Figure - available from: Frontiers in Neuroscience
This content is subject to copyright.
Phylogeny of fossil mammals. Critical phylogenetic nodes are shown in numbers. The inset provides a summary diagram of the different clades. Cynodonts are shown in purple. Node (1, blue) mammaliamorphs, a group of advanced cynodonts; (2, also blue) mammaliaforms. The common ancestor of modern mammals (crown mammals) is shown at the base of the green tree. This line gives rise to most mesozoic mammals (3, yellow) and to monotremes (4, green). The common ancestor of therians (marsupials and placentals) stays at the base of (5, blue) marsupials or metatherians and (6, red) placentals or eutherians. Note the dramatic extinction of mammalian lineages at the end of the Cretaceous, concomitant with the extinction of the dinosaurs. With permission from Luo (2007).
Source publication
There are remarkable similarities between the brains of mammals and birds in terms of microcircuit architecture, despite obvious differences in gross morphology and development. While in reptiles and birds the most expanding component (the dorsal ventricular ridge) displays an overall nuclear shape and derives from the lateral and ventral pallium,...
Similar publications
The representation of multiple acoustic sources in a virtual image of the field of audition based on binaural synthetic-aperture computation (SAC) is described through use of simulated inter-aural time delay (ITD) data. Directions to the acoustic sources may be extracted from the image. ITDs for multiple acoustic sources at an effective instant in...
The ability of robots to listen to several things at once with their own 'ears', that is, robot audition, is an important factor in improving interaction and symbiosis between humans and robots. The critical issue in robot audition is real-time processing and robustness against noisy environments with high flexibility to support various kinds of ro...
Background:
We report a case of an elderly patient who was diagnosed with lateral atlantoaxial subluxation with type II odontoid fracture, an extremely uncommon upper cervical spine injury that has not been previously reported in the literature to the knowledge of the authors.
Methods:
An 87-year-old male reported to the emergency room following...
INTRO: A Guide to Communication Sciences and Disorders, Third Edition is designed for the undergraduate student with an interest in entering the field of communication sciences and disorders. INTRO is an introduction to the professions of speech-language pathology and audiology and the underlying discipline on which they are based, communication sc...
Reward value guides goal-directed behavior and modulates early sensory processing. Rewarding stimuli are often multisensory but it is not known how reward value is combined across sensory modalities. Here we show that the integration of reward value critically depends on whether the distinct sensory inputs are perceived to emanate from the same mul...
Citations
... It is believed that brains originally evolved to organize the motor response in pursuit of chemical stimuli. Indeed, some of the oldest regions of the mammalian brain, including the hippocampus, seem organized around an axis that processes smells (Jacobs, 2012;Aboitiz and Montiel, 2015). ...
An animal entering a new environment typically faces three challenges: explore the space for resources, memorize their locations, and navigate towards those targets as needed. Here we propose a neural algorithm that can solve all these problems and operates reliably in diverse and complex environments. At its core, the mechanism makes use of a behavioral module common to all motile animals, namely the ability to follow an odor to its source. We show how the brain can learn to generate internal “virtual odors” that guide the animal to any location of interest. This endotaxis algorithm can be implemented with a simple 3-layer neural circuit using only biologically realistic structures and learning rules. Several neural components of this scheme are found in brains from insects to humans. Nature may have evolved a general mechanism for search and navigation on the ancient backbone of chemotaxis.
... B, map of character evolution on the phylogenetic tree illustrating the independent emergence of neocortical DCX + neuron densities in the mammalian species considered. Reproduced with permission from eLife, Elife Sciences Publications (La Rosa et al. 2020a) related to olfaction-mediated goal-directed and navigational behaviors, accompanied by integrated sensory map development, which in turn resulted in developmental changes in the distribution of cells and the formation of circuits in the telencephalon (Aboitiz et al. 2003;Aboitiz and Montiel 2015). Early mammals likely adopted a nocturnal and burrowing lifestyle, utilizing internal cues such as proprioceptive information in conjunction with sensory inputs from the olfactory and somatosensory systems for spatial navigation. ...
