Format-dependent and format-independent representation of sequential and simultaneous numerosity in the crow endbrain

Humans’ symbolic counting skills are built on a primordial ability to approximately estimate the number of items, or numerosity. To date it is debated whether numerosities presented in categorically different formats, that is as temporal sequences versus spatial arrays, are represented abstractly in the brain. To address this issue, we identified the behavioral characteristics and neuronal codes for sequential and simultaneous number formats in crows. We find a format-dependent representation by distinct groups of selective neurons during the sensory encoding stage. However, an abstract and format-independent numerosity code emerges once the encoding phase is completed and numerosities needed to be memorized. These results suggest a successive two-stage code for categorically different number formats and help to reconcile conflicting findings observed in psychophysics and brain imaging. Numbers are processed as abstract categories, despite considerable variations in presentation formats. By recording single-neuron activity in behaving crows, the authors show successive format-dependent and format-independent numerosity codes in the avian endbrain.

[1]  S. Blair Hedges,et al.  The origin and evolution of model organisms , 2002, Nature Reviews Genetics.

[2]  Bertrand Thirion,et al.  Deciphering Cortical Number Coding from Human Brain Activity