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

Research output: Contribution to journalArticle

2 Citations (Scopus)

Abstract

Sensory adaptation is a source of experience-dependent feedback that impacts responses to environmental cues. In the mammalian main olfactory system (MOS), adaptation influences sensory coding at its earliest processing stages. Sensory adaptation in the accessory olfactory system (AOS) remains incompletely explored, leaving many aspects of the phenomenon unclear. We investigated sensory adaptation in vomeronasal sensory neurons (VSNs) using a combination of in situ Ca2+ imaging and electrophysiology. Parallel studies revealed prominent short-term sensory adaptation in VSNs upon repeated stimulation with mouse urine and monomolecular bile acid ligands at interstimulus intervals (ISIs) less than 30 s. In such conditions, Ca2+ signals and spike rates were often reduced by more than 50%, leading to dramatically reduced chemosensory sensitivity. Short-term adaptation was reversible over the course of minutes. Population Ca2+ imaging experiments revealed the presence of a slower form of VSN adaptation that accumulated over dozens of stimulus presentations delivered over tens of minutes. Most VSNs showed strong adaptation, but in a substantial VSN subpopulation adaptation was diminished or absent. Investigation of same-and opposite-sex urine responses in male and female VSNs revealed that adaptation to same-sex cues occurred at ISIs up to 180 s, conditions that did not induce adaptation to opposite-sex cues. This result suggests that VSN sensory adaptation can be modulated by sensory experience. These studies comprehensively establish the presence of VSN sensory adaptation and provide a foundation for future inquiries into the molecular and cellular mechanisms of this phenomenon and its impact on mammalian behavior.

Original languageEnglish (US)
Article numbere0223-18.2018
JournaleNeuro
Volume5
Issue number4
DOIs
StatePublished - Jul 1 2018

Fingerprint

Sensory Receptor Cells
Cues
Urine
Electrophysiology
Bile Acids and Salts
Ligands
Population

Keywords

  • Adaptation
  • Calcium imaging
  • Chemical senses
  • Electrophysiology
  • Olfaction
  • Vomeronasal system

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Wong, W. M., Nagel, M., Hernandez-Clavijo, A., Pifferi, S., Menini, A., Spehr, M., & Meeks, J. P. (2018). Sensory adaptation to chemical cues by vomeronasal sensory neurons. eNeuro, 5(4), [e0223-18.2018]. https://doi.org/10.1523/ENEURO.0223-18.2018

Sensory adaptation to chemical cues by vomeronasal sensory neurons. / Wong, Wen Mai; Nagel, Maximilian; Hernandez-Clavijo, Andres; Pifferi, Simone; Menini, Anna; Spehr, Marc; Meeks, Julian P.

In: eNeuro, Vol. 5, No. 4, e0223-18.2018, 01.07.2018.

Research output: Contribution to journalArticle

Wong, WM, Nagel, M, Hernandez-Clavijo, A, Pifferi, S, Menini, A, Spehr, M & Meeks, JP 2018, 'Sensory adaptation to chemical cues by vomeronasal sensory neurons', eNeuro, vol. 5, no. 4, e0223-18.2018. https://doi.org/10.1523/ENEURO.0223-18.2018
Wong WM, Nagel M, Hernandez-Clavijo A, Pifferi S, Menini A, Spehr M et al. Sensory adaptation to chemical cues by vomeronasal sensory neurons. eNeuro. 2018 Jul 1;5(4). e0223-18.2018. https://doi.org/10.1523/ENEURO.0223-18.2018
Wong, Wen Mai ; Nagel, Maximilian ; Hernandez-Clavijo, Andres ; Pifferi, Simone ; Menini, Anna ; Spehr, Marc ; Meeks, Julian P. / Sensory adaptation to chemical cues by vomeronasal sensory neurons. In: eNeuro. 2018 ; Vol. 5, No. 4.
@article{77c05bc9c73341138c3e85801098f750,
title = "Sensory adaptation to chemical cues by vomeronasal sensory neurons",
abstract = "Sensory adaptation is a source of experience-dependent feedback that impacts responses to environmental cues. In the mammalian main olfactory system (MOS), adaptation influences sensory coding at its earliest processing stages. Sensory adaptation in the accessory olfactory system (AOS) remains incompletely explored, leaving many aspects of the phenomenon unclear. We investigated sensory adaptation in vomeronasal sensory neurons (VSNs) using a combination of in situ Ca2+ imaging and electrophysiology. Parallel studies revealed prominent short-term sensory adaptation in VSNs upon repeated stimulation with mouse urine and monomolecular bile acid ligands at interstimulus intervals (ISIs) less than 30 s. In such conditions, Ca2+ signals and spike rates were often reduced by more than 50{\%}, leading to dramatically reduced chemosensory sensitivity. Short-term adaptation was reversible over the course of minutes. Population Ca2+ imaging experiments revealed the presence of a slower form of VSN adaptation that accumulated over dozens of stimulus presentations delivered over tens of minutes. Most VSNs showed strong adaptation, but in a substantial VSN subpopulation adaptation was diminished or absent. Investigation of same-and opposite-sex urine responses in male and female VSNs revealed that adaptation to same-sex cues occurred at ISIs up to 180 s, conditions that did not induce adaptation to opposite-sex cues. This result suggests that VSN sensory adaptation can be modulated by sensory experience. These studies comprehensively establish the presence of VSN sensory adaptation and provide a foundation for future inquiries into the molecular and cellular mechanisms of this phenomenon and its impact on mammalian behavior.",
keywords = "Adaptation, Calcium imaging, Chemical senses, Electrophysiology, Olfaction, Vomeronasal system",
author = "Wong, {Wen Mai} and Maximilian Nagel and Andres Hernandez-Clavijo and Simone Pifferi and Anna Menini and Marc Spehr and Meeks, {Julian P.}",
year = "2018",
month = "7",
day = "1",
doi = "10.1523/ENEURO.0223-18.2018",
language = "English (US)",
volume = "5",
journal = "eNeuro",
issn = "2373-2822",
publisher = "Society for Neuroscience",
number = "4",

