Attraction to sexual pheromones and associated odorants in female mice involves activation of the reward system and basolateral amygdala

Moncho-Bogani, José; Martı́nez-Garcı́a, Fernando; Novejarque, Amparo; Lanuza, Enrique

doi:10.1111/j.1460-9568.2005.04036.x

Cited by 87 publications

(88 citation statements)

References 60 publications

(90 reference statements)

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“…This result corroborated findings of several previous studies in which significant increments in Fos expression were observed in the AcbC and/or the AcbSh of male rats (Bakker, Baum, & Slob, 1996;Lopez & Ettenberg, 2002;Paredes, Lopez, & Baum, 1998) and of ovariectomized, testosterone-primed female rats (Bressler & Baum, 1996) following exposure to soiled estrous female bedding. Likewise, exposure to soiled male bedding stimulated Fos-IR cells in the AcbSh of female mice (Moncho-Bogani et al, 2005). Studies using male rats (Hosokawa & Chiba, 2005;Kippin, Cain, & Pfaus, 2003;Lopez & Ettenberg, 2002) showed that the ability of estrous female bedding to augment Fos expression in either the AcbC or the AcbSh was greater in mice that had previously mated with a female.…”

Section: Discussionmentioning

confidence: 99%

“…We examined regions receiving inputs from the VNO including the mitral and granule cell layers of the AOB, the anterior portion (MeA) and posterior dorsal portion (MePD) of the medial amygdala, the bed nucleus of the stria terminalis (BNST), the ventral lateral ventromedial hypothalamus (VMHVL), and the medial preoptic area (MPA; Halpern & Martinez-Marcos, 2003). We also examined corticoamygdaloid sites that receive input from the main olfactory bulb including the anterior (ACo) and posterolateral (PLCo) cortical amygdaloid nucleus, areas of the corticolimbic amygdala including the posterior part of the basomedial amygdaloid nucleus (BMP) as well as the anterior (BLA) and posterior (BLP) parts of the basolateral amygdaloid nucleus that have been shown to mediate conditioned sexual reward (Everitt, Cador, & Robbins, 1989) and more recently to be involved in vomeronasalolfactory reward (Moncho-Bogani, Martinez-Garcia, Novejarque, & Lanuza, 2005), and areas of the mesolimbic dopamine pathway (Salamone, 2002) including the AcbC and AcbSh and the ventral tegmental area (VTA). See Figure 2 for drawings of the specific sites where Fos-IR cells were counted in each of these brain regions.…”

Section: Experiments 4: Fos-ir Induced In Different Forebrain Regions mentioning

confidence: 99%

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Effect of vomeronasal organ removal from male mice on their preference for and neural Fos responses to female urinary odors.

Pankevich¹,

Cherry²,

Baum³

2006

Behavioral Neuroscience

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Four experiments were conducted to determine whether vomeronasal organ (VNO) inputs in male mice mediate the rewarding properties of estrous female urinary odors. Sexually naive male mice with either an intact (VNOi) or lesioned (VNOx) VNO preferred to investigate female urine over water in Y-maze tests. Subsequently, VNOi males ran significantly more quickly and remained in nasal contact longer with estrous female urine than with male urine, whereas VNOx males investigated these odors equally. In home-cage habituation-dishabituation tests, VNOi males also investigated female urine significantly longer than did VNOx males, although both groups investigated female urine longer than other non-body odors. Finally, female urinary odors induced Fos in the nucleus accumbens core of VNOi males but not of VNOx males. Our results suggest that female urinary odors retain some incentive value in VNOx males. However, once direct nasal contact is made with female urine, VNO inputs further activate forebrain mechanisms that amplify the reward salience of this stimulus for the male mouse. Keywordsaccessory olfactory bulb; nucleus accumbens; pheromones; sexual behavior Social communication in rodents occurs via volatile as well as nonvolatile components of urine and other body odorants (Brown, 1979). Several studies (Lin, Zhang, Block, & Katz, 2005;Schaefer, Yamazaki, Osada, Restrepo, & Beauchamp, 2002;Schaefer, Young, & Restrepo, 2001) suggest that volatile components of urine are detected by receptor neurons in the main olfactory epithelium and processed in the main olfactory bulb, whereas other studies suggest that nonvolatile components of urine (Luo, Fee, & Katz, 2003) as well as extraorbital lacrimal gland secretions (Kimoto, Haga, Sato, & Touhara, 2005) are detected by receptor neurons in the vomeronasal organ (VNO) and processed in the accessory olfactory bulb (AOB). Socially relevant olfactory signals from both the main and accessory systems are integrated in the medial amygdala prior to being conveyed to different hypothalamic regions (Boehm, Zou, & Buck, 2005;Kevetter & Winans, 1981a, 1981bLicht & Meredith, 1987). We (Pankevich, Baum, & Cherry, 2004) reported that surgical VNO removal (VNOx) eliminated the normal preference of male mice to remain in nasal contact with estrous female as opposed to male urine in the home cage. Likewise, VNO removal significantly reduced the preference of female mice to directly investigate male as opposed to female urine spots in Y-maze tests (Keller, Pierman, Douhard, Baum, & Bakker, 2006). Taken together, these results raise the possibility that inputs from the VNO-accessory olfactory system are rewarding and thereby enhance the motivation Correspondence concerning this article should be addressed to Michael J. Baum, Department of Biology, Boston University, 5 Cummington Street, Boston, MA 02215. E-mail: baum@bu.edu. Diana E. Pankevich, James A. Cherry, and Michael J. Baum, Departments of Biology and Psychology, Boston University. (Beauchamp, Martin, Wysocki, & Wellington, 1...

