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Broadly tuned and respiration-independent inhibition in the olfactory bulb of awake mice

Nature Neuroscience volume 17, pages 569–576 (2014)Cite this article

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Abstract

Olfactory representations are shaped by brain state and respiration. The interaction and circuit substrates of these influences are unclear. Granule cells (GCs) in the main olfactory bulb (MOB) are presumed to sculpt activity reaching the cortex via inhibition of mitral/tufted cells (MTs). GCs potentially make ensemble activity more sparse by facilitating lateral inhibition among MTs and/or enforce temporally precise activity locked to breathing. Yet the selectivity and temporal structure of wakeful GC activity are unknown. We recorded GCs in the MOB of anesthetized and awake mice and identified state-dependent features of odor coding and temporal patterning. Under anesthesia, GCs were sparsely active and strongly and synchronously coupled to respiration. Upon waking, GCs desynchronized, broadened their tuning and largely fired independently from respiration. Thus, during wakefulness, GCs exhibited stronger odor responses with less temporal structure. We propose that during wakefulness GCs may shape MT odor responses through broadened lateral interactions rather than respiratory synchronization.

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Figure 1: Recording from identified MOB GCs in the awake and anesthetized mouse.
Figure 2: Measures of GC firing rates showed stronger and more dynamic odor responses during wakefulness.
Figure 3: GCs showed strong synchronous coupling to respiration in anesthesia and weak divergent coupling to respiration in wakefulness.
Figure 4: Respiratory coupling phase of GC spiking was unaffected by odor stimuli.
Figure 5: Temporal structure of odor responses differs in anesthetized-state and awake-state GCs.
Figure 6: Information about odors depends on the respiratory cycle in anesthetized-state GCs but not in awake-state GCs.

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Acknowledgements

We thank A. Kepecs, S. Ranade and J. Sanders for technical advice, and A. Zador, B. Li, R. Mooney, A. Fontanini, R. Froemke and Y. Ben-Shaul for comments on an earlier version of the manuscript. B.N.C. is the recipient of a Natural Sciences and Engineering Research Council of Canada Postgraduate Scholarship. This study was supported in part by an award to S.D.S. from the Esther A. & Joseph Klingenstein Fund.

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  1. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, USA

    Brittany N Cazakoff, Billy Y B Lau, Kerensa L Crump, Heike S Demmer & Stephen D Shea

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Contributions

S.D.S. supervised the project and designed the experiments together with B.N.C. and B.Y.B.L. All authors developed the methods and participated in collecting the data. S.D.S., B.N.C. and B.Y.B.L. analyzed the data and wrote the paper.

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Correspondence to Stephen D Shea.

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Integrated supplementary information

Supplementary Figure 1 Physiology and anatomical recovery methods for GCs in awake mice.

(a) Mice were head-fixed on a Styrofoam ball by clamping a head bar affixed to the skull with dental cement. Mice could move freely in 1 dimension (forward or backward). An odor delivery tube (yellow) attached to an olfactometer was placed ∼ 5 cm from the animal's nose. Both odor and isoflurane (during anesthesia) were delivered through this tube. Water reward was delivered through a lick-port positioned below the odor delivery tube. (b) A typical recording from a GC across awake and anesthetized states. Upon several presentations of odor stimuli, animals were transitioned from awake to asleep using isoflurane anesthetic (red line). Where recording stability allowed, recordings were then conducted from the same cell in the anesthetized animal for several odor presentations. Then, anesthetic was turned off, and recording continued as the animal recovered. Timing of odor presentations are not shown. (c) Granule cells in the awake animal were labeled using the same methods as for granule cells in the anesthetized animal. Movement limited cell fill times, but anatomical location, cell size, and the presence of an EPL projecting apical dendrite (arrows) confirmed GC identity. Scale bar = 20 um. (GCL = granule cell layer, EPL = external plexiform layer).

