... In 1995, Barbara Finlay and Richard Darlington launched a series of studies that supplied an answer to the fundamental question of why sizes of brain regions vary (Finlay and ... , 1995). Proposed initially for mammals but extended to basal vertebrates (e.g., sharks) and evolution by artificial selection (e.g., domestication), it supplied the missing link between the constraints of development and allometry. The & ... important exception: the olfactory bulb (OB). The size of this forebrain structure, within species, order, or class, does not scale with the rest, and indeed the entire olfactory limbic system (LI), including the hippocampus and amygdala, does not conform to this otherwise universal scaling law (...

... much selection for olfactory variability, but rather selection for tighter coupling of the other sensory systems that must share thalamic projections and neocortical representations.” I would like to propose instead that such selection for olfactory variability exists. The commonly conceived ... for olfaction is the ability to detect and discriminate odorants (Bargmann, 2006; Arzi and Sobel, 2011; Murthy, 2011). A second function, spatial orientation to odorants, is seen as an application of olfactory discrimination. Reversing the ... of these two functions turns many assumptions and interpretations of olfaction on their heads. What I will call the olfactory spatial (OS) hypothesis offers a unique explanation for the independent ... of the vertebrate OB: that the scaling reflects directional selection on animals to decode and map patterns of odorants for the purpose of spatial navigation....

... CONVERGENCE IN OLFACTORY SYSTEM STRUCTURE AND FUNCTION...

... The need to orient in space to maximize fitness by acquiring resources and avoiding competition and predation is universal. Indeed it is a defining archetype of what it means to be an animal, most of which are mobile. Olfaction is also universal: &...

... Not only do all animals use chemical stimuli, but they do so by using similar mechanisms (Ache and Young, 2005; Bargmann, 2006; Jacobs, 2012, Fig. S1). Eisthen documents four convergences in the olfactory system in insects, crustaceans, nematodes, ... , and vertebrates: odorant binding proteins in the fluid overlying olfactory receptor (OR) neurons, G protein-coupled receptors as odorant receptors, a two- ... pathway in the transduction of odorant signals, and the presence of glomerular neuropils in the first central target of the axons of OR cells (Eisthen, 2002)....

... Such structural similarities in olfactory systems remain a remarkable and somewhat mysterious phenomenon. The olfactory system presents other problems: OR projections segregate and project to receptor-specific glomeruli, ...

... Thus, the study of olfaction is a world of paradoxes: the independent scaling of the OB, the function of convergent neuro-architectures, and the diversity of OR genes. However, perhaps these paradoxes arise from the assumption that the primary function is discrimination. If instead the OS ... is correct, the structural similarities may be explained by convergent cognitive processes for spatial navigation. Likewise, variability in OB size and OR gene number could reflect the species’ use of odorants in spatial navigation. To explore this proposal, first it is necessary to consider ...

... By its physical properties, the chemical world must be encoded differently. As Bargmann (2006) concluded, “the visual system and auditory system are stable because light and sound are immutable physical entities. By contrast, the olfactory system, like the immune system, tracks ... moving world of cues generated by other organisms, and must constantly generate, test, and discard receptor genes and coding strategies over evolutionary time.” Olfaction’s genius for tracking moving targets has important implications. As Osorio et al. ( ... ) concluded: “the mammalian neocortex with its protean powers has evolved from the olfactory forebrain of primitive vertebrates [Sarnat and Netsky, 1981]. Perhaps...

... because olfaction demands a neural architecture preadapted to learning complex input patterns.”...

... There is a rich literature on olfactory perception in humans and other animals, including insects, crustaceans, and rodents (Wilson and Stevenson, 2006). A primary finding is that the percept of an odorant is nonlinearly intensity dependent. Low and high concentrations of the same ... can be perceived as dissimilar and unrelated (Wilson and Stevenson, 2006, table 4.1). A second finding is that an odorant mixture can be perceived as a mixture of its elemental components (i.e., individual ... ) or as a synthetic odor object, which cannot be decomposed. Studies pitting different histories and rewards for different configurations, both in invertebrate and vertebrate taxa, demonstrate that the ability to switch from the elemental to the ... percept is widespread (Wilson and Stevenson, 2006). The mechanism for this allocation of perception and attention is not yet understood, however (Kay et al., 2005; Frederick et al., 2009)....

