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Research ArticleNew Research, Sensory and Motor Systems

Sensory Adaptation to Chemical Cues by Vomeronasal Sensory Neurons

Wen Mai Wong, Maximilian Nagel, Andres Hernandez-Clavijo, Simone Pifferi, Anna Menini, Marc Spehr and Julian P. Meeks
eNeuro 26 July 2018, 5 (4) ENEURO.0223-18.2018; https://doi.org/10.1523/ENEURO.0223-18.2018
Wen Mai Wong
1Department of Neuroscience, University of Texas Southwestern Medical Center, Dallas, TX 75390
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Maximilian Nagel
2Department of Chemosensation, Institute for Biology II, Rheinisch-Westfälische Technische Hochschule Aachen University, Aachen D-52074, Germany
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Andres Hernandez-Clavijo
3Neurobiology Group, SISSA, Scuola Internazionale Superiore di Studi Avanzati, Trieste 34136, Italy
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Simone Pifferi
3Neurobiology Group, SISSA, Scuola Internazionale Superiore di Studi Avanzati, Trieste 34136, Italy
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Anna Menini
3Neurobiology Group, SISSA, Scuola Internazionale Superiore di Studi Avanzati, Trieste 34136, Italy
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Marc Spehr
2Department of Chemosensation, Institute for Biology II, Rheinisch-Westfälische Technische Hochschule Aachen University, Aachen D-52074, Germany
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Julian P. Meeks
1Department of Neuroscience, University of Texas Southwestern Medical Center, Dallas, TX 75390
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    Figure 1.

    The majority of mouse VSNs display sensory adaptation on repeated stimulation with diluted urine. A, Loading of sensory neurons in acute VNO slices with a synthetic Ca2+ indicator. Top, Low-magnification DIC (left) and epi-fluorescence image (right) of a VNO section bulk-loaded with Cal-520/AM. Bottom, High-magnification images of a region of the sensory epithelium (white box in top image). Confocal DIC (left) and fluorescence (middle) images are merged (right) to show dye loading of sensory neurons. B, Representative original recordings of cytosolic Ca2+ signals in different VSN somata in response to diluted urine (1:100; 10 s) and elevated extracellular potassium (K+; 50 mM; 10 s). The integrated relative fluorescence intensities (ΔF/F) in user-defined ROIs are displayed in arbitrary units and viewed as a function of time. Neurons are stimulated at decreasing ISI of 180 s (1 → 2), 60 s (2 → 3), and 30 s (3 → 4). Black traces represent VSNs that undergo sensory adaptation of variable degree. Red trace shows a neuron that displays no adaptation. C, left, Scatter dot plot depicting relative Ca2+ signal amplitudes recorded from a total of 259 VSNs in response to stimulation 4 [data points show signal strength as percentage of the initial response amplitude (1)]. Data are categorized as indicative of adaptation (<95%; gray; n = 227) or the lack thereof (≥95%; white; n = 32). Data points marked by different red symbols correspond to original recordings shown in B. Solid horizontal line and gray shadow indicate mean ± SD of adapting VSNs. Right, Box plots illustrating the Ca2+ signal amplitudes evoked by stimulations 2 (180 s ISI), 3 (60 s ISI), and 4 (30 s ISI). Data are shown as percentage of the response to initial stimulation (1). Median values (horizontal lines), the interquartile ranges (height of the box), and the minimum and maximum values (whiskers) are plotted. Circles depict values that were >1.5 times the interquartile range from the lower or upper quartile. White box (right) corresponds to the VSNs categorized as not adapting. D, top, Original recording from a representative VSN consecutively challenged with male (black trace) and female (purple trace) urine. Interval between recordings 26 min. Fluorescence intensity (ΔF/F) is plotted as a function of time. Stimulation paradigm as in B. Bottom, Box plot (left; n = 27) quantifying and comparing the Ca2+ signal amplitudes evoked by the initial stimulations with diluted male and female urine, respectively. Note that sensitivity is fully restored after 26 min. Middle/right, Original traces and box plot quantification illustrating initial responses (black traces), responses to stimulation 4 (30 s ISI; red traces and box), and responses to a fifth stimulation after an additional 180 s recovery period (green traces and box). Asterisk (*) indicates statistical significance, p < 0.01 (one-way ANOVA in C; paired t-test in D). BV, blood vessel; DL, dendritic layer; KL, knob layer; L, lumen; SE, sensory epithelium; SL, soma layer; VNO, vomeronasal organ.