... These senses are vital for generating accurate two-dimensional and time-independent spatial maps, providing more detailed information relevant to navigation (Buzsáki 2005;Eichenbaum 2014). Over time, the expanding neocortex played an increasingly prominent role in the formation of multimodal association networks and map-like representations of space (Aboitiz and Montiel 2015). ...
Neuronal plasticity can vary remarkably in its form and degree across animal species. Adult neurogenesis, namely the capacity to produce new neurons from neural stem cells through adulthood, appears widespread in non-mammalian vertebrates, whereas it is reduced in mammals. A growing body of comparative studies also report variation in the occurrence and activity of neural stem cell niches between mammals, with a general trend of reduction from small-brained to large-brained species. Conversely, recent studies have shown that large-brained mammals host large amounts of neurons expressing typical markers of neurogenesis in the absence of cell division. In layer II of the cerebral cortex, populations of prenatally generated, non-dividing neurons continue to express molecules indicative of immaturity throughout life (cortical immature neurons; cINs). After remaining in a dormant state for a very long time, these cINs retain the potential of differentiating into mature neurons that integrate within the preexisting neural circuits. They are restricted to the paleocortex in small-brained rodents, while extending into the widely expanded neocortex of highly gyrencephalic, large-brained species. The current hypothesis is that these populations of non-newly generated “immature” neurons might represent a reservoir of developmentally plastic cells for mammalian species that are characterized by reduced stem cell-driven adult neurogenesis. This indicates that there may be a trade-off between various forms of plasticity that coexist during brain evolution. This balance may be necessary to maintain a “reservoir of plasticity” in brain regions that have distinct roles in species-specific socioecological adaptations, such as the neocortex and olfactory structures.
... Olfactory bulb, cortex, pallial amygdala, and other pallial structures are thought to have evolved as elaborations of the olfactory system, with the addition of more sensory inputs from complex exteroceptors such as mediate vision, audition, proprioception, and taste (Reiner et al., 1998;Redgrave et al., 1999;Smeets et al., 2000;Aboitiz et al., 2003;Grillner et al., 2013;Aboitiz and Montiel, 2015;Jacobs, 2023). Functionally, these structures interact with each other and the subpallial striatum to integrate reward, motivation, affect, and memory to compute incentive for decision making and to place it in physical context with directional information. ...
Nervous systems of vertebrates and invertebrates show a common modular theme in the flow of information for cost-benefit decisions. Sensory inputs are incentivized by integrating stimulus qualities with motivation and memory to affect appetitive state, a system of homeostatic drives, and labelled for directionality. Appetitive state determines action responses from a repertory of possibles and transmits the decision to a premotor system that frames the selected action in motor arousal and appropriate postural and locomotion commands. These commands are then sent to the primary motor pattern generators controlling the motorneurons, with feedback at each stage. In the vertebrates, these stages are mediated by forebrain pallial derivatives for incentive and directionality (olfactory bulb, cerebral cortex, pallial amygdala, etc.) interacting with hypothalamus (homeostasis, motivation, and reward) for action selection in the forebrain basal ganglia, the mid/hindbrain reticular formation as a premotor translator for posture, locomotion, and arousal state, and the spinal cord and cranial nuclei as primary motor pattern generators. Gastropods, like the predatory sea slug Pleurobranchaea californica, show a similar organization but with differences that suggest how complex brains evolved from an ancestral soft-bodied bilaterian along with segmentation, jointed skeletons, and complex exteroceptors. Their premotor feeding network combines functions of hypothalamus and basal ganglia for homeostasis, motivation, presumed reward, and action selection for stimulus approach or avoidance. In Pleurobranchaea, the premotor analogy to the vertebrate reticular formation is the bilateral “A-cluster” of cerebral ganglion neurons that controls posture, locomotion, and serotonergic motor arousal. The A-cluster transmits motor commands to the pedal ganglia analogs of the spinal cord, for primary patterned motor output. Apparent pallial precursors are not immediately evident in Pleurobranchaea’s central nervous system, but a notable candidate is a subepithelial nerve net in the peripheral head region that integrates chemotactile stimuli for incentive and directionality. Evolutionary centralization of its computational functions may have led to the olfaction-derived pallial forebrain in the ancestor’s vertebrate descendants and their analogs in arthropods and annelids.
