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Developmental broadening of inhibitory sensory maps

Nature Neuroscience volume 20, pages 189–199 (2017)Cite this article

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Abstract

Sensory maps are created by networks of neuronal responses that vary with their anatomical position, such that representations of the external world are systematically and topographically organized in the brain. Current understanding from studying excitatory maps is that maps are sculpted and refined throughout development and/or through sensory experience. Investigating the mouse olfactory bulb, where ongoing neurogenesis continually supplies new inhibitory granule cells into existing circuitry, we isolated the development of sensory maps formed by inhibitory networks. Using in vivo calcium imaging of odor responses, we compared functional responses of both maturing and established granule cells. We found that, in contrast to the refinement observed for excitatory maps, inhibitory sensory maps became broader with maturation. However, like excitatory maps, inhibitory sensory maps are sensitive to experience. These data describe the development of an inhibitory sensory map as a network, highlighting the differences from previously described excitatory maps.

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Figure 1: Genetically targeting populations of granule cells in the adult olfactory bulb.
Figure 2: Comparison of membrane and firing properties of functionally immature Dlx5/6 versus functionally mature Crhr1 granule cells.
Figure 3: Olfactory sensory maps from different populations of olfactory bulb neurons visualized through calcium imaging.
Figure 4: Inhibitory sensory maps broaden with maturation.
Figure 5: Mature granule cells show recruitment over refinement of synaptic inputs.
Figure 6: Individual granule cells respond to more odors with maturation.
Figure 7: Decreased sensory experience prevents sensory map expansion.
Figure 8: Olfactory learning precociously expands inhibitory sensory maps.

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Acknowledgements

We would like to thank A. Herman, C. Kim, H. Lu, D. Murphey, K. Schulze and R. Sillitoe for discussion and critical input on this manuscript. This work was supported by the McNair Medical Institute, the Charif Souki Fund, IRACDA Fellowship K12 GM084897 to K.Q., NRSA F31NS089178 to K.U., NINDS grant F31NS081805 to I.G., NINDS R01NS078294 to B.R.A., U54HD083092 to the BCM IDDRC, and the Intelligence Advanced Research Projects Activity (IARPA) via Department of Interior/Interior Business Center (DoI/IBC) contract number D16PC00003 to A.S.T. The US Government is authorized to reproduce and distribute reprints for Governmental purposes notwithstanding any copyright annotation thereon. Disclaimer: The views and conclusions contained herein are those of the authors and should not be interpreted as necessarily representing the official policies or endorsements, either expressed or implied, of IARPA, DoI/IBC or the US Government.

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Authors and Affiliations

  1. Department of Molecular & Human Genetics, Baylor College of Medicine, Houston, Texas, USA

    Kathleen B Quast & Benjamin R Arenkiel

  2. Program in Developmental Biology, Baylor College of Medicine, Houston, Texas, USA

    Kevin Ung, Isabella Herman, Joshua Ortiz-Guzman & Benjamin R Arenkiel

  3. Department of Neuroscience, Baylor College of Medicine, Houston, Texas, USA

    Emmanouil Froudarakis, Longwen Huang, Keith Cordiner, Peter Saggau, Andreas S Tolias & Benjamin R Arenkiel

  4. Medical Scientist Training Program, Baylor College of Medicine, Houston, Texas, USA

    Isabella Herman

  5. SMART Program, Baylor College of Medicine, Houston, Texas, USA

    Angela P Addison

  6. University of St. Thomas, Houston, Texas, USA

    Angela P Addison

  7. Allen Institute for Brain Science, Seattle, Washington, USA

    Peter Saggau

  8. Department of Electrical and Computer Engineering, Rice University, Houston, Texas, USA

    Andreas S Tolias

  9. Jan and Dan Duncan Neurological Research Institute at Texas Children's Hospital, Houston, Texas, USA

    Benjamin R Arenkiel

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Contributions

K.B.Q. and B.R.A. designed the study, performed the analysis and wrote the manuscript. K.B.Q. performed most of the experiments. K.U. contributed to the behavior and wide-field imaging. E.F. and A.S.T. performed the two-photon experiments. L.H. performed the optogenetic mapping experiments on the AOD set up designed by L.H., K.C., P.S. and B.R.A. A.P.A., J.O.-G. and I.H. assisted with behavior, histology and surgeries.

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Correspondence to Benjamin R Arenkiel.

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Integrated supplementary information

Supplementary Figure 1 Stable cell morphology.

(a) Overview of olfactory bulb slices from Dlx5/6-Cre and Crhr1-Cre animals injected with high titer AAV-flex-GFP (Scale bar 500 μm). (b) Example GFP neuron outlines as traced in Neurolucida from immature Dlx5/6-Cre + AAV-flex-GFP (left) and mature Crhr1-Cre + AAV-flex-GFP (right) animals (Scale bar 50 μm). No significant changes in the size of the cell body (c), total apical dendrite length (d), number of basal dendrites (e) or the distance from the mitral cell layer (f). (data point represent individual cells, red line at the mean ±SEM).

Supplementary Figure 2 Viral GCaMP expression does not change the membrane properties of granule cells.

No significant changes between Dlx5/6 expressing neurons labeled with viral GFP or GCaMP6 measured by (a) membrane capacitance p = 0.1315, (b) membrane resistance p = 0.1626, (c) action potential half-width p = 0.9024, (d) frequency-current curves, (e) resting potential p = 0.4202, (f) current required for action potential (resting potential between -60 and -65 mV)p = 0.0720, or (g) time to action potential peak in response to 30 pA current injection p = 0.5480. (data points represent individual cells, bars at averages ± SEM, n = 26 for GFP, n = 11 for GCaMP6).

