Pheromones Modulate Learning by Regulating the Balanced Signals of Two Insulin-like Peptides

TY - JOUR

T1 - Pheromones Modulate Learning by Regulating the Balanced Signals of Two Insulin-like Peptides

AU - Wu, Taihong

AU - Duan, Fengyun

AU - Yang, Wenxing

AU - Liu, He

AU - Caballero, Antonio

AU - Fernandes de Abreu, Diana Andrea

AU - Dar, Abdul Rouf

AU - Alcedo, Joy

AU - Ch'ng, Quee Lim

AU - Butcher, Rebecca A.

AU - Zhang, Yun

PY - 2019/12/18

Y1 - 2019/12/18

N2 - Social environment modulates learning through unknown mechanisms. Here, we report that a pheromone mixture that signals overcrowding inhibits C. elegans from learning to avoid pathogenic bacteria. We find that learning depends on the balanced signaling of two insulin-like peptides (ILPs), INS-16 and INS-4, which act respectively in the pheromone-sensing neuron ADL and the bacteria-sensing neuron AWA. Pheromone exposure inhibits learning by disrupting this balance: it activates ADL and increases expression of ins-16, and this cellular effect reduces AWA activity and AWA-expressed ins-4. The activities of the sensory neurons are required for learning and the expression of the ILPs. Interestingly, pheromones also promote the ingestion of pathogenic bacteria while increasing resistance to the pathogen. Thus, the balance of the ILP signals integrates social information into the learning process as part of a coordinated adaptive response that allows consumption of harmful food during times of high population density.

AB - Social environment modulates learning through unknown mechanisms. Here, we report that a pheromone mixture that signals overcrowding inhibits C. elegans from learning to avoid pathogenic bacteria. We find that learning depends on the balanced signaling of two insulin-like peptides (ILPs), INS-16 and INS-4, which act respectively in the pheromone-sensing neuron ADL and the bacteria-sensing neuron AWA. Pheromone exposure inhibits learning by disrupting this balance: it activates ADL and increases expression of ins-16, and this cellular effect reduces AWA activity and AWA-expressed ins-4. The activities of the sensory neurons are required for learning and the expression of the ILPs. Interestingly, pheromones also promote the ingestion of pathogenic bacteria while increasing resistance to the pathogen. Thus, the balance of the ILP signals integrates social information into the learning process as part of a coordinated adaptive response that allows consumption of harmful food during times of high population density.

KW - high population density

KW - insulin-like peptides

KW - learning

KW - neuromodulation

KW - pheromones

UR - http://www.scopus.com/inward/record.url?scp=85076238519&partnerID=8YFLogxK

U2 - 10.1016/j.neuron.2019.09.006

DO - 10.1016/j.neuron.2019.09.006

M3 - Article

C2 - 31676170

AN - SCOPUS:85076238519

SN - 0896-6273

VL - 104

SP - 1095-1109.e5

JO - Neuron

JF - Neuron

IS - 6

ER -