The OB is a troublesome structure, one that does not scale predictably with the rest of the brain, regardless of taxonomic level of analysis, whether order, family, species, or even individual (Finlay et al., 2011). At present, there is no accepted functional hypothesis to explain this pattern of variation. The OS hypothesis offers a possible solution to this problem by proposing that olfaction evolved for the primary purpose of navigating in a chemical world. From this beginning, I propose that it developed specializations not just for the discrimination of odorants but for organizing the stimuli into functional associative memory structures. I suggest that olfactory percepts may bear evidence that this organization is a parallel map structure.
If the OS hypothesis is correct, the implications are profound. First, the primary function of olfaction would be navigation and its organization explained not by its ability to discriminate but to map odorants in space. Second, the OS system would represent the first and primary driving force in the evolution of associative learning, instantiated by the hippocampus in vertebrates and the mushroom body in arthropods and other protostomes. Not least, the hypothesis lays out a broad research program in “cognitive evo devo,” an enterprise to identify the primitives of cognition hand-in-hand with the primitives of the nervous system (Jacobs, 2012, Fig. S3). The peculiar properties of olfaction, as an optimal substrate for combinatorial associative learning, may supply a foundation for this enterprise and thereby inform our understanding not just of the limbic system but of the isocortex as well.
The author thanks Georg Striedter, Francisco Ayala, and John Avise for organizing the Sackler Colloquium; Leslie Kay, Randolf Menzel, Rachel Herz, and Françoise Schenk for their insights; Georg Striedter and two anonymous reviewers for comments on the manuscript; and the following for their discussion and contributions: Dan Koditschek, Bob Full, C. J. Taylor, Paul Roosin, April Gornik, Eric Fischl, Barbara Meyer, Tom Cline, Cori Bargmann, Mikel Delgado, Scott Bradley, Zoe Burr, Patrick Slattery, Dillon Niederhut, Katia Altschuller Jacobs, John Kedzie Jacobs, and finally Jeff Bitterman (1921–2011), to whom this work is dedicated. This work was supported by funding from National Science Foundation Electrical, Communications and Cyber Systems Grant 1028319.