Designing Brains for Pain: Human to Mollusc.

Subjective sensory experience, or what it feels like, arises in the cerebral cortex of humans and mammals. While humans verbally report their experiences, other species' awareness is inferred from behavior. Cephalopods have been considered sentient due to complex behavior, but analyzing avoidance learning and brain lesion studies shows no evidence they feel pain. Anthropometric assumptions become questionable with greater phylogenetic distance. Understanding invertebrate sentience requires defining the neural circuits for subjective awareness, which depends on observer neural networks that introspect sensory processing and create predictive internal models. An algorithm using parallel observer networks generates multiple awareness levels; human cortical regions match its predicted circuitry for pain awareness, but cephalopod brains lack the necessary neural architecture. Thus, no compelling evidence indicates cephalopods feel pain.

Study at a glance

Abstract

There is compelling evidence that the "what it feels like" subjective experience of sensory stimuli arises in the cerebral cortex in both humans as well as mammalian experimental animal models. Humans are alone in their ability to verbally communicate their experience of the external environment. In other species, sensory awareness is extrapolated on the basis of behavioral indicators. For instance, cephalopods have been claimed to be sentient on the basis of their complex behavior and anecdotal reports of human-like intelligence. We have interrogated the findings of avoidance learning behavioral paradigms and classical brain lesion studies and conclude that there is no evidence for cephalopods feeling pain. This analysis highlighted the questionable nature of anthropometric assumptions about sensory experience with increased phylogenetic distance from humans. We contend that understanding whether invertebrates such as molluscs are sentient should first begin with defining the computational processes and neural circuitries underpinning subjective awareness. Using fundamental design principles, we advance the notion that subjective awareness is dependent on observer neural networks (networks that in some sense introspect the neural processing generating neural representations of sensory stimuli). This introspective process allows the observer network to create an internal model that predicts the neural processing taking place in the network being surveyed. Predictions arising from the internal model form the basis of a rudimentary form of awareness. We develop an algorithm built on parallel observer networks that generates multiple levels of sensory awareness. A network of cortical regions in the human brain has the appropriate functional properties and neural interconnectivity that is consistent with the predicted circuitry of the algorithm generating pain awareness. By contrast, the cephalopod brain lacks the necessary neural circuitry to implement such an algorithm. In conclusion, we find no compelling behavioral, functional, or neuroanatomical evidence to indicate that cephalopods feel pain.