... FIGURE 12.1 Schematic predictions of the spatial olfaction hypothesis. A hypothetical orthogonal grid created by plumes from two odorants, A and B, which increase in concentration from one to three arbitrary units. With increasing intensity, there is a qualitative shift in percept (indicated ...

... by this principle into local areas of odorant mixtures, which herein will be called neighborhoods. A neighborhood organization could be used to learn the geometrical relationships among odorants, that is, the olfactory space, which is a mental map of the spatial relationships among odorant ...

.... 12.2). Now, in addition to the low-resolution neighborhoods, the olfactory space could also have high-resolution locations. These synthetic object landmarks could be associated with a neighborhood as well as with other objects in the same neighborhood....

... Such an olfactory space would allow a navigator to extract new information from learned odorants. Knowing its speed and rate of sampling, a navigator could extrapolate into the future, predicting the percept farther up the gradient, that is, both in space and time. If ...

... FIGURE 12.2 Schematic predictions of the spatial olfaction hypothesis. The distributions of synthetic odor objects are landmarks in a dynamic olfactory space. (A) Encoding of odorant ratios as synthetic odor object percepts. (B) Synthetic objects occur at known locations, ... defined by odorant ratios, and therefore are landmarks in olfactory space. (C) The coordinate of a synthetic object can therefore be computed from its elemental components. The coordinate system ... (u, v) are adopted from meteorology, where u designates streamwise direction and v crosswind direction (Conover, 2007)....

... neighborhoods and/or synthetic objects. These two mapping systems for olfactory space would differ in other ways as well. The neighborhood system could be used to ... form a low-resolution map, on which the navigator deduces direction and general location from changes in intensity and the order of neighborhoods. The synthetic object map would have higher spatial resolution but would also be slower to construct, with the navigator ... relationships among these synthetic objects. These new relationships could be used to simulate trajectories in physical space linking two locations and they could also be used to create higher-level categorizations of the original synthetic objects....

... Obviously, the question of turbulence looms large, yet animals are highly adapted to decode turbulence (Atema, 1996; Koehl, 2006; Gardiner and Atema, 2007), and odorant distributions may be stable, even in air (Wallraff, 2004). Olfactory systems are also notably integrated with ... systems to measure turbulence, such as vibrissae (mammals), antennae (insects), antennules (crustaceans), and lateral lines (fish) (Dehnhardt and Mauck, 2008; Thewissen and Nummela, 2008). Thus, theoretically animals could collect the necessary mechanosensory data to decode the spatial ...

... I propose it for two reasons: first, it is a hypothesis that incorporates the known oddities of olfactory perception. Second, Françoise Schenk and I have proposed a similar parallel structure for the hippocampal cognitive map (Jacobs and Schenk, 2003). If the OS hypothesis is correct, it ...

... The parallel map theory (PMT), illustrated in Fig. 12.3, was first proposed as a cognitive mechanism for true navigation in vertebrates, and second, to explain the evolution and function of the mammalian hippocampus (Jacobs, 2003, 2006; Jacobs and Schenk, 2003). In PMT, the bearing map (BE)...

... FIGURE 12.3 The parallel map theory of navigation, illustrated with real-world examples and with abstract schematics. (A) BE: arrows indicate the vector information extracted from two directional cues, a distant mountain and the polarized ... of an oblong body of water. The schematic shows the abstract bicoordinate map and movements of a navigator. (B) SKs: shapes outline three unique posi-tional cues. The schematic represents three SKs near the home base of the ...

... space, comparing successive samples along gradients of graded stimuli, that is, directional cues. With just a BE, a navigator can extrapolate and predict a future location, even in unexplored territory. In mammals, the proposed neural substrate of the BE is the dentate gyrus. In contrast, the ...

... landmarks; Fig. 12.3B). The SK encodes the topological arrangement of positional cues to derive relational and temporal order information, and its proposed substrate is the CA1 subfield of Ammon’s horn. The BE and SK are brought into register on the integrated map, subserved by ... CA3, in which objects on the SK are recoded in BE coordinates (Fig. 12.3C). In concordance with PMT predictions, Manahan-Vaughn and coworkers have recently shown that directional cues facilitate long-term depression (LTD) in the dentate gyrus whereas positional cues facilitate LTD ... CA1, and both cue types facilitate LTD in CA3 (Kemp and Manahan-Vaughan, 2008; Hagena and Manahan-Vaughan, 2011)....

