Behavioral Performance and Neural Systems Are Robust to Sensory Injury in Workers of the Ant Pheidole dentata

Abstract

Miniaturized nervous systems have been thought to limit behavioral ability, and animals with miniaturized brains may be less flexible when challenged by injuries resulting in sensory deficits that impact the development, maintenance, and plasticity of small-scale neural networks. We experimentally examined how injuries to sensory structures critical for olfactory ability affect behavioral performance in workers of the ant Pheidole dentata, which have minute brains (0.01 mm³) and primarily rely on the perception and processing of chemical signals and cues to direct their social behavior. We employed unilateral antennal denervation to decrease the olfactory perception ability of workers and quantified consequential neuroanatomical and behavioral performance effects. Postablation neuroanatomical metrics revealed a 25% reduction in the volume of the antennal lobe ipsilateral to the antennal lesion relative to the contralateral lobe, indicating atrophy of the input-deprived tissue. However, antennectomy did not affect the volumes of the mushroom body or its subcompartments or the number of mushroom body synaptic complexes (microglomeruli) in either brain hemisphere. Synapsin immunoreactivity, however, was significantly higher in the ipsilateral mushroom body calyces, which could reflect presynaptic potentiation and homeostatic compensation in higher-order olfactory regions. Despite tissue loss caused by antennal lesioning and resulting unilateral sensory deprivation, the ability of workers to perform behaviors that encompass the breadth of their task repertoire and meet demands for colony labor remained largely intact. The few behavioral deficits recorded were restricted to pheromone trail-following ability, a result that was expected due to the need for bilateral olfactory input to process spatial odor information. Our macroscopic and cellular neuroanatomical measurements and assessments of task performance demonstrate that the miniaturized brains of P. dentata workers and their sensorimotor functions are remarkably robust to injury-related size reduction and remain capable of generating behaviors required to respond appropriately to chemical social signals and effectively nurse immatures, as well as participate in coordinated foraging.