... The human brain, with its strikingly enormous neocortex dominating the relatively small limbic system, is the product of a disproportionate expansion of the neocortical prefrontal and the parietal association regions, with the vital memory-recoding machinery (including entorhinal cortices and the hippocampus) lagging behind [146,[194][195][196]. This disproportional expansion of the neocortical/limbic region induced by the evolutionary neocortical 'Big Bang' might be a contributing factor in the development of AD in the longer-living, aging brain. ...
... The current enormous 6-layer cortex is the product of a 3-layer reptilian-like brain consisting of periventricular sheets known as medial, dorsal, lateral, and ventral pallia, each with only one layer of pyramidal neurons [177][178][179][180][181]194,197,198]. Between the medial and lateral pallia was a narrow wedge of dorsal neuropil with an immense World-changing future-the enormous human neocortex. ...
... One major brain-altering consequence of avoiding dinosaurs and coping with the lack of oxygen was a large expansion of the olfactory bulbs and the pre-piriform lateral pallium [146,181,194,201,202]. Consequently, the expanding lateral pallium slid over the dorsal pallial wedge to produce a potent double allocortical 'sandwich' with multiple layers of wide-ranging pyramidal neurons. ...
The enormous, 2–3-million-year evolutionary expansion of hominin neocortices to the current enormity enabled humans to take over the planet. However, there appears to have been a glitch, and it occurred without a compensatory expansion of the entorhinal cortical (EC) gateway to the hippocampal memory-encoding system needed to manage the processing of the increasing volume of neocortical data converging on it. The resulting age-dependent connectopathic glitch was unnoticed by the early short-lived populations. It has now surfaced as Alzheimer’s disease (AD) in today’s long-lived populations. With advancing age, processing of the converging neocortical data by the neurons of the relatively small lateral entorhinal cortex (LEC) inflicts persistent strain and high energy costs on these cells. This may result in their hyper-release of harmless Aβ1–42 monomers into the interstitial fluid, where they seed the formation of toxic amyloid-β oligomers (AβOs) that initiate AD. At the core of connectopathic AD are the postsynaptic cellular prion protein (PrPC). Electrostatic binding of the negatively charged AβOs to the positively charged N-terminus of PrPC induces hyperphosphorylation of tau that destroys synapses. The spread of these accumulating AβOs from ground zero is supported by Aβ’s own production mediated by target cells’ Ca2+-sensing receptors (CaSRs). These data suggest that an early administration of a strongly positively charged, AβOs-interacting peptide or protein, plus an inhibitor of CaSR, might be an effective AD-arresting therapeutic combination.
... This layer of cells represents the animal's location. 1 Each neuron in this population has a small response field within the environment. The neuron fires when the animal enters that response field. ...
... From the state of the network (M and G) we compute the goal signal E yj at every node j. When the agent is at node j it chooses among the neighbor nodes the one with the highest sum of goal signal and noise (1). Based on the goal signal E yj and the noise ϵ one can compute the probability for each such possible step from j. ...
