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or paired antennae for spatial olfaction (Plotnick et al., 2010). The situation changed dramatically as 2D Precambrian matgrounds transformed to 3D Phanerozoic mixgrounds (Seilacher, 1999). The increasing energy content of prey could have fueled the Cambrian arms race, resulting in ever bigger and more complex predators (Plotnick et al., 2010) and associative learning (Ginsburg and Jablonka, 2010). Nonassociative learning processes, such as habituation, were likely present before the evolution of the brain, even of neurons (Moroz, 2009; Corning et al., 1973). However, it was the challenge of the transition from the peaceful “Garden of Edicara” (Seilacher, 1999) to the Cambrian bloodbath of predator eating predator that probably supplied the selective force necessary for the evolution of the first brains.

In a highly competitive regime, active prey demand active predators. It is possible that the Cambrian arms race began with the evolution of spatial olfaction and the selective advantage this would give mobile predators. Spatial representation therefore would have evolved as a concrete and specific adaptation for this purpose, exapted from the primitive building blocks of chemotaxis and chemoreception. It would function to encode, organize, and predict the locations of prey, first in olfactory space. As the arms race accelerated, predators with new sensory modalities, such as vision, could detect prey hiding in olfactory refugia, such as turbulent eddies (Conover, 2007). Adding visual cues to the olfactory space would create a robust, multisensory BE. This could then be calibrated and anchored to other reliable environmental features, such as benthic algal mats, rock formations, and magnetic fields. At this point in time, the ancestors of deuterostomes and protostomes, using the common genetic toolkit (Tomer et al., 2010), could have diverged in the details of their OS system, according to developmental constraints. However, all would retain the primacy of olfaction, that is, olfactory-guided navigation, as the ancestral function of the forebrain (Jacobs, 2012, Fig. S3), and they would for this reason eventually converge on a similar neuroarchitecture and similar cognitive mechanisms, such as cognitive mapping.

Built on the olfactory integrated map, this forebrain could encode inputs and memories at both global (i.e., BE) and local (i.e., SK) frames of reference. These frames could be used to organize new data by their similarity to old data and to make supracategorical concepts, by linking local neighborhoods via common vectors. Now the forebrain would not only encode and recall data, it could also extract new relationships de novo—relationships, like the cognitive map shortcut, that had not yet been experienced. By making this construction first in olfactory space, then in a multisensory BE, olfaction may have laid the foundation for the evolution of memory organization in the bilaterian brain.



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