Cell and circuit origins of fast network oscillations in the mammalian main olfactory bulb
- Department of Neurobiology, University of Pittsburgh, United States
- Center for the Neural Basis of Cognition, United States
Figures
Figure 1 with 4 supplements
Multiglomerular activation evokes widespread synchronization of tufted cell (TC) firing across fast- and slow-gamma frequencies and limited synchronization of mitral cell (MC) firing across slow-gamma frequencies.
(A) Example cell-attached recording of a heterotypic MC pair during photostimulation. Morphology (upper) and representative trial (lower; blue rectangles: 10 ms light pulses of the 5 Hz …
Figure 1—figure supplement 1
Multiglomerular activation evokes higher firing rates and more phasic firing patterns among tufted cells (TCs) than mitral cells (MCs).
(A) Raster plots of spike times recorded during photostimulation across all trials in the MCs in Figure 1A (‘expt.’), as well as across 500 trials of spike times simulated from rate-matched …
Figure 1—figure supplement 2
Mitral cell (MC) pairs and tufted cell (TC) pairs exhibit greater gamma-frequency spike-time synchrony than spike times simulated from rate-matched independent Poisson processes.
(A) Trial-averaged experimental spike-time cross-power spectral density (CPSD) spectrogram from the MC pair in Figure 1A following photostimulation onset at 0.0 s (upper), and equivalent …
Figure 1—figure supplement 3
Tufted cells (TCs) exhibit greater gamma-frequency spike-time synchrony than mitral cells (MCs) on both a per-pair basis and independent of ridge-based analyses.
(A) Distribution of ridge cross-power spectral density (CPSD) vs. frequency for the 5/16 MC pairs and 24/26 TC pairs exhibiting spike-time CPSD ridges. Ellipses denote mean ± standard deviation of …
Figure 1—figure supplement 4
Fast-gamma-frequency spike-time synchrony emerges early in each 5 Hz photostimulation cycle and decelerates toward slow-gamma frequencies.
(A) Mean spike-time cross-power spectral density (CPSD) ridge frequency across all pairs following photostimulation onset at 0.0 s. (B) Mean derivative of spike-time CPSD ridge frequency across all …
Figure 2 with 1 supplement
Greater synchronization of tufted cell (TC) than mitral cell (MC) firing persists throughout the average 5 Hz photostimulation cycle.
(A) Experimental spike times recorded across MC pairs (‘expt.’) within consecutive 50 ms windows of the 5 Hz photostimulation cycle exhibited consistently higher cross-correlogram peaks (within |Δtsp…
Figure 2—figure supplement 1
Full-field photostimulation evokes comparable excitatory currents in tufted cells (TCs) and mitral cells (MCs).
(A) Trial-averaged excitatory currents recorded in TCs and MCs during photostimulation. Blue rectangles: 10 ms light pulses of the 5 Hz photostimulation protocol. (B) TCs and MCs exhibited …
Figure 3 with 2 supplements
Greater synchronization of tufted cell (TC) than mitral cell (MC) firing extends across distinct patterns of glomerular organization and is not driven by intraglomerular lateral excitation.
(A) MCs and TCs included comparable proportions of homotypic and heterotypic pairs (chi-squared test: p=0.26, χ2 = 1.3). (B) Spike-time cross-power spectral density (CPSD) spectrograms averaged …
Figure 3—figure supplement 1
Profound cell-type differences in spike-time synchrony cannot be explained by differences in within-pair intersomatic distance.
(A, B) Mitral cells (MCs) and tufted cells (TCs) exhibited comparable within-pair total intersomatic distance (A) (Wilcoxon rank-sum test: p=0.51), while TCs exhibited shorter within-pair lateral …
Figure 3—figure supplement 2
Tufted cell (TC) spike-time synchrony does not correlate with within-pair intersomatic differences in external plexiform layer (EPL) depth.
(A) Normalized depth of TC somata within the EPL; lines connect recorded pairs. (B, C) Within-pair intersomatic differences in EPL depth did not correlate with spike-time cross-correlogram peaks …
Figure 4
Mitral cells (MCs) and tufted cells (TCs) exhibit distinct patterns of gamma-frequency spike-time synchrony across the 5 Hz photostimulation cycle.
(A) Spike-time cross-power spectral density (CPSD) spectrograms averaged across all TC pairs (upper) and MC pairs (lower) expanded in time across consecutive photostimulation cycles (dashed lines). …
Figure 5 with 1 supplement
Tufted cells (TCs) exhibit greater spike-time synchrony across theta frequencies than mitral cells (MCs).
(A) Expanded-timescale cross-correlogram of spike times recorded in the MC pair in Figure 1A, with 50-ms-long sliding window average applied to highlight temporal patterning at frequencies < 20 Hz. …
Figure 5—figure supplement 1
Multiglomerular activation at different theta frequencies evokes qualitatively similar patterns of periodic spike-time synchrony.
(A, B) Trial-averaged cross-power spectral density (CPSD) spectrograms of spike times evoked in a heterotypic tufted cell (TC) pair (A) and homotypic TC pair (B) following 2 Hz, 5 Hz, and 8 Hz …
Figure 6 with 8 supplements
Multiglomerular activation evokes weak synchronization of inhibitory postsynaptic current (IPSC) times across gamma frequencies among both mitral cells (MCs) and tufted cells (TCs).
(A) Example voltage-clamp recording of a heterotypic MC pair during photostimulation. Morphology (upper) and representative trial (lower; blue rectangles: 10 ms light pulses of the 5 Hz …
Figure 6—figure supplement 1
Multiglomerular activation evokes a tonic increase in inhibitory postsynaptic current (IPSC) rates among both mitral cells (MCs) and tufted cells (TCs).