Supplementary Figure 2 Comparison of two methods for measuring respiration.

(a) Example raw traces from simultaneous respiratory recordings using a nasally implanted thermocouple (red) and a foil strain gauge (black). We observed that the peak of the strain gauge signal closely matched the point of maximum rate of change for the thermocouple signal. (b) Cross correlation of the two signals shows a lag of 68 ms for the thermocouple relative to the strain gauge. Mean and s.d. time between peaks was 67 +/- 5 ms (c) Comparison of the strain gauge with the differentiated thermocouple signal shows a good match of the signal peaks. (d) Cross correlation of the two signals in (d) shows a greatly reduced lag of 15 ms for the strain gauge relative to the thermocouple. Mean and s.d. time between peaks was 0 +/- 7 ms.

Supplementary Figure 3 Granule cell layer neurons (putative GCs) and identified GCs do not differ in their properties.

(a) Histogram of identified GCs (grey) and putative GCs (black) shows no difference in spontaneous activity between the two cell populations U(54) = 784, p = 0.8249. Identified GCs had a mean ± s.d. baseline rate of 7.30 ± 6.55 spikes/s (n = 28 cells from 19 animals) while putative GCs had a baseline rate of 7.99 ± 7.76 (n = 28 cells from 17 animals). (b) Ranked tuning curves for identified and putative GCs are similar. Identified GC curve is plotted in grey, putative GCs are plotted in black, and the combined curve is plotted in red. Only spike rates during the odor presentation are shown. (c) Response modulation index (RMI, see Online Methods) does not differ between the two groups. Each data point represents the RMI value for one cell. Mean ± s.d. RMI identified GC = 0.81 ± 0.42, n = 28 cells from 19 animals; RMI putative GC = 0.98 ± 0.54, n = 28 cells from 17 animals; U(54) = 706, p = 0.1890. (d) Coupling of spiking to breathing is not significantly different in the two groups (U(16) = 43, p = 0.2129). In both the identified GC (grey outline, n = 6 cells from 5 animals) and putative GC (black, n = 12 cells from 6 animals) groups, most cells show little coupling with breathing.

Supplementary Figure 4 Recordings from GCs across wakefulness state show state-dependent activity changes within individual GCs.

In a subpopulation of cells (n=6 cells from 6 animals), recordings were made from the same cell in both the awake and isoflurane anesthetized animal. (a) Spontaneous activity significantly increased in GCs across the anesthetized (black) to awake (grey) transition (U(5) = 25, p = 0.026). Mean firing rate ± s.e.m (red line and black lines respectively) are plotted. Anesthetized state mean ± s.d. = 2.86 ± 0.91; mean firing rate in the awake state = 13.00 ± 4.21. Paired data are plotted for each cell with the connecting line linking mean firing rate for an individual cell in each state. (b) Ranked tuning curves during 2 s odor presenta- tion and 1 s after odor offset are plotted for transitional cells in both the anesthetized (black line) and awake (grey line) state. (c) Tuning curve variance during both the 2 s odor presentation and 1 s following odor offset was greater in the awake state (during mean ± s.e.m = 17.04 ± 6.42; after = 26.94 ± 14.13) than in the anesthe- tized state (during = 1.64 ± 0.53; after = 3.53 ± 0.95, during U(5) = 22, p = 0.043; after U(5) = 25, p = 0.026). Individual data points represent one cell and mean ± s.e.m. are plotted as horizontal red and black lines respectively.

Supplementary Figure 5 Changes in breathing and GC firing with changes in locomotion.