... As with olfactory space, the hippocampal parallel map provides a powerful tool for mapping spatial relations, with global generalization (i.e., BE) and local specificity (i.e., SK), and the ability to move between these representations in the fully encoded integrated map. In olfactory space, the map ... based on chemosensory and mechanosensory inputs. In the BE, chemosensory, mechanosensory inputs as well as other sensory (e.g., visual, auditory, electrosensory) inputs are ...

... The close relationship between the olfactory system and the hippocampus in mammals has long been recognized; indeed, olfaction was once believed to be the primary function of the hippocampus (Sarnat and ... ). Thus, the OS hypothesis is not necessarily radical or new, but is instead the revisiting of an old idea in light of new evidence about olfaction and new insights from evolutionary neuroscience....

... If the function of olfaction is navigation, perhaps using a parallel map geometry, olfactory structure size should scale with navigational demand. At the same time, the impairment of olfactory structures should impair olfactory discrimination and olfactory navigation. Discrimination of odorants ... a separate function of the olfactory system and a component of navigation. It is possible and even likely that these two functions, discrimination and navigation, will be found to segregate in olfactory systems by anatomical locus, physiological mechanism, and/or genetic encoding. However, at ... , the genetic code for olfactory perception remains unbroken, and most olfaction research focuses on the discrimination of static odorants, not spatial orientation to changing odorant distributions (Arzi and Sobel, ... ; Murthy, 2011). What is needed to test the OS hypothesis are behavioral and physiological disassociations of the two functions...

... lacking. There is not sufficient space here to review the pertinent scientific literatures (e.g., physiology of animal olfaction, the hippocampus and spatial navigation). Instead, the studies most relevant to the question of the scaling of the OB in vertebrates are mentioned. Even in vertebrates, ... of the vomeronasal and accessory olfactory systems, or the question of patterns in OR gene number, cannot be assessed here, although an OS-based analysis of these ... and gene families is under way....

... maps of odorants, the absolute size of the OB should covary with the need to make maps of high spatial resolution. It should not scale with demand for the fine discrimination of odorants, for example, those used in social interactions or discriminating foods by taste. Such discrimination should ... to the experiences of the individual (Beshel et al., 2007; Kay et al., 2009). Therefore, absolute OB size should be predicted by navigational demand. Further, it should be that form of navigation subserved by the BE: first creating vectors from graded stimuli, then combining these into ... maps for short-cutting and extrapolation (Fig. 12.3). Thus, the OS hypothesis also predicts that olfactory impairment should impair the BE, and thereby the integrated map and cognitive mapping. Evidence across vertebrates is reviewed later, with a short foray into arthropods, and the chapter ...

... Although the primacy of olfactory inputs for mammals is widely accepted (Davis and Eichenbaum, 1991), there are surprisingly few experimental studies of the use of air- or waterborne odorants for navigation. Studies of olfactory ... by rescue dogs are one exception but are few in number (Hepper and Wells, 2005). Most studies are those of laboratory rats orienting to discrete sources of odors in a laboratory maze. Under these conditions, rats ... track an odor trail to a goal (Wallace et al., 2002), even underwater (Means et al., 1992). They can also orient to an array of odorant sources and will do so in the absence of visual cues (Lavenex and Schenk, 1996). As they mature, however, rats require visual cues to orient in a lighted maze, ... of learned olfactory cues. This accords with PMT, which predicts an ontogenetic change from the gradient-based BE to the object-based SK (Jacobs and Schenk, 2003; Rossier and Schenk, 2003). In the laboratory, such effects might be stronger if the static atmospheric conditions could be redesigned ...

... of olfaction via peripheral anosmia showed no impairment, relying instead on visual cues. In contrast, rats with olfactory bulbectomy showed a severe and long-lasting (6 wk) impairment (van Rijzingen et al., 1995). This suggests that the olfactory system acts as a necessary scaffold for visual ... , that is, the same scaffolding function originally proposed for the BE (Jacobs and Schenk, 2003). It illustrates a basic tenet of the OS hypothesis: that the function of the OB is spatial navigation, not simply odorant ...