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    Figure 2.

    Evaluating sensory adaptation to monomolecular AOS ligands with population VSN Ca2+ imaging. A, VNO imaging setup using OCPI (light sheet) microscopy, which enables volumetric imaging of thousands of VSNs in the intact vomeronasal epithelium. B, Experimental design for accelerating protocol of stimulus acquisition. Two monomolecular ligands, DCA and CA, were applied in blocks of six trials (three each for DCA and CA) with the noted recovery periods within each block. C, D, Example images taken from a single frame of a 51-frame z-stack showing the responses of VSNs to repeated stimulation with 10 µM DCA in “Block 1” (180 s recovery, C) and “Block 5” (60 s recovery, D). Arrowheads mark the position of a DCA-responsive cell. Scale bar: 100 µm. Symbols refer to derivative images in E–G and traces shown in H. E–G, Normalized change in fluorescence (ΔF/F) of VSNs on trial 1 of 3 (left) and trial 3 of 3 (right) in Block 1 (180 s recovery, E), Block 5 (60 s recovery, F), and Block 7 (15 s recovery, G). Arrowheads mark the same cell as in C, D. H, Across-trial responses of a DCA-selective cell (top, same as the cell shown in C–G), a DCA- and CA-responsive cell (middle), and a CA-selective cell (bottom). Symbols refer to the responses noted in C–G.

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    Figure 3.

    VSN responses to monomolecular bile acid ligands in the accelerating intertrial interval paradigm. A, Clustering of VSN responses to 10 µM bile acids reveals three populations: those that respond to DCA-only, CA and DCA (CA + DCA), and CA-only. Each column represents ΔF/F for a single VSN across six trials of each stimulus (all trials from blocks 1 and 2). Includes responses from 486 VSNs across four tissues (four animals). Two experiments presented DCA first and two presented CA first. B, Normalized response patterns of clustered VSNs across all blocks/trials. Shown are VSNs from two experiments in which DCA was presented first. Each row is a VSN and each column a single trial. Blocks are noted by vertical ticks. C, Adaptation across and within each stimulus block, arranged by cluster. Box plots indicate the median (dark line) and 25–75% interquartile range of the per-VSN normalized response magnitude of the first trial (t1) of each block. Solid black lines/symbols indicate the degree of intrablock adaptation ([t3-t1]/[t1+offset]). D, Reduction in cluster discriminability (d’) resulting from inter- and intratrial adaptation.

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    Figure 4.

    VSN responses to monomolecular bile acid ligands in the decelerating intertrial interval paradigm. A, Stimulus delivery design. B, Example ΔF/F images showing the responses of VSNs to repeated stimulation with 10 µM DCA and 10 µM CA in “Block 1” (15 s recovery, left) and “Block 7” (180 s recovery, right). White and red arrowheads mark VSNs in the CA+DCA and CA-only clusters, respectively. C, Normalized ΔF/F responses of clustered VSNs across blocks/trials. Shown are VSNs from three experiments in which DCA was presented first. Note that cross-adaptation is largely restricted to the CA+DCA cluster. D, Interblock and intrablock adaptation, arranged by cluster. E, In stark contrast to the accelerating protocol (gray line), discriminability between the DCA-only and CA-only clusters in the decelerating protocol (black line) remained high except in trials separated by 15 s.

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    Figure 5.

