Opposite-sex attraction in male mice requires testosterone-dependent regulation of adult olfactory bulb neurogenesis

Schellino, Roberta; Trova, Sara; Cimino, Irène; Farinetti, Alice; Jongbloets, Bart C.; Pasterkamp, R. Jeroen; Panzica, Giancarlo; Giacobini, Paolo; Marchis, Silvia De; Peretto, Paolo

doi:10.1038/srep36063

Cited by 26 publications

(32 citation statements)

References 72 publications

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“…At the level of the accessory olfactory bulb, mating causes a lasting increase in baseline activity by selective regulation of local inhibition (Binns and Brennan, 2005). Furthermore, recent work shows that adult neurogenesis in the AOB can be regulated by sex hormones, suggesting another mechanism by which sexual experience can regulate early sensory processing (Schellino et al, 2016). …”

Section: Discussionmentioning

confidence: 99%

Neuronal Representation of Social Information in the Medial Amygdala of Awake Behaving Mice

Mathis

Grewe

et al. 2017

Cell

230

182

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SUMMARY The medial amygdala (MeA) plays a critical role in processing species- and sex-specific signals that trigger social and defensive behaviors. However, the principles by which this deep brain structure encodes social information is poorly understood. We used a miniature microscope to image the Ca2+ dynamics of large neural ensembles in awake behaving mice and tracked the responses of MeA neurons over several months. These recordings revealed spatially intermingled subsets of MeA neurons with distinct temporal dynamics. The encoding of social information in the MeA differed between males and females and relied on information from both individual cells and neuronal populations. By performing long-term Ca2+ imaging across different social contexts, we found that sexual experience triggers lasting and sex-specific changes in MeA activity, which, in males, involve signaling by oxytocin. These findings reveal basic principles underlying the brain’s representation of social information and its modulation by intrinsic and extrinsic factors.

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Section: Discussionmentioning

confidence: 99%

Neuronal Representation of Social Information in the Medial Amygdala of Awake Behaving Mice

Mathis

Grewe

et al. 2017

Cell

230

182

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“…This procedure allowed us to analyse about one‐fourth of the area of interest. Cells contacting a line on the upper or left edge of the counting square were excluded from the counts, whereas those contacting the lower or right edge of the square were considered in the counts (Schellino et al., ). Cell densities were then calculated relative to the brain structure volume using the formula D = N /[( A × t )/10 6 ], where N is the number of counted cells, A is the sampled area (μm 2 ), and t is the thickness of the section analyzed (40 μm).…”

Section: Methodsmentioning

confidence: 99%

Positive reinforcement and c‐Fos expression following abuse‐like thinner inhalation in mice: Behavioural and immunohistochemical assessment

Malloul

Bennis

Ba‐M’hamed

2018

Eur J of Neuroscience

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Thinners are organic solvents widely used in industrial applications, but they have also been subject to abuse by inhalation for their psychoactive and rewarding properties. In spite of the prevalence of inhalant abuse, the addictive potential and pathways mediating their reinforcing effects are not yet fully understood and thus still subject of further investigations. Here, we assessed in mice the locomotor activity and the ability of paint thinner to reinforce the conditioning in the place preference paradigm following acute (1 day), subchronic (6 weeks) and chronic (12 weeks) exposures to 300 and 600 ppm of thinner vapor. While locomotor activity was unaffected by the different thinner treatments, a positive conditioned place preference to inhaled thinner was found upon subchronic and chronic exposures. To investigate the activated brain structures underlying such behavioural changes, we analyzed the distribution of c-Fos immunoreactivity, a marker for neuronal activation, following acute and repeated exposures to 600 ppm of thinner. Notably, thinner exposure increased the number of c-Fos immunoreactive neurons with increasing duration of exposure in the majority of structures examined; including those typically involved in the processing of rewarding or emotionally stimuli (e.g., ventral tegmental area, core and shell of nucleus accumbens, amygdala, bed nucleus of the stria terminalis, and cingulate cortex), and olfactory stimuli (e.g., piriform cortex and olfactory tubercle). Moreover, prolonged, but not acute thinner inhalation significantly increased c-Fos immunoreactivity in all hippocampal subregions. Taken together, the expanded distribution of thinner-induced c-Fos expression may underlie the observed positive reinforcement upon long-term thinner inhalation.

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“…Considerable evidence indicates that newly generated neurons in the olfactory bulbs play a critical role in odor discrimination broadly and pheromonal signaling among adults in particular [6,83]. As one relevant example, transgenic mice (Sema7A knockout) that have reduced GnRH release from the hypothalamus, and therefore reduced testosterone levels from birth, showed no preference for female odors over male odors in adulthood (i.e., they lacked typical male sex preferences) [84]. These transgenic animals showed a significant increase in neurogenesis within the accessory olfactory bulbs in response to exposure to male urine [84], a response not observed in wild type males but typical of wild type female mice.…”

Section: Testosterone and Adult Neurogenesis In The Olfactory Bulbsmentioning

confidence: 99%

Testosterone and Adult Neurogenesis

Spritzer

Roy

2020

Biomolecules

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It is now well established that neurogenesis occurs throughout adulthood in select brain regions, but the functional significance of adult neurogenesis remains unclear. There is considerable evidence that steroid hormones modulate various stages of adult neurogenesis, and this review provides a focused summary of the effects of testosterone on adult neurogenesis. Initial evidence came from field studies with birds and wild rodent populations. Subsequent experiments with laboratory rodents have tested the effects of testosterone and its steroid metabolites upon adult neurogenesis, as well as the functional consequences of induced changes in neurogenesis. These experiments have provided clear evidence that testosterone increases adult neurogenesis within the dentate gyrus region of the hippocampus through an androgen-dependent pathway. Most evidence indicates that androgens selectively enhance the survival of newly generated neurons, while having little effect on cell proliferation. Whether this is a result of androgens acting directly on receptors of new neurons remains unclear, and indirect routes involving brain-derived neurotrophic factor (BDNF) and glucocorticoids may be involved. In vitro experiments suggest that testosterone has broad-ranging neuroprotective effects, which will be briefly reviewed. A better understanding of the effects of testosterone upon adult neurogenesis could shed light on neurological diseases that show sex differences.

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Opposite-sex attraction in male mice requires testosterone-dependent regulation of adult olfactory bulb neurogenesis

Cited by 26 publications

References 72 publications

Neuronal Representation of Social Information in the Medial Amygdala of Awake Behaving Mice

Neuronal Representation of Social Information in the Medial Amygdala of Awake Behaving Mice

Positive reinforcement and c‐Fos expression following abuse‐like thinner inhalation in mice: Behavioural and immunohistochemical assessment

Testosterone and Adult Neurogenesis

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