... which showed that relative OB size increased with home range size. More recently, Reep et al. (2007) examined the relationship between isocortex (IS) and the LI (OB, olfactory cortex, subicular cortices, hippocampus, septum) in diverse mammalian groups (carnivores, ungulates, xenarthrans, and sirenians) ... that of the hippocampus, but was inversely related to the absolute size of the IS, as was the size of the LI to the IS. However, when comparing LI and IS in relation to “brain core” volume [defined as striatum, diencephalon, medulla, and mesencephalon (Finlay et al., 2001)], different ... emerged. These included high IS plus high LI in carnivores, high IS plus low LI in simians, low IS plus low LI in microbats, and low IS plus high LI in insectivores. Megabats (pteropids) had intermediate IS plus intermediate LI, and ungulates and marine mammals had intermediate ... and low LI (Jacobs, 2012, Fig. S2). The authors made the case that such patterns emerged from developmental constraints (Reep et al., 2007)....

... The OS hypothesis would predict that the size of the LI should increase in predators whose prey are predictable in time and space and who can be tracked by their odorants. Likewise, the size of the multisensory IS might be related to planning ability, with an IS increasing in size ... prey are predictable but wily and difficult to capture. To apply this corollary of the OS hypothesis, I divide the world into foragers that are “detectors” or “ ... .” Detectors eat prey that are easy to find (e.g., grasses) or impossible to find (e.g., aerial insect clouds) and should thus not invest in brain space for a spatial tracking system. Predictors eat prey the locations...

... of which can be predicted with sufficient data and should therefore invest as needed in a spatial tracking system, whether olfactory (i.e., LI) or not....

... confirmed in the results of Reep et al. (2007): low LI plus low IS should be found in detectors. Indeed, this is the pattern for grazing ungulates and sirenians and the echolocating microbats, many of which feed on aerial insects (Jacobs, 2012, Fig. S2). In contrast, the ancestral mammal was ... predator (Conover, 2007). This should be reflected in a predictor pattern of high LI plus low IS. This pattern is indeed seen in insectivores and prosimians (Jacobs, 2012, Fig. S2). If, however, predictors also face the challenge of eating prey that can map and avoid their movements (Conover, ...

... The pinnipeds present a quandary at first, as they are carnivores, and therefore should be predictors, with a high IS, whereas theirs is only intermediate. Olfaction must be jettisoned, however, in terrestrial species ... return to the water, because of its incompatibility with respiration (Thewissen and Nummela, 2008). However, as Reep et al. (2007) conclude, “the reduction of volume in the hippocampus, which gets only a minor olfactory ...

... sea floor for stationary prey, and others use the vibrissae to track the hydrodynamic trails of prey such as fish (Dehnhardt and Mauck, 2008). Schools of highly mobile prey may represent an ephemeral food source that is easier to find than predict in the absence of olfaction, the main sensory ...

... Chiropterans are interesting because of the divergence in predatory behavior between the microbats, specialized for echolocation, and megabats (pteropids), who use simple or no echolocation, relying on vision and olfaction to detect prey, for example, fruit. As predicted by the OS ...

... Hippocampal plasticity, which should also reflect OS function, also differs between microbats and megabats. Adult neurogenesis is found widely in animals but in vertebrates it is always found in the OB and the medial pallium (hippocampus in ... with spatial exploration (Lledo et al., 2006). This vertebrate pattern of neurogenesis suggests its ancestral function was related to mapping and encoding the spatial distributions of novel odorants (Jacobs and Schenk, 2003)....

..., microbats present the exception to this vertebrate rule, despite showing normal hippocampal function, including hippocampal place cells (Ulanovsky and Moss, 2007). A study of 12 microbat species found no hippocampal neurogenesis in nine species and greatly reduced levels in the others; measures of ... OS interpretation of this labile pattern is that detector microbats, relying heavily on spatial audition, have fundamentally replaced their OS system and now require less plasticity in BE components (e.g., OB, dentate gyrus). This hypothesis is supported by new data from the same group on megabats, ... appear to be the predictors of the chiropterans. As with fruit-eating simians, these bats forage for a food resource that can be tracked in space and time. Cognitive mapping has also been demonstrated in a wild megabat, the Egyptian fruit bat (Tsoar et al., 2011), as have medial entorhinal grid ... intermediate LI/intermediate IS pattern (Reep et al., 2007). Further evidence comes from a comparative study of relative OB size, hippocampal size, and wing size in bats (Safi and Dechmann, 2005), in which wing size is a proxy for navigational ability, increasing in cluttered environments. Wing size ... with relative hippocampal size in microbats, but was unrelated to relative OB size. In contrast, relative OB size and wing size...