    Electrophysiological recordings of evoked firing activity from individual VSNs. A, Schematic representation of a VNO coronal slice and a patch pipette in preparation for electrophysiological recordings from a VSN. B, Representative recordings in the on-cell loose-patch configuration from a single VSN showing the firing activity in response to high K+ solution (top), diluted urine (1:50; middle), or diluted artificial urine (1:50; bottom). Time of stimulus presentation is indicated by the top bars. C, Raster plots of firing activity from the same VSN in B. The recovery time between individual stimuli was at least 2 min. D, Heat map showing the average spike frequency of the traces in C in bins of 1 s. The firing frequency increased in response to urine, or to high K+ solution as a positive control, but not in response to artificial urine.

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    Figure 6.

    Spike frequency adaptation to repeated mouse urine stimulation of VSNs. A, Representative loose-patch recordings from two individual VSNs in response to double-pulse stimulations with diluted urine (1:50). A 5 s urine pulse was delivered, followed by a second identical pulse with ISIs ranging from 5 to 60 s. The recovery time between each double-pulse experiment was at least 2 min. In black, a urine-responsive VSN did not fire in response to a second pulse of urine after 5 s, showed a reduced firing frequency to the second urine pulse at 10 s ISI, and a recovery at 60 s ISI. In pink, another VSN showing a smaller reduction in firing frequency at 5- and 10-s ISIs compared to the previous VSN. B, Heat map of normalized mean firing frequency from double-pulse urine stimulations at different ISIs for 14 VSNs. The mean frequency during the second urine pulse was normalized to the mean frequency evoked by the first pulse. VSNs shown in A are indicated by black and green circles. C, Box and scatter plots of the normalized frequency at different ISIs. Each dot represents an individual VSN at a given ISI. In the box plot horizontal lines represent the median, lower and upper box boundaries represent the first and third quartile, respectively, and upper and lower whiskers represent the 5th and 95th percentile. Statistics: Tukey–Nemenyi test after Friedman test: *p < 0.01.

  • Figure 7.
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    Figure 7.

    Susceptibility to sensory adaptation is a sex-specific function of the stimulus-recipient combination. A, Representative original recordings of cytosolic Ca2+ signals from individual VSN somata in Cal-520/AM-loaded acute VNO slices. The integrated relative fluorescence intensities (ΔF/F) in user-defined ROIs are displayed in arbitrary units and viewed as a function of time. Ca2+ transients are evoked by diluted urine (1:100; 10 s) and elevated extracellular potassium (K+; 50 mM; 10 s). Temporal stimulation paradigm as in Figure 1. Trace colors indicate specific stimulus-recipient combinations: male VNO/female urine (dark gray), male VNO/male urine (purple), female VNO/male urine (light gray), female VNO/female urine (light red). B, Box plots of Ca2+ signal amplitudes (normalized to the initial response) evoked by the 2nd, 3rd, and 4th exposure to urine. Colors denote stimulus-recipient combination as in A: male VNO/female urine (dark gray; n = 60), male VNO/male urine (purple; n = 46), female VNO/male urine (light gray, n = 42), female VNO/female urine (light red, n = 79). Note that more pronounced sensory adaptation is apparently evoked by same sex (male-male; female-female) stimulation. Asterisks (*) indicate statistical significance, p < 0.05 (Dunnett test).

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Sensory Adaptation to Chemical Cues by Vomeronasal Sensory Neurons
Wen Mai Wong, Maximilian Nagel, Andres Hernandez-Clavijo, Simone Pifferi, Anna Menini, Marc Spehr, Julian P. Meeks
eNeuro 26 July 2018, 5 (4) ENEURO.0223-18.2018; DOI: 10.1523/ENEURO.0223-18.2018

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Sensory Adaptation to Chemical Cues by Vomeronasal Sensory Neurons
Wen Mai Wong, Maximilian Nagel, Andres Hernandez-Clavijo, Simone Pifferi, Anna Menini, Marc Spehr, Julian P. Meeks
eNeuro 26 July 2018, 5 (4) ENEURO.0223-18.2018; DOI: 10.1523/ENEURO.0223-18.2018
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Keywords

  • adaptation
  • calcium imaging
  • chemical senses
  • electrophysiology
  • olfaction
  • vomeronasal system

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