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Section: Discussionmentioning

confidence: 99%

Section: Experiments 4: Fos-ir Induced In Different Forebrain Regions mentioning

confidence: 99%

Effect of vomeronasal organ removal from male mice on their preference for and neural Fos responses to female urinary odors.

Pankevich¹,

Cherry²,

Baum³

2006

Behavioral Neuroscience

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“…This projection is via the medial amygdala to the various hypothalamic nuclei that regulate these behaviours. These same neural pathways that transduce pheromone signals also access the brain's 'reward' circuitry via the amygdala to the shell of the NAcc (Moncho-Bogani et al 2005). The main olfactory projections also relay in the amygdala via the main OB and pyriform cortex, the pyriform cortex also making connections with the frontal cortex via the medial-dorsal nucleus of the thalamus (figure 2).…”

Section: A Declining Role For Olfactory Systems In Social Reward For mentioning

confidence: 99%

“…The amygdala has reciprocal connections with the NAcc, and both structures show enhanced levels of neural activation in rodents following exposure to biologically significant odours (Moncho-Bogani et al 2005). Olfactory activation during social encounters between mother and pups induces neural activation of the amygdala (Fleming & Korsmit 1996), lesions to the amygdala eliminate aversion of pup odours in virgin rats (Fleming et al 1980), and both OTand vasopressin release in the central amygdala regulates the autonomic expression of fearful or neophobic responses (Huber et al 2005).…”

Section: Parental Bonds In Small-brained Mammalsmentioning

confidence: 99%

Mother–infant bonding and the evolution of mammalian social relationships

Broad

Curley

Keverne

2006

Phil. Trans. R. Soc. B

234

193

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A wide variety of maternal, social and sexual bonding strategies have been described across mammalian species, including humans. Many of the neural and hormonal mechanisms that underpin the formation and maintenance of these bonds demonstrate a considerable degree of evolutionary conservation across a representative range of these species. However, there is also a considerable degree of diversity in both the way these mechanisms are activated and in the behavioural responses that result. In the majority of small-brained mammals (including rodents), the formation of a maternal or partner preference bond requires individual recognition by olfactory cues, activation of neural mechanisms concerned with social reward by these cues and gender-specific hormonal priming for behavioural output. With the evolutionary increase of neocortex seen in monkeys and apes, there has been a corresponding increase in the complexity of social relationships and bonding strategies together with a significant redundancy in hormonal priming for motivated behaviour. Olfactory recognition and olfactory inputs to areas of the brain concerned with social reward are downregulated and recognition is based on integration of multimodal sensory cues requiring an expanded neocortex, particularly the association cortex. This emancipation from olfactory and hormonal determinants of bonding has been succeeded by the increased importance of social learning that is necessitated by living in a complex social world and, especially in humans, a world that is dominated by cultural inheritance.

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“…ImageJ software (National Institutes of Health) was used for image analysis. Following the method of Moncho-Bogani et al (52), counts were obtained and calculated per 0.1 mm 2 ( Fig. S7).…”

Section: Methodsmentioning

confidence: 99%

Synthetic zinc finger repressors reduce mutant huntingtin expression in the brain of R6/2 mice

Garriga-Canut

Agustín-Pavón

Herrmann

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

173

142

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Huntington's disease (HD) is a dominantly inherited neurodegenerative disorder caused by expanded CAG repeats in the huntingtin (HTT) gene. Although several palliative treatments are available, there is currently no cure and patients generally die 10-15 y after diagnosis. Several promising approaches for HD therapy are currently in development, including RNAi and antisense analogs. We developed a complementary strategy to test repression of mutant HTT with zinc finger proteins (ZFPs) in an HD model. We tested a "molecular tape measure" approach, using long artificial ZFP chains, designed to bind longer CAG repeats more strongly than shorter repeats. After optimization, stable ZFP expression in a model HD cell line reduced chromosomal expression of the mutant gene at both the protein and mRNA levels (95% and 78% reduction, respectively). This was achieved chromosomally in the context of endogenous mouse HTT genes, with variable CAG-repeat lengths. Shorter wild-type alleles, other genomic CAG-repeat genes, and neighboring genes were unaffected. In vivo, striatal adeno-associated virus viral delivery in R6/2 mice was efficient and revealed dose-dependent repression of mutant HTT in the brain (up to 60%). Furthermore, zinc finger repression was tested at several levels, resulting in protein aggregate reduction, reduced decline in rotarod performance, and alleviation of clasping in R6/2 mice, establishing a proof-of-principle for synthetic transcription factor repressors in the brain.

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Attraction to sexual pheromones and associated odorants in female mice involves activation of the reward system and basolateral amygdala

Cited by 87 publications

References 60 publications

Effect of vomeronasal organ removal from male mice on their preference for and neural Fos responses to female urinary odors.

Effect of vomeronasal organ removal from male mice on their preference for and neural Fos responses to female urinary odors.

Mother–infant bonding and the evolution of mammalian social relationships

Synthetic zinc finger repressors reduce mutant huntingtin expression in the brain of R6/2 mice

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