, these results provide evidence of a causal link between two of the distinguishing characteristics of the olivocerebellar system, its ability to generate synchronous activity and the waveform of the CS.

View Article: PubMed Central - PubMed

Affiliation: Department of Neuroscience and Physiology, New York University School of Medicine New York, NY, USA.

ABSTRACT
Purkinje cells (PCs) generate complex spikes (CSs) when activated by the olivocerebellar system. Unlike most spikes, the CS waveform is highly variable, with the number, amplitude, and timing of the spikelets that comprise it varying with each occurrence. This variability suggests that CS waveform could be an important control parameter of olivocerebellar activity. The origin of this variation is not well known. Thus, we obtained extracellular recordings of CSs to investigate the possibility that the electrical coupling state of the inferior olive (IO) affects the CS waveform. Using multielectrode recordings from arrays of PCs we showed that the variance in the recording signal during the period when the spikelets occur is correlated with CS synchrony levels in local groups of PCs. The correlation was demonstrated under both ketamine and urethane, indicating that it is robust. Moreover, climbing fiber reflex evoked CSs showed an analogous positive correlation between spikelet-related variance and the number of cells that responded to a stimulus. Intra-IO injections of GABA-A receptor antagonists or the gap junction blocker carbenoxolone produced correlated changes in the variance and synchrony levels, indicating the presence of a causal relationship. Control experiments showed that changes in variance with synchrony were primarily due to changes in the CS waveform, as opposed to changes in the strength of field potentials from surrounding cells. Direct counts of spikelets showed that their number increased with synchronization of CS activity. In sum, these results provide evidence of a causal link between two of the distinguishing characteristics of the olivocerebellar system, its ability to generate synchronous activity and the waveform of the CS.

No MeSH data available.


Related in: MedlinePlus