... were positively correlated in megabats (Safi and Dechmann, 2005), again supporting the hypothesis that megabats are olfactory predictors whereas microbats are auditory detectors....

... In summary, scaling analyses of mammalian LI and IS show distinct patterns of covariation (Reep et al., 2007). The OS hypothesis offers a unified explanation for these patterns, by proposing an ... in OS structures in predictors and a decrease in detectors. Decreases in LI size occur with shifts in sensory ecology (e.g., pinniped return to water, primate shift to diurnal ... , microchiropteran shift to aerial echolocator). Likewise, when prey are mobile and encephalized, the predator’s need to predict their movements drives an increased investment in LI and IS....

... study that used high-resolution X-ray computed tomography was able to identify three transitions in which early Jurassic mammals showed a significant and sudden increase in absolute brain size (Rowe et al., 2011). At all three transitions, the increase in brain size could be ascribed primarily to ... in absolute OB and olfactory cortex size. The authors conclude, “but at its start, the brain in the ancestral mammal differed from even its closest extinct ... specifically in its degree of high-resolution olfaction, as it exploited a world of information dominated to an unprecedented degree by odors and scents” (Rowe et al., 2011). The alternative OS explanation is that this is evidence of mammals evolving more sophisticated spatial cognitive ... , with increases in OB size accompanied by increases in hippocampal size and olfactory cortex size with eventual increases in IS. The mammalian brain may thus have evolved first via mosaic evolution for olfaction, then via ...

... studies of the relatives of modern birds, the theropod dinosaurs, have shown that OB size was larger in active predators, relative to cerebral size and corrected for phylogenetic independence. Moreover, an analysis of phylogenetic trends showed that the direct ancestors of modern birds did not show ... ). This implies that carnivorous predators, whether diurnal theropods or nocturnal terrestrial mammals (Gittleman, 1991), are olfactory predictors, and require an enhanced OS system to track mobile, dispersed prey....

... species still require olfaction for spatial navigation (DeBose and Nevitt, 2008). For example, procellariform (tube-nosed) seabirds, the “fishes of the air,” use olfaction to track unpredictable ... nocturnal species, there is an increase in relative OB size in birds; this has evolved independently multiple times in modern birds (Healy and Guilford, 1990)....

... its ability to home from unknown locales for many centuries. Compared with nonhoming strains, the homing pigeon has in absolute size both a larger OB and a larger hippocampus (Rehkämper et al., 1988). Originally proposed by Papi and later developed by Wallraff, it has now been well established ... olfaction for navigation. As reviewed by Wallraff (2005), the olfactory navigation hypothesis has been widely tested, across different laboratories and continents, by using a variety of behavioral and physiological manipulations. Physiological impairments have included blocking nostrils, ... the olfactory epithelium, transecting the olfactory nerve, and ablating the piriform cortex. Such procedures impair navigation even when visual cues are available (Wallraff, 2005). Although homing pigeons also ... by using geomagnetic fields (Wiltschko and Wiltschko, 2005), this input appears to be weighted less heavily than olfaction in experimentally displaced homing pigeons (Gagliardo et al., 2006) ... in migrating songbirds (Holland et al., 2009). Such experimental evidence for the primacy of olfactory inputs in navigation, across multiple diurnal bird orders, lends strong ...

... Chemical stimuli play a pivotal role in the behavior of reptiles, but we lack studies addressing the covariation of absolute OB size and navigational ability. There is a correlation, however, between relative medial cortex (medial pallium homologue) size and active predation, whereby ... cortex size is larger in active than in sit-and-wait lizards (Day et al., 1999). In snakes, rattlesnakes forced to navigate after experimental displacement have an increased volume of medial, but ...

... has been well studied in several species of turtles. The semiaquatic red slider turtle can orient by using true spatial strategies in the laboratory, and this ability is impaired after lesions of the medial cortex (López et al., 2003). Sea turtles orient to magnetic fields and to a...

