Title: The Neural Circuitry of Aggression, Sex and Sexual Aggression
Name: David J. Anderson
Tianqiao and Chrissy Chen Institute for Neuroscience
California Institute of Technology

http://www.davidandersonlab.caltech.edu/

Year: 2014
Type: Research Grant
Summary:

Mating and aggression are innate (or instinctive) behaviors that are performed without training. Interestingly, among animals, these two seemingly different behaviors appear to be inextricably intertwined: aggressive encounters are often associated with mating, when males exhibit their dominance for sexual opportunities. However, male-female interactions are primarily sexual (mating) and male-male interactions tend to be aggressive, while aggression towards females is more often the exception than the norm. What brain mechanisms are responsible for separating sexual behavior towards females, and violent aggression towards males, under normal conditions?

To investigate the brain mechanisms, we used a technique called microendoscopy that allowed us to image deep-brain (hypothalamic) neuronal activity in male mice engaged in social behaviors. We recorded over two hundred neurons on average in each mouse (total 25 mice) and the mice had no trouble fighting or mating because of the microendoscope neural implant.

In sexually and socially experienced adult male mice, neurons were strongly active during interactions with conspecifics, but not with a toy. It was immediately clear that characteristic, yet separate, ensembles of neurons were active during interactions with male or female conspecifics. But surprisingly, in inexperienced adult males common populations of neurons were activated by both male and female conspecifics. The sex-specific ensembles gradually emerged as the mice acquired social and sexual experience. These observations indicated that interactions with males and females was required for the distinct representations of males and females in the adult mouse brain.

We performed another set of experiments were adult male mice were permitted to investigate (touch, smell etc.) but not mount or attack other female or male mice. In this case we did not observe female or male-specific ensembles or divergent representations in the brain, suggesting that sensory exposure itself was insufficient. However, providing male mice with brief sexual experience was sufficient to generate neuronal ensembles that were specific males and females, divergent neural representations of conspecific sex and aggression towards males. This experiment demonstrated that social interactions are necessary for the formation of male and female specific neuronal ensembles.

These observations reveal an unexpected requirement of experience for behaviors that were traditionally viewed as a "hard-wired" or innate. Social experience was required for the formation of neuronal ensembles that themselves control social behavior.

Bibliography:

Remedios R, Kennedy A, Zelikowsky M, Grewe BF, Schnitzer MJ, Anderson DJ. (2017) Social Behaviour Shapes Hypothalamic Neural Ensemble Representations Of Conspecific Sex. Nature. In Press.

Kennedy A, Asahina K, Hoopfer E, Inagaki H, Jung Y, Lee H, Remedios R, Anderson DJ. (2015) Internal States and Behavioral Decision-Making: Toward an Integration of Emotion and Cognition. Cold Spring Harb Symp Quant Biol. 79:199-210.