Sexy neurogenesis

Animal communication is wonderfully diverse, ranging from the dance of a bee, to written language, to a dog urinating on a tree. For many (all?) animal species, the majority of animal communication is strategically targeted with one goal in mind: sex. Most species lack our oratory competence, yet seem to be procreating rather successfully, able to wordlessly identify and attract mates with desirable genetic backgrounds.

Although sight and sound dominate human communication, many animals use smell to exchange information, able to convey age, social status, sexual receptivity, gender, and health with the chemicals released by their bodies. In fact, many species can recognize individuals by their olfactory "signature" alone, allowing, for example, a mother to recognize her young, and preventing siblings from mating with each other.

This type of communication is mediated, in part, by poorly understood chemicals called pheromones. Mammalian pheromones can elicit immediate behavioral responses, such as aggression (when a male mouse detects the urine of another male mouse) or sexual behavior (when a female mouse detects the same). Of course, the behavioral effects of pheromones are context-dependent; in fact, the fiercest, most aggressive mouse fights I’ve ever witnessed arise when lactating females catch a whiff of a novel male mouse, upon which she unleashes a bloody, ferocious attack on his genitals.

Mammalian pheromones can also elicit long-lasting effects that alter the physiological state of the animal. For example, the detection of male pheromones by a juvenile female mouse may result in an advance in the onset of puberty. If, however, a pregnant female mouse detects the pheromones of a novel male mouse (e.g. one who has dueled and defeated her current suitor and the “father” of her embryos), she will terminate her pregnancy. The latter is an act of mercy--if she did not abort her pups, the male mouse would have killed them upon birth, ensuring that his chosen mate devotes her time and efforts solely to his genetic material.

Crucial to these pheromone-elicited behaviors is the ability to recognize and discriminate between pheromones. Such social recognition thus requires olfactory memories; just as the evanescent taste of a madeleine cookie evokes the Belle Époque world of Proust’s childhood, a female mouse can associate the scent and taste of a “special” male mouse’s urine with the protection he offers her and her pups. Such olfactory memories may require not only the olfactory bulb (the neural structure involved in perceiving odors), but also the hippocampus (a structure crucial for certain types of memory formation).

These structures happen to be the two primary locations where new neurons continue to be born into adulthood (a process called adult neurogenesis). Since I began research on adult neurogenesis, I have been captivated by the myriad of factors (e.g. running, stress, pregnancy, cognitive stimulation, a multitude of drugs…) that affect the birth, survival, and functionality of new neurons. Given that such modulation must be functionally advantageous, this plasticity has fascinating implications for the evolution of adult neurogenesis, as well as the impact these neurons may have on neural circuits and behaviors.

One matter that has always intrigued me is that the modulators of neurogenesis affect either hippocampal or olfactory bulb neurogenesis, but not both. Thus, I was excited to see an advance online publication in Nature Neuroscience that sought to link neurogenesis in both structures to mating behavior. The research, performed by Sam Weiss at the University of Calgary, focused on female mice, and the olfactory memories endowing them with the ability to identify and select prospective mates.

The researchers found that week-long exposure to male mouse urine simultaneously increased the birth of new neurons in the hippocampus and a region called the subventricular zone (SVZ, the birthplace of neurons destined for the olfactory bulb). Congruent with female preference for powerful men, this response was specific for the urine of dominant males; exposure to urine of subordinate did not result in enhanced neurogenesis.

Two weeks after exposure to either dominant or subordinate male urine, the females were placed in a test cage, in which they could smell and see, but not contact, both the dominant and subordinate male. Females primed with the dominant male pheromones had a preference for the dominant male (determined by quantification of “sniffing time”), whereas females exposed to the subordinate male did not show a preference. When neurogenesis was inhibited by a chemical treatment, however, the females did not show a preference regardless of the male with which she was "primed," implicating that male pheromone-induced neurogenesis was necessary for olfactory recognition and/or discrimination.

The results imply that the exposure to a dominant male may provide the impetus for a female to form a new olfactory memory, mediated by the birth of new neurons. Her olfactory system, constantly barraged with olfactory signals, lies in wait for a whiff of something enchanting and unique, which calls it to attention and prompts it to take action. These specialized olfactory memories allow her to distinguish the males with the greatest genetic gifts from the undesirables.