An animal entering a new environment typically faces three challenges: explore the space for resources, memorize their locations, and navigate towards those targets as needed. Experimental work on exploration, mapping, and navigation has mostly focused on simple environments – such as an open arena [55], a pond [35], or a desert [37] – and much has been learned about neural signals in diverse brain areas under these conditions [11, 45]. However, many natural environments are highly complex, such as a system of burrows, or of intersecting paths through the underbrush. The same applies to many cognitive tasks, that typically allow only a limited set of actions at any given stage in the process. Here we propose an algorithm that learns the structure of a complex environment, discovers useful targets during exploration, and navigates back to those targets by the shortest path. It makes use of a behavioral module common to all motile animals, namely the ability to follow an odor to its source [4]. We show how the brain can learn to generate internal “virtual odors” that guide the animal to any location of interest. This endotaxis algorithm can be implemented with a simple 3-layer neural circuit using only biologically realistic structures and learning rules. Several neural components of this scheme are found in brains from insects to humans. Nature may have evolved a general mechanism for search and navigation on the ancient backbone of chemotaxis.
... It is believed that brains originally evolved to organize the motor response in pursuit of chemical stimuli. Indeed, some of the oldest regions of the mammalian brain, including the hippocampus, seem organized around an axis that processes smells (Jacobs, 2012;Aboitiz and Montiel, 2015). ...
An animal entering a new environment typically faces three challenges: explore the space for resources, memorize their locations, and navigate towards those targets as needed. Experimental work on exploration, mapping, and navigation has mostly focused on simple environments – such as an open arena [55], a pond [35], or a desert [37] – and much has been learned about neural signals in diverse brain areas under these conditions [11, 45]. However, many natural environments are highly complex, such as a system of burrows, or of intersecting paths through the underbrush. The same applies to many cognitive tasks, that typically allow only a limited set of actions at any given stage in the process. Here we propose an algorithm that learns the structure of a complex environment, discovers useful targets during exploration, and navigates back to those targets by the shortest path. It makes use of a behavioral module common to all motile animals, namely the ability to follow an odor to its source [4]. We show how the brain can learn to generate internal “virtual odors” that guide the animal to any location of interest. This endotaxis algorithm can be implemented with a simple 3-layer neural circuit using only biologically realistic structures and learning rules. Several neural components of this scheme are found in brains from insects to humans. Nature may have evolved a general mechanism for search and navigation on the ancient backbone of chemotaxis.
... In the animal kingdom, the sense of smell still plays a vital role in navigation and spatial orientation. A hippocampal region associated with spatial orientation and an olfactory-hippocampal projection is preserved in some groups of animals, such as rodents, in which the olfactory system is connected to the hippocampus through the entorhinal cortex [16]. With regard to the spatial organization, young rats are better at using the sense of smell but are less efficient at using visual information as opposed to older rats, although there is still an interaction between different sensory modalities [17]. ...
Many studies have focused on navigation, spatial skills, and the olfactory system in comparative models, including those concerning the relationship between them and physical activity. Although the results are often in contrast with each other, it is assumed that physical activity can affect cognition in different ways—both indirectly and through a certain influence on some brain structures. In contrast, there is little research that focuses on the relationship between spatial abilities and olfactory abilities in humans. This research aimed to evaluate and compare the performance in working memory tasks of athletes and non-athletes who require good visual–spatial navigation, olfactory–spatial navigation, and olfactory–semantic skills. The study involved 236 participants (83 athletes) between the ages of 18 and 40. All subjects were matched by age or sex. The standard Corsi Block Tapping Test (CBTT) was administrated to investigate the visual-spatial memory. Olfactory–spatial navigation and olfactory–semantic skills were assessed with two modified versions of CBTT: Olfactory CBTT (OCBTT) and Semantic–Olfactory CBTT (SOCBTT) respectively. The results show differences between the CORSI conditions in direction of a poor performance for athletes. A gender effect in favor of men was also found, particularly in the classic version of the CBTT. Both groups performed better in the classic version of the CBTT than OCBTT and SOCBTT. The mean of SOCBTT results is markedly lower, perhaps due to the different information processing systems needed to perform this kind of task. It is possible to explain how sports practice can affect tasks that require spatial skills and olfactory perception differently, thus supporting new hypotheses and opening new scientific horizons.