(a) Example trace of GC activity (bottom), respiration (middle), and running velocity (top). Running was measured on an axially rotating Styrofoam ball via a rotary encoder. Locomotor activity was divided into 2 s bins, and running bins with RMS > 2 (red lines; Scale bar is 1 s and 4 cm/s for locomotion, 1 mV for breathing and 1.5 mV for GC spiking. (b) Breathing frequency increases with running. Breathing during the entire recording session was binned into 2 s intervals, and a mean rate during periods of rest or during periods of running was calculated. For all animals (n = 16 cells from 8 animals), breathing significantly increased during running (Mean breathing rate ± s.e.m. rest = 2.69 ± 0.08; running 3.68 ± 0.16; U(15) = 157, p = 0.000026). (c) GC activity is largely invariant with activity. Mean spike rate ± s.e.m. between periods of rest (8.15 ± 1.46 spikes/s) and periods of increased locomotion (8.08 ± 1.50 spikes/s) was not significantly different (U(32) = 1077, p = 0.71, left). Plotting individual data points (middle, left histogram, n = 33 cells from 19 animals) indicates a sub-population of cells is modulated with activity. Dotted red line runrate = stillrate.

Supplementary Figure 6 Assessment of respiratory coupling when GC spiking is aligned to onset of breathing.

a) Histogram (bin size = 0.1) of respiratory coupling strength (r) for anesthetized state awake state GCs. As with alignment to peak inspiration, GCs still show weak respiratory coupling. (b) Heatmap depicting baseline respiratory phase spike histograms for all awake state GCs (bin size = pi/10). Each row is a cell, and for each cell, spike count is normalized to the maximal bin for that cell. White dots denote the mean phase angle of firing for each cell. A representative breath trace is shown in black (top). Grey box in trace represents the inhalation period. (c) Histogram of mean firing phase for all cells during wakefulness (gray).

Supplementary Figure 7 Weak phase coupling in awake-state GCs is not a result of differences in breath parameters between wakefulness and anesthesia.

All breaths from 18 cells recorded in 13 awake animals were divided into quartiles for each cell according to one of four breath parameters. Respiratory coupling strength for spikes did not systematically vary with any of the breath parameters we measured: breathing rate (a), inspiratory duration (b), expiratory duration (c), and inspiratory amplitude (d). Comparing the distribution of coupling strength across quartiles for each parameter, we saw no significant differences (Kruskal-Wallis test; n = 18; p = 0.79 (a), p = 0.66 (b), p = 0.70 (c), p = 0.66 (d)).

Supplementary Figure 8 Coupling strength in GCs recorded during wakefulness did not differ between baseline breaths, the first sniffs of the odor and all subsequent odor sniffs.

(a-c) Histograms showing the distributions of coupling strength across 18 GCs recorded in 13 awake mice computed from data gathered between trials (baseline) (a), from the first sniff to odors (b), or from all subsequent odor sniffs. median coupling strength was 0.07 in (a), 0.18 in (b), and 0.13 in (c). Comparing the distributions of coupling strength across sniff type, we saw no significant differences (n = 18; H(2,51) = 2.54, p = 0.28).

Supplementary Figure 9 GCs exhibit similar activity under two anesthesia regimes.

(a) Histogram of mean spontaneous firing rates from ketamine-xylazine (grey) and isoflurane (black) animals. Mean ± s.e.m. results are summarized in boxplots (kx = 2.13 ± 0.92, iso = 2.42 ± 0.71 ). Rates between these two groups did not significantly differ (U(21) = 54, p = 0.65). Kx = ketamine-xylazine, Iso = isoflurane. (b) Ranked tuning curves for both during odor presentation and after odor offset are plotted. Data are represented as the mean ± s.e.m. for each odor and plotted in order from the odor eliciting the most inhibitory response to the odor eliciting the most excitatory response. Curve slope was calculated for both the kx and isoflurane conditions and did not differ across the two anesthetics used (kx during = 0.18, iso during = 0.1611; kx after = 0.24, iso during = 0.25).

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Cazakoff, B., Lau, B., Crump, K. et al. Broadly tuned and respiration-independent inhibition in the olfactory bulb of awake mice. Nat Neurosci 17, 569–576 (2014). https://doi.org/10.1038/nn.3669

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