... map-like representation of such fields, adjusting their heading in response to simulated ocean locations in the laboratory (Lohmann and Lohmann, 1996; Putman et al., 2011). In the field, sea turtles may also use windborne odorants to locate their natal beach by orienting upwind (Hays ... al., 2003), but as secondarily aquatic vertebrates, sea turtles have a smaller relative OB size and fewer OR genes than land turtles (Vieyra, 2011). Thus, living and extinct reptiles appear to show predictable heterogeneity and plasticity in the components of the OS system, ...

.... Across all spatial scales, fish orient to odorants by calibrating odor sampling to their lateral line perception of hydrodynamic trails (DeBose and Nevitt, 2008). The smooth dogfish not only requires intact lateral lines to use odorant sources for orientation, but uses the internostril time delay ... determine its location relative to the plume (Gardiner and Atema, 2010). Experimental studies of navigation in goldfish demonstrate that it is mediated by the medial pallium homologue in teleosts, the ... ventral region of the telencephalon (Salas et al., 2006). As in birds and mammals (Jacobs, 2009), mating system predicts sex differences in the relative size of this region (Costa et al., 2011)....

... of brain scaling in cartilaginous fish has shown that, as in mammals, OB size variance is unrelated to phylogeny. Instead, as in the analysis of LI and IS in mammals (Reep et al., 2007), the patterns of absolute telencephalon and OB size admitted of no ready explanation (Yopak et al., 2010). However, ... of the observed patterns may be addressed with the OS hypothesis. For example, telencephalon and OB absolute size are larger in deep-water than reef-associated species. The shark in deep water may face the same challenge as a nocturnal carnivore ... land. In both cases, the predator must predict prey movements and locations by using an olfactory BE, as the positional cues for the SK are absent (deep water) or ambiguous (low light). Therefore, sharks in deep ...

... similar highly conserved gene networks are found in the vertebrate pallium and the mushroom body of a marine annelid. They conclude that this ancestral gene network could underlie the evolution and development of complex brains ... vertebrates and annelids (Tomer et al., 2010)....

... mapping. Orienting to laboratory simulations of local geomagnetic fields, Caribbean spiny lobsters can accurately orient toward their home den (Boles and Lohmann, 2003). Studies of cognitive mapping in honeybees by Menzel et al. (2005, 2012) have shown that displaced honeybees can initiate homing ... from any location within the explored area along novel shortcuts and can choose among at least three goals. Honeybees can also shortcut between vectors learned from exploration and those learned from the waggle dance (...

... Applying the same OS logic to arthropods, navigational demand should predict larger investment in the olfactory glomerular structure (i.e., OB in vertebrates) and the multisensory associational structure (i.e., ... ). In insects, this is the antennal lobe and mushroom body (Strausfeld et al., 2009; Strausfeld, 2012). Antennal lobe size should covary with the use of olfaction in navigation, whereas the ... mushroom body, encoding visual, mechanosensory, and olfactory information, should covary with antennal lobe size when navigation is primarily in relation to odorants. There are some indications that ... could be the case. As in pinnipeds and sea turtles, secondarily aquatic insects, such as hemipteran water striders, have reduced antennal lobes but large mushroom bodies. Like audition in ... that causes them to be retained when olfaction is lost” (Strausfeld et al., 2009) may therefore have the same answer as in mammals. To understand these potential adaptive radiations in olfactory systems across such diverse taxa, I next consider how the OS system might have evolved in their ...

... EVOLUTION OF OLFACTION AND EVOLUTION OF NAVIGATION...

... Molecular clock and geological evidence agree that the history of bilateria began in the Ediacaran Period, 635 to 542 Myr ago (Peterson et al., 2008). This fauna lived ... or just below the tough, erosion-resistant biomat surface, supporting lifestyles such as mat encrusters, mat scratchers, mat stickers, and undermat miners (Seilacher, 1999). There was no evidence for spatial sensory organs, such as paired eyes for spatial vision,...

... 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 ...

... 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 ... 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, ... , and predict the locations of prey, first in olfactory space. As the arms race accelerated, predators with new sensory modalities, such as vision, could ... 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 ... 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 ... , 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 ... , 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. ...

... 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 ...

... 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 ... 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 ... 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 ... 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 ... 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 ... , Communications and Cyber Systems Grant 1028319....