... The skull endocasts of successive early mammals show continuous size increase in olfactory bulbs [117,121] correlated with increased telencephalic and cerebellar size [122,123]. The improvement of olfaction imposed high demands in anatomic and computational resources for creating and memorizing precise navigational maps, to find foods, recognizing dangers, friends and relatives, and is currently considered capital for the development of the distinctive mammalian isocortex [124,125]. As Rowe [117] summarized, "the ancestral mammal was a tiny terrestrial creature that scurried and climbed over complex three-dimensional surfaces of its microhabitat, carrying its young in a pouch, and nurturing them with milk and warmth until they were self-sufficient in feeding and could regulate their own body temperatures. ...
Mammals evolved from small-sized reptiles that developed endothermic metabolism.
This allowed filling the nocturnal niche. They traded-off visual acuity for sensitivity but became
defenseless against the dangerous daylight. To avoid such danger, they rested with closed eyes in
lightproof burrows during light-time. This was the birth of the mammalian sleep, the main finding of
this report. Improved audition and olfaction counterweighed the visual impairments and facilitated
the cortical development. This process is called “The Nocturnal Evolutionary Bottleneck”. Premammals
were nocturnal until the Cretacic-Paleogene extinction of dinosaurs. Some early mammals
returned to diurnal activity, and this allowed the high variability in sleeping patterns observed today.
The traits of Waking Idleness are almost identical to those of behavioral sleep, including homeostatic
regulation. This is another important finding of this report. In summary, behavioral sleep seems to be
an upgrade ofWaking Idleness Indeed, the trait that never fails to show is quiescence. We conclude
that the main function of sleep consists in guaranteeing it during a part of the daily cycle.
... Notwithstanding caveats of translating inferences across species (Bonfanti and Amrein, 2018), one could hypothesize that integration of dormant precursors in different areas of the neocortex also accounts for improved multimodal sensory processing along adulthood in gyrencephalic mammals (Aboitiz and Montiel, 2015;La Rosa et al., 2020). Humans may even use dormant precursors to better manage their highly variable ecosystems, not only in terms of time and space, but also culture, language, and patterns of social interactions. ...
Dormant non-proliferative neuronal precursors (dormant precursors) are a unique type of undifferentiated neuron, found in the adult brain of several mammalian species, including humans. Dormant precursors are fundamentally different from canonical neurogenic-niche progenitors as they are generated exquisitely during the embryonic development and maintain a state of protracted postmitotic immaturity lasting up to several decades after birth. Thus, dormant precursors are not pluripotent progenitors, but to all effects extremely immature neurons. Recently, transgenic models allowed to reveal that with age virtually all dormant precursors progressively awaken, abandon the immature state, and become fully functional neurons. Despite the limited common awareness about these cells, the deep implications of recent discoveries will likely lead to revisit our understanding of the adult brain. Thus, it is timely to revisit and critically assess the essential evidences that help pondering on the possible role(s) of these cells in relation to cognition, aging, and pathology. By highlighting pivoting findings as well as controversies and open questions, we offer an exciting perspective over the field of research that studies these mysterious cells and suggest the next steps toward the answer of a crucial question: why does the brain need dormant neuronal precursors?
... The rapid rate of OR pseudogenation observed in many mammalian clades (Young et al. 2010;Niimura 2012) is further evidence of rapid OR evolution, and further emphasizes the rapidity of change in chemical environments successfully occupied by early mammals. As Aboitiz and Montiel (2015) comment: "our hypothesis has common ground with those proposed by Lynch (1986), Rowe et al. (2011) and Rowe and Shepherd (2016) that olfactory systems were key in early mammalian evolution. Here we add to these hypotheses the role of the emergent isocortex [neocortex] as a multimodal interface in the olfactoryhippocampal axis for behavioral navigation". ...
