Role of ortho‐retronasal olfaction in mammalian cortical evolution

Abstract

Fossils of mammals and their extinct relatives among cynodonts give evidence of correlated transformations affecting olfaction as well as mastication, head movement, and ventilation, and suggest evolutionary coupling of these seemingly separate anatomical regions into a larger integrated system of ortho-retronasal olfaction. Evidence from paleontology and physiology suggests that ortho-retronasal olfaction played a critical role at three stages of mammalian cortical evolution: early mammalian brain development was driven in part by ortho-nasal olfaction; the bauplan for neocortex had higher-level association functions derived from olfactory cortex; and human cortical evolution was enhanced by ortho-retronasal smell.

Functional constraints in the evolution of brain circuits

“…The subplate served as a substrate for thalamic axonal growth in the white matter underlying the cortical plate (Aboitiz et al, 2005 ). In line with this hypothesis, several authors have very recently highlighted striking connectional and functional similarities between the mammalian olfactory cortex and the reptilian dorsal cortex (the latter deriving from the dorsal pallium, and the likely regional homolog of the mammalian isocortex), both exhibiting similar laminar organization and an apparent poor topographic mapping of the sensory surfaces (Fournier et al, 2015 ; Naumann et al, 2015 ; Rowe and Shepherd, 2015 ). This indicates a shared combinatorial and associative array in both structures.…”

“…Some macroscopic features of a primitive telencephalon may help to understand the organization of a very simple ancestral circuit. The rudimentary telencephalon of early amniotes was a quite a small tubular structure (Kielan-Jaworowska et al, 2004 ; Rowe and Shepherd, 2015 ), perhaps more similar in morphology to the telencephalon of present amphibians, who display a very limited degree of radial neuronal migration and a conspicuous tangential arrangement of inputs in the superficial or molecular layer. Furthermore, both within therians (placental and marsupial mammals) and within sauropsids, an increase in complexity can be observed from more basal forms to more derived forms, associated with the development of an embryonic subventricular zone housing intermediate progenitor neurons (Cheung et al, 2010 ).…”

“…Another approach regarding the ancestral circuitry of mammals and sauropsids (in this case, reptiles) has highlighted the similarities in tangential organization of the mammalian isocortex and olfactory cortex, together with that of the reptilian cortical structures (Lynch, 1986 ; Shepherd, 2011 ; Rowe and Shepherd, 2015 ). In this scenario, the isocortex is primarily a tangentially associative network, where afferents were ancestrally located in the superficial marginal zone, running parallel to the cortical surface and contacting several pyramidal cell apical dendrites in tandem.…”

“…Inhibitory interneurons may have served to regulate the oscillatory dynamics of such primordial circuits (Tiesinga and Sejnowski, 2009 ). Accordingly, a rudimentary circuit architecture, organized through input receiving and output sending neurons, with intermediate associative excitatory neurons and inhibitory interneurons providing feedforward and lateral interactions, is very likely to have existed in pallial regions of the ancestral amniote (see also Rowe and Shepherd, 2015 ). It is possible though, like in the reptilian cortex, that input and output neurons were tangentially separated (Dugas-Ford et al, 2012 ).…”

Probing the proboscidea: Lessons from the past

“…1;Elliot Smith, 1903), and fossil fish, amphibian, and reptile species (Case, 1921(Case, , 1928Moodie, 1915aMoodie, ,b, 1920. In the same years, many studies on the endocranial and brain anatomy of fossil mammals, including a hominin, in comparison with their extant relatives (Black, 1915(Black, , 1920Dempster, 1935;Moodie, 1922) were published in JCN, as well as, in more recent years, some of the earliest evolutionary interpretations of structure in the context of systems neuroscience in the pioneering work of Leonard Radinsky (Radinsky, 1968), which recently culminated in a review of olfaction in the evolution of the mammalian cerebral cortex (Rowe and Shepherd, 2015).…”