}

TY - JOUR

T1 - Sensory adaptation to chemical cues by vomeronasal sensory neurons

AU - Wong, Wen Mai

AU - Nagel, Maximilian

AU - Hernandez-Clavijo, Andres

AU - Pifferi, Simone

AU - Menini, Anna

AU - Spehr, Marc

AU - Meeks, Julian P.

PY - 2018/7/1

Y1 - 2018/7/1

N2 - Sensory adaptation is a source of experience-dependent feedback that impacts responses to environmental cues. In the mammalian main olfactory system (MOS), adaptation influences sensory coding at its earliest processing stages. Sensory adaptation in the accessory olfactory system (AOS) remains incompletely explored, leaving many aspects of the phenomenon unclear. We investigated sensory adaptation in vomeronasal sensory neurons (VSNs) using a combination of in situ Ca2+ imaging and electrophysiology. Parallel studies revealed prominent short-term sensory adaptation in VSNs upon repeated stimulation with mouse urine and monomolecular bile acid ligands at interstimulus intervals (ISIs) less than 30 s. In such conditions, Ca2+ signals and spike rates were often reduced by more than 50%, leading to dramatically reduced chemosensory sensitivity. Short-term adaptation was reversible over the course of minutes. Population Ca2+ imaging experiments revealed the presence of a slower form of VSN adaptation that accumulated over dozens of stimulus presentations delivered over tens of minutes. Most VSNs showed strong adaptation, but in a substantial VSN subpopulation adaptation was diminished or absent. Investigation of same-and opposite-sex urine responses in male and female VSNs revealed that adaptation to same-sex cues occurred at ISIs up to 180 s, conditions that did not induce adaptation to opposite-sex cues. This result suggests that VSN sensory adaptation can be modulated by sensory experience. These studies comprehensively establish the presence of VSN sensory adaptation and provide a foundation for future inquiries into the molecular and cellular mechanisms of this phenomenon and its impact on mammalian behavior.

AB - Sensory adaptation is a source of experience-dependent feedback that impacts responses to environmental cues. In the mammalian main olfactory system (MOS), adaptation influences sensory coding at its earliest processing stages. Sensory adaptation in the accessory olfactory system (AOS) remains incompletely explored, leaving many aspects of the phenomenon unclear. We investigated sensory adaptation in vomeronasal sensory neurons (VSNs) using a combination of in situ Ca2+ imaging and electrophysiology. Parallel studies revealed prominent short-term sensory adaptation in VSNs upon repeated stimulation with mouse urine and monomolecular bile acid ligands at interstimulus intervals (ISIs) less than 30 s. In such conditions, Ca2+ signals and spike rates were often reduced by more than 50%, leading to dramatically reduced chemosensory sensitivity. Short-term adaptation was reversible over the course of minutes. Population Ca2+ imaging experiments revealed the presence of a slower form of VSN adaptation that accumulated over dozens of stimulus presentations delivered over tens of minutes. Most VSNs showed strong adaptation, but in a substantial VSN subpopulation adaptation was diminished or absent. Investigation of same-and opposite-sex urine responses in male and female VSNs revealed that adaptation to same-sex cues occurred at ISIs up to 180 s, conditions that did not induce adaptation to opposite-sex cues. This result suggests that VSN sensory adaptation can be modulated by sensory experience. These studies comprehensively establish the presence of VSN sensory adaptation and provide a foundation for future inquiries into the molecular and cellular mechanisms of this phenomenon and its impact on mammalian behavior.

KW - Adaptation

KW - Calcium imaging

KW - Chemical senses

KW - Electrophysiology

KW - Olfaction

KW - Vomeronasal system

UR - http://www.scopus.com/inward/record.url?scp=85053275727&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85053275727&partnerID=8YFLogxK

U2 - 10.1523/ENEURO.0223-18.2018

DO - 10.1523/ENEURO.0223-18.2018

M3 - Article

C2 - 30105301

AN - SCOPUS:85053275727

VL - 5

JO - eNeuro

JF - eNeuro

SN - 2373-2822

IS - 4

M1 - e0223-18.2018

ER -