(A) Raster plots of IPSC times recorded during photostimulation across all trials in the MCs in Figure 6A (‘expt.’), as well as across 500 trials of spike times simulated from rate-matched …
Figure 6—figure supplement 2
Spontaneous and evoked inhibitory postsynaptic current (IPSC) properties are similar among mitral cells (MCs) and tufted cells (TCs).
(A, B) Trial-averaged IPSC rates (A) and amplitudes (B; averaged within 20 ms time bins) across all TCs and MCs during photostimulation. Blue rectangles: 10 ms light pulses of the 5 Hz …
Figure 6—figure supplement 3
Mitral cells (MCs) and tufted cells (TCs) exhibit comparable proportions of evoked synchronous to asynchronous inhibitory postsynaptic current (IPSC) rates and amplitudes.
(A) Trial-averaged rates of IPSCs occurring synchronously (|ΔtIPSC| ≤ 1 ms) and asynchronously (|ΔtIPSC| > 1 ms) between MCs of the pair in Figure 6A following photostimulation onset at 0.0 s. …
Figure 6—figure supplement 4
Mitral cell (MC) pairs and tufted cell (TC) pairs do not exhibit greater gamma-frequency inhibitory postsynaptic current (IPSC)-time synchrony than IPSC times simulated from rate-matched independent Poisson processes.
(A) Trial-averaged experimental IPSC-time cross-power spectral density (CPSD) spectrogram from the MC pair in Figure 6A following photostimulation onset at 0.0 s (upper), and equivalent …
Figure 6—figure supplement 5
Tufted cells (TCs) do not exhibit greater gamma-frequency inhibitory postsynaptic current (IPSC)-time synchrony.
(A) Time-independent IPSC-time cross-power spectral density (CPSD) of mitral cell (MC) pairs and TC pairs recorded throughout the photostimulation protocol. (B) MC pairs exhibited greater IPSC-time …
Figure 6—figure supplement 6
Inhibitory postsynaptic current (IPSC)-time synchrony does not correlate with within-pair intersomatic distance.
(A, B) Mitral cells (MCs) and tufted cells (TCs) exhibited comparable within-pair total intersomatic distance (A) (two-sample t-test: p=0.93, t7 = 0.089) and lateral intersomatic distance (B) …
Figure 6—figure supplement 7
Tufted cell (TC) inhibitory postsynaptic current (IPSC)-time synchrony does not correlate with within-pair intersomatic differences in external plexiform layer (EPL) depth.
(A) Normalized depth of TC somata within the EPL; lines connect recorded pairs. (B, C) Within-pair intersomatic differences in EPL depth did not correlate with IPSC-time cross-correlogram peaks …
Figure 6—figure supplement 8
Gamma-frequency synchronization of inhibitory currents is weak among both mitral cells (MCs) and tufted cells (TCs).
(A) Trial-averaged cross-correlogram of inhibitory currents recorded throughout the photostimulation protocol in the MC pair in Figure 6A. (B) Trial-averaged cross-power spectral density (CPSD) …
Figure 7 with 3 supplements
Greater oscillatory behavior among tufted cells (TCs) than mitral cells (MCs) promotes gamma-frequency spike-time synchrony.
(A) Trial-averaged spike-time auto-power spectral density (APSD) spectrogram from the MCs in Figure 1A. Continuous epochs (ΔHz/ms < 150) of high APSD reflecting robust periodic firing are defined as …
Figure 7—figure supplement 1
Mitral cells (MCs) and tufted cells (TCs) exhibit greater gamma-frequency spike-time periodicity than spike times simulated from rate-matched independent Poisson processes.
(A) Trial-averaged experimental spike-time auto-power spectral density (APSD) spectrogram from the anterior MC in Figure 1A following photostimulation onset at 0.0 s (upper), and equivalent …
Figure 7—figure supplement 2
Tufted cells (TCs) exhibit greater oscillatory behavior than mitral cells (MCs) on both a per-cell basis and independent of ridge-based or spectral analyses.
(A) Cellwise distribution of ridge auto-power spectral density (APSD) vs. frequency. Ellipses denote mean ± standard deviation of APSD and frequencies across all ridges detected in each cell. (B) …
Figure 7—figure supplement 3
Greater periodicity of tufted cell (TC) than mitral cell (MC) firing persists throughout the average 5 Hz photostimulation cycle.
The probability of robust spike-time periodicity reflected in spike-time auto-power spectral density (APSD) ridges was consistently higher among TCs than MCs throughout the average photostimulation …
Figure 8 with 1 supplement
Mitral cell (MC) pairs and tufted cell (TC) pairs exhibit gamma-frequency spike-time synchrony specifically when firing at gamma frequencies.
(A) Instantaneous firing rate of the MCs in Figure 1A plotted against the simultaneous frequency of periodic spike-time synchrony during each spike-time cross-power spectral density (CPSD) ridge. …
Figure 8—figure supplement 1
Firing rate differences attenuate periodic spike-time synchrony.
(A) Tufted cell (TC) pairs exhibited smaller mean firing rate differences, averaged throughout the photostimulation protocol and relative to the mean firing rate of the pair, than mitral cell (MC) …
Figure 9
Intrinsic resonance is more widespread and better entrains firing among tufted cells (TCs) than mitral cells (MCs).
(A, B) Example recording of a resonant MC. Reconstructed morphology (A) and representative response to depolarizing step current injection (B) (light trace: original membrane potential; dark trace: …
Additional files
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Transparent reporting form
- https://cdn.elifesciences.org/articles/74213/elife-74213-transrepform1-v2.pdf
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Source data 1
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- https://cdn.elifesciences.org/articles/74213/elife-74213-supp1-v2.xlsx
