Spark or Sound: How Two Differing Explanatory Strategies Impact the Debate on the Physical Nature of Neuronal Excitability

Neuronal excitability manifests itself mainly in the form of non-linear, self-regenerative waves of electricity moving along the surface of neuronal axons. These waves are commonly known as action potentials (APs). Theorizing and experimental investigation of the physical and functional characteristics of APs has broadly followed along the lines of the ionic hypothesis and the associated mathematical model introduced by Hodgkin and Huxley (HH). In the current form of this bioelectrical framework, adopted in mainstream physiology and other biological sciences, the axonal membrane is conceptualized as an electronic circuit where electric current is generated and propelled as the result of time-dependent opening and closure of voltage-operated ion channel proteins allowing passive flow of specific ions across and along the membrane powered by their respective electrochemical gradients. Although representing mainstream research, the bioelectric perspective has been criticized for its narrow focus on electrical characteristics of APs, whilst ignoring other physical manifestations of the nerve signal, in particular mechanical and thermal changes coinciding with AP propagation. As an alternative, a thermodynamics-based acoustic theory has been outlined in which all, electric and non-electric, manifestations of the nerve signal are considered as the result of a single density pulse in the axonal membrane carried by a reversible lipid membrane phase transition and momentum conservation. Representing a minority view, however, this unified, thermodynamic perspective on the physical nature of neuronal excitability is largely ignored by representatives of the bioelectric perspective.Here we draw special attention to the philosophical dimension of the communication failure between the two communities of scientists. We argue that adherents of the bioelectric perspective favor a mechanist-type of explanation, whilst supporters of the thermodynamic perspective are committed to so-called covering-law types of explanation. We conclude that it is this, thus far unrecognized, philosophical rift, rather than specific scientific differences of opinion that blocks fruitful interdisciplinary cooperation necessary for building a comprehensive, fully integrated, notion of the physical nature of neuronal excitability. Suggestions of how to bridge this conceptual gap are formulated.