Elsevier

Neuroscience

Volume 164, Issue 4, 29 December 2009, Pages 1468-1476
Neuroscience

Behavioural Neuroscience
Research Paper
The vomeronasal organ is required for the male mouse medial amygdala response to chemical-communication signals, as assessed by immediate early gene expression

https://doi.org/10.1016/j.neuroscience.2009.09.030Get rights and content

Abstract

Many species use chemical signals to convey information relevant to social and reproductive status between members of the same species (conspecific), but some chemical signals may also provide information to another species (heterospecific). Both of these types of complex chemical signals may be detected by the vomeronasal organ, which sends projections to the accessory olfactory bulb and on to the medial amygdala. Previous reports in hamster and mouse suggest that the medial amygdala sorts this complex chemosensory information categorically, according to its biological relevance (salience). In the present set of experiments, male mice having undergone vomeronasal removal surgery (VNX) or a sham-operation (SHAM) were exposed to conspecific (male and female mouse urine) or heterospecific (hamster vaginal fluid and worn cat collar) chemical stimuli. Similarly to our previous report with intact male mice [Samuelsen and Meredith (2009) Brain Res 1263:33–42], SHAM mice exhibit different immediate early gene (IEG) expression patterns in the medial amygdala dependent upon the biological relevance of the chemical stimuli. However, regardless of biological relevance, vomeronasal organ removal eliminates all responses in the medial amygdala to any of the chemical stimuli. Interestingly, VNX also disrupts the avoidance of (an unfamiliar) predator odor, worn cat collar. Here we show that the medial amygdala response to the tested chemical signals is dependent upon an intact vomeronasal organ.

Section snippets

Animals

Forty eight (Exp. 1) and 24 (Exp. 2) sexually naive 3–4 month old male C57 BL/6 mice (Jackson Laboratory) were maintained on a reverse 12/12 h light/dark cycle with food and water ad libitum. All animal procedures were approved by the Florida State University Institutional Animal Care and Use Committee. Animals had no contact with any heterospecific stimuli before the experimental session, no contact with females or female stimuli since weaning and no contact with the male or female conspecific

Results

Exposure to mMU, fMU or CC stimuli, all representatives of behaviorally salient stimuli, increased IEG expression in both MeA and MeP in sham-operated (SHAM) male mice. HVF, selected as a representative non-salient stimulus, increased IEG expression in MeA, but not MeP of SHAM mice. These expression patterns confirm our previous findings, using intact mice, of the characteristic and categorical difference between medial amygdala response to biologically relevant and to non-relevant stimuli (

Discussion

In this report, we provide evidence that IEG response to biologically relevant chemical signals in the medial amygdala depends on an intact VNO. We have previously reported that the pattern of IEG expression in medial amygdala to biologically relevant (mainly conspecific) chemical signals is categorically different from the pattern of most heterospecific stimuli. These non-relevant heterospecific chemosensory stimuli do elicit an amygdala response, but have little or no effect on behavior and

Acknowledgments

This work was supported by National Institute on Deafness and Other Communication Disorders grants dc 005813 and T32 DC00044 (M.M.) and fellowship F31 DC08062 (C.L.S.).

References (62)

  • M. Kavaliers et al.

    Estrogen receptors alpha and beta mediate different aspects of the facilitatory effects of female cues on male risk taking

    Psychoneuroendocrinology

    (2008)
  • M.N. Lehman et al.

    Vomeronasal and olfactory pathways to the amygdala controlling male hamster sexual behavior: autoradiographic and behavioral analyses

    Brain Res

    (1982)
  • M. Meredith

    Vomeronasal organ removal before sexual experience impairs male hamster mating behavior

    Physiol Behav

    (1986)
  • K. Nakamura et al.

    The critical role of familiar urine odor in diminishing territorial aggression toward a castrated intruder in mice

    Physiol Behav

    (2007)
  • C.M. Nolte et al.

    mGluR2 activation of medial amygdala input impairs vomeronasal organ-mediated behavior

    Physiol Behav

    (2005)
  • S. Pierman et al.

    Attraction thresholds and sex discrimination of urinary odorants in male and female aromatase knockout (ArKO) mice

    Horm Behav

    (2006)
  • A. Pitkanen et al.

    Organization of intra-amygdaloid circuitries in the rat: an emerging framework for understanding functions of the amygdala

    Trends Neurosci

    (1997)
  • C.L. Samuelsen et al.

    Categorization of biologically relevant chemical signals in the medial amygdala

    Brain Res

    (2009)
  • M.T. Shipley et al.

    The connections of the mouse olfactory bulb: a study using orthograde and retrograde transport of wheat germ agglutinin conjugated to horseradish peroxidase

    Brain Res Bull

    (1984)
  • L.K. Takahashi et al.

    The smell of danger: a behavioral and neural analysis of predator odor-induced fear

    Neurosci Biobehav Rev

    (2005)
  • J. Westberry et al.

    The influence of chemosensory input and gonadotropin releasing hormone on mating behavior circuits in male hamsters

    Brain Res

    (2003)
  • M. Yang et al.

    The rat exposure test: a model of mouse defensive behaviors

    Physiol Behav

    (2004)
  • P. Chamero et al.

    Identification of protein pheromones that promote aggressive behaviour

    Nature

    (2007)
  • A.K. Champlin et al.

    Determining the stage of the estrous cycle in the mouse by the appearance of the vagina

    Biol Reprod

    (1973)
  • L.M. Coolen et al.

    Bidirectional connections of the medial amygdaloid nucleus in the Syrian hamster brain: simultaneous anterograde and retrograde tract tracing

    J Comp Neurol

    (1998)
  • A. Coquelin et al.

    Pheromonally induced release of luteinizing hormone in male mice: involvement of the vomeronasal system

    J Neurosci

    (1984)
  • C. Desjardins et al.

    Social rank in house mice: differentiation revealed by ultraviolet visualization of urinary marking patterns

    Science

    (1973)
  • G.D. Fernandez-Fewell et al.

    c-fos expression in vomeronasal pathways of mated or pheromone-stimulated male golden hamsters: contributions from vomeronasal sensory input and expression related to mating performance

    J Neurosci

    (1994)
  • J. He et al.

    Encoding gender and individual information in the mouse vomeronasal organ

    Science

    (2008)
  • J.L. Hurst et al.

    Scent wars: the chemobiology of competitive signalling in mice

    Bioessays

    (2004)
  • N. Kang et al.

    A direct main olfactory bulb projection to the ‘vomeronasal' amygdala in female mice selectively responds to volatile pheromones from males

    Eur J Neurosci

    (2009)
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