The Evolutionary History of Brains for Numbers

Diverse species from across the animal tree of life share an intuitive understanding countable quantities.In vertebrates such as fishes, birds, and mammals, telencephalic pallium emerges independently a key brain area for numerical representations. This suggests that is ideal candidate region number representations in convergently evolved brains.The neural basis sense has not been studied invertebrate so far, but promising regions brains insects, spiders, cephalopods can be identified.Number seem to have by convergent evolution result common selection pressures different vertebrate taxa. Humans other animals sense’, quantities. Having independent one another hundreds millions years, these diverse species, including monkeys, crows, zebrafishes, bees, squids, differ radically. However, all investigated, telencephalon implicated processing. properties make it ideally suited host pressures. In addition, invertebrates, cephalopods, identified, opening possibility even deeper commonalities sense. nonhuman kingdom quantities, or quantity (see Glossary) (henceforth ‘number’) [1.Nieder A. A Brain Numbers: The Biology Number Instinct. MIT Press, 2019Crossref Google Scholar]. Distinct zoological groups arising ancestral bilaterian (Box 1) – like mammals invertebrates possess ability discriminate quantity. Numerical refers elements set (‘numerosity’) needs differentiated representation continuous 2). ‘sense number’ provides survival reproductive advantages various taxa traced through evolutionary history [2.Nieder adaptive value competence.Trends Ecol. Evol. 2020; 35: 605-617Abstract Full Text PDF PubMed Scholar].Box 1Phylogeny Bilateral Animals: Protostomes DeuterostomesAll advanced we see on planet today are ‘bilaterians’; they bilaterally symmetrical body with front rear end. Around 600 million years ago, large trunk split into two major branches.One branch constitutes protostomes maintain primordial mouth forms early ontogeny adult stage. central nervous system (nerve cord) ventral side body.The deuterostomes do formed instead develop new gut system. (as members phylum Chordata) belong deuterostomes. They (neural tube) dorsal body.Some taxa, protostome arthropods deuterostome vertebrates, neuron concentrations at anterior pole body, have. finding gene expression patterns suggest last ancestor bilateral animals, hypothetical ‘urbilaterian’, most likely did [136.Martín-Durán J.M. et al.Convergent nerve cords.Nature. 2018; 553: 45-50Crossref Scopus (63) From this generally inferred must (unless maintains unlikely scenario had already existed ancestors vanished several times over evolution). despite parallel brains, genes become expressed build phylogeny, well neuronal circuitries seen remotely related surprisingly similar. points facing harsh constraints when reinventing course evolution. Evolution thus seems resort strikingly similar principles building based evolution, processing.Box 2Demonstrating Representations AnimalsAnimal studies cognition widely respect testing procedures, stimuli, complexity These differences need considered evaluating claims competence [137.Leibovich T. al.From “sense number” magnitude”: role magnitudes cognition.Behav. Sci. 2017; 40e164Crossref (0) Scholar].In wild untrained mainly free-choice experiments performed. Here, subjects spontaneously choose between alternatives (e.g., sets food items) according preference. systematic preference choice indicates discriminated. Because items inherently relevant focal usually confounded Moreover, motivational status (whether want quantities) typically unknown approaches. also only probe simple abilities, relative numerosity judgments require ‘more than’ versus ‘less decisions. Therefore, spontaneous tests provide suggestive evidence competence.These problems bypassed training controlled environment. performance tested motivated meticulously designed stimuli control non-numerical factors. Training test more capabilities, flexible discrimination precise numerosities processing rules. Last least, combined research.A notorious problem non-numerical, Without specific adjustments, total array, presentation duration shown sequentially) co-varies changes number, could learn respond For instance, four bananas occupy twice much visual may amount yellow rather than bananas. Control factors achieved equating computer-controlled and/or using protocols which co-varying same session unbeknown [55.Brannon E.M. Terrace H.S. Ordering 1 9 monkeys.Science. 1998; 282: 746-749Crossref (395) Scholar,61.Nieder al.Representation primate prefrontal cortex.Science. 2002; 297: 1708-1711Crossref (466) Representation ensured if continues irrespective appearance stimuli.To demonstrate abstract required represent time (i.e., presented sequentially one-by-one) space (items arrays) sensory modalities auditory items). methodological constraints, list requirements cannot fulfilled single experiment. combinations clearly show least some notably monkeys [66.Nieder Supramodal selectivity neurons posterior parietal cortices.Proc. Natl. Acad. U. S. 2012; 109: 11860-11865Crossref (103) Scholar,138.Jordan K.E. al.Monkeys match tally quantities senses.Cognition. 2008; 108: 617-625Crossref Scholar] crows [42.Ditz H.M. Nieder Format-dependent format-independent sequential simultaneous crow endbrain.Nat. Commun. 11: 686Crossref (9) Scholar], discriminated numbers way spatiotemporal modalities. flexibility yet demonstrated fishes trained others fixed rule. All branches. One body. Some Animal competence. research. stimuli. To years. As consequence, distantly radically their complexity, mechanisms, organization. So, how give rise number? explanation would was present bilaterians. If true, expected descendants conserved structures emerged. According scenario, homologous trait reaches back basal Alternatively, lineages without numerically competent via supporting shaped populations faced struggle survival. choosing larger dissimilar assures greater energy intake possessing advantage social interactions determine outcome potentially lethal fights within [3.Benson-Amram al.Numerical assessment wild: insights carnivores.Philos. Trans. R. Soc. Lond. B Biol. 37320160508Crossref benefit competence, endowing them arise maintained populations. Independent innovations often capitalize pre-existing favorable originally served functions before further modification [4.Jacob F. tinkering.Science. 1977; 196: 1161-1166Crossref applies brain, areas appear malleable development support elaborate cognitive functioning others. review uses comparative, approach explore anatomy physiology capabilities emerge. I argue anatomical physiological parts (members ‘deuterostomes’) were vertebrates. Neural data (more precisely, ‘protostomes’) currently lacking, high-level identified future research phylogenetic roots number. extremely group aquatic jawless cyclostomes (hagfish, lampreys), cartilaginous (sharks, rays), bony (coelacanths, lungfishes, ray-finned fishes). Ray-finned belonging teleosts, exhibit many innovations, partly whole-genome duplications [5.Pasquier J. al.Gene after whole genome duplication fish: PhyloFish database.BMC Genomics. 2016; 17: 368Crossref (132) reported basic skills domain, reports involve teleosts ‘fishes’) [6.Agrillo C. al.Large mosquitofish.PLoS One. 2010; 5e15232Crossref (55) Scholar, 7.Agrillo acuity fish improved presence moving targets, subitizing range.Anim. Cogn. 2014; 307-316Crossref (28) 8.Miletto Petrazzini M.E. al.Relative absolute guppies “fourness”?.Anim. 2015; 18: 1007-1017Crossref (19) 9.DeLong C.M. al.Small goldfish (Carassius auratus) extensive training.Behav. Process. 141: 172-183Crossref (20) Scholar]; contrast, lacking. ‘go more’ picking hedonic alternative tasks. Fish approximate fashion showing precision small opposed sets, discriminations Recent explored correlates 3). relatively underdeveloped both size differentiation [10.Striedter G.F. Northcutt R.G. Brains Through Time: Natural History Vertebrates. Oxford University 2020Google (Figure 1, Key Figure). (teleosts), subdivided five parts: medial (Dm), (Dd), (Dc), lateral (Dl), (Dp) subdivision [11.Nieuwenhuys forebrain actinopterygians revisited.Brain Behav. 2009; 73: 229-252Crossref (69) Scholar,12.Ganz al.Subdivisions zebrafish molecular marker analysis.J. Comp. Neurol. 3: 308Google Despite its simplicity, subdivisions homologies resolved remain controversial, especially since telencephala unique process outward folding [13.Mueller al.The zebrafish, Danio rerio (Cyprinidae, Teleostei).Brain Res. 2011; 1381: 95-105Crossref (127) 3Evolution Vertebrate Telencephalon (Endbrain)All principal divisions, telencephalon, endbrain, pole. comprises (Latin mantle) subpallium; latter includes striatum septum. innovation regarded crowning achievement Originally associated expanded olfactory endbrain began small, simple, undifferentiated part. condition still visible fishes. With tetrapods conquered land (amphibians), changed little.However, dramatic expansions organization accompanied amniotes (mammals sauropsids; i.e., reptiles birds). Independently time, particular, became dominant largest integration center birds. medial, dorsal, lateral, ventral. destinies pallial drastically birds: while lineage leading dramatically modern birds.Mammals transformed six-layered ‘neocortex’ runs surface prime emerges. cortex birds so-called ‘Wulst’ (German ‘bulge’) Both reptilian avian Wulst receive unimodal input thalamus [139.Medina L. Do homologues mammalian visual, somatosensory, motor cortices?.in: Kaas J.H. Bullock T.H. Nervous Systems. Vol. 2. Elsevier, 2007: 163-194Crossref neocortex far complex cortex. structurally Wulst.Different situation dominating structure sauropsids, forming large, elongated ridge protrudes ventricle therefore called ‘dorsal ventricular ridge’ (DVR). DVR develops nuclear termed hyperpallium, entopallium, mesopallium, nidopallium, arcopallium, comprise [140.Jarvis E.D. al.Avian evolution.Nat. Rev. Neurosci. 2005; 6: 151-159Crossref (653) Aspects assume associative neocortical mammals. By claustro-amygdalar complex.Both retained pallium, hippocampus Similarly, groups. little. Mammals Wulst. Different complex. Neurons responses recently histological methods [14.Messina al.Response change zebrafish: behavioural study.Sci. Rep. 10: 5769Crossref (2) behaviorally passive habituation–dishabituation protocol comprising arrays containing dots. paradigm builds repeated stimulus causes reduction activity responsive (habituation). After process, sudden switch will engage sensitive (dishabituation). example, repeatedly three-dot (controlled physical variables) during