What if worms were sentient? Insights into subjective experience from the Caenorhabditis elegans connectome

Abstract

Deciphering the neural basis of subjective experience remains one of the great challenges in the natural sciences. The structural complexity and the limitations around invasive experimental manipulations of the human brain have impeded progress towards this goal. While animals cannot directly report first-person subjective experiences, their ability to exhibit flexible behaviours such as motivational trade-offs are generally considered evidence of sentience. The worm Caenorhabditis elegans affords the unique opportunity to describe the circuitry underlying subjective experience at a single cell level as its whole neural connectome is known and moreover, these animals exhibit motivational trade-offs. We started with the premise that these worms were sentient and then sought to understand the neurons that were both necessary and sufficient for a motivational trade-off involving the rewarding experience of food and the negative experience of an aversive odour. A simple hierarchical network consisting of two chemosensory neurons and three interneurons was found to produce an output to motoneurons that enabled worms to respond in a contextually appropriate manner to an aversive odour according to the worm's hunger state. Given that this circuitry is like that found in the human spinal cord, retina, and primary visual cortex, three regions which are neither necessary nor sufficient for subjective experience, we conclude that motivational trade-offs are not a criterion for subjective experience in worms. Furthermore, once the neural substrate for a behaviour is described, we question the explanatory role of subjective experience in behaviour.