Supplementary Figure 3 Analyzing ΔF/F of pentanol activation.

(a and b) Example sensory map for pentanol (top), and the area activated at 50% or more of the maximal change in fluorescence (50% max ΔF/F) (bottom) (Scale bar 1 mm). (c) No change in maximal ΔF/F value across animals. (d) Significant increase in the 50% max ΔF/F area of the mature granule cells. (data points represent individual animals, bar at mean ± SEM, n = 7 animals per genotype, minimum of 3 trials per odorant, * p = 0.0491 Students t-test)

Supplementary Figure 4 Broader sensory maps of mature inhibitory neurons for multiple stimuli.

Example ΔF sensory map for anisole (a and b), and isoamyl acetate (e and f) (Scale bar 1 mm). (c and g) No change in maximal ΔF value across animals. Significant increase in the 50% max ΔF area of the mature granule cells for both (d) p=0.0187 and (h) p=0.0345. (data points represent individual animals, bars at mean ± SEM, n = 7 animals per genotype, minimum of 3 trials per odorant, * p<0.05 Students t-test)

Supplementary Figure 5 Inhibitory sensory maps broaden with maturation regardless of genetic marker.

a) Example ΔF sensory maps for pentanol for a Dlx5/6-Cre animal 2-3 weeks after viral injection (top), a Crhr1-Cre animal 2-3 weeks after viral injection (middle) and a Dlx5/6-Cre animal 6-8 weeks after viral injection (bottom) (Scale bar 1 mm). (b) Significant increase in the 50% max ΔF area of the mature granule cells across stimuli regardless of genetic marker (data points represent averages ± SEM, n = 7 Dlx5/6, n = 7 Crhr1, n = 3 Dlx5/6 6-8 weeks, minimum of 3 trials per odorant, * p<0.05, ** p<0.01 One-way ANOVA, Sidak’s multiple comparison).

Supplementary Figure 6 AOD-assisted optogenetic targeting of mitral cells.

(a) Diagram of AOD microscope and patched cells, (yellow = mitral cells as in Supplemental Fig. 6, red = granule cell as in Fig. 5). (b) Example patched mitral cell and location of light stimulation grid to ensure excitation of mitral cells was limited to stimulation over cell body as quantified in (c) which shows the probability of eliciting and action potential from AOD stimulation over a 30 μm2 grid around a patched mitral cell (asterisk) (n = 6 mitral cells). (d) Representative action potentials elicited from light stimulation over the soma of an example mitral cell. (Scale bar: 10 mV, 5 ms).

Supplementary Figure 7 Olfactory learning and immature granule cell synaptic changes.

(a) Performance of mice across many trials (about 200 trials/day) increases through training. (data points represent averages ± SEM, n = 10 animals for Dlx5/6-Cre and n=12 for Crhr1-Cre). (b) Example ΔF sensory maps for control and trained Dlx5/6-Cre mice in response to the S- odor (carvone(+)) and a novel odor (anisole) (e and f) and quantification in (c) showing map expansion is generalizable to other trained odors. (data points represent individual animals, bar at mean values ± SEM, n = 5 animals trained, 6 animals control, * p = 0.0123, One-way ANOVA, Sidak’s correction). (d) Representative mEPSC traces from Dlx5/6 expressing neurons from either control (top) or trained animals (bottom) with example averaged event on right (Scale bars full trace: 20 pA, 1 s; average: 8 pA, 10 ms). (e) Cumulative interval and (f) cumulative amplitude are significantly different in control versus trained mice (p < 0.0001 KS test), however the mean frequency (e, inset) shows increased variance (F test p < 0.0001) and trend toward increased frequency and no change in mean amplitude (f, inset) (data points represent individual cells, bars at mean values ± SEM, for mini data: n = 13 control granule cells and 12 trained cells from 4 animals each control and trained, injected with AAV-flex-GFP or AAV-flex-tdTomato).

Supplementary Figure 8 Passive odor exposure does not expand inhibitory sensory maps.

(a) Diagram of experimental setup showing 2 tea-strainer balls containing different odors that were hung in the animal’s home cage for an hour per day. (b) Timeline of experiment. (c) Example ΔF sensory maps for control and exposed mice in response to one exposed odor (anisole) and a novel odor (acetephenone) and quantification in (d) showing map no expansion. (data points represent individual animals, bars at mean values ± SEM, n = 4 Dlx5/6-Cre animals control, 4 Dlx5/6-Cre animals exposed, all injected with AAV-flex-GCaMP6m).

Supplementary Figure 9 Olfactory learning does not expand sensory maps for mature granule cells.

(a) Representative ΔF sensory map for control and trained mice in response to the unrewarded trained odor (carvone (+) and a novel odor (anisole) (scale bar 1 mm). (b) Mean activated area (± SEM, n = 4 animals control, 4 animals exposed all Crhr1-Cre injected with AAV-flex-GCaMP6). (c) Representative mEPSC traces from Crhr1 expressing neurons from either control (left) or trained animals (right) with example averaged event below (Scale bars full trace: 20 pA, 1 s; average: 8 pA, 10 ms). Cumulative interval distribution (d) and amplitude distribution (e) with cell means inset. (bar graphs represent mean values ± SEM, for mini data: n = 13 control granule cells and 8 occluded cells from 4 Crhr1-Cre animals + AAV-flex-GFP, each control and trained).

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Quast, K., Ung, K., Froudarakis, E. et al. Developmental broadening of inhibitory sensory maps. Nat Neurosci 20, 189–199 (2017). https://doi.org/10.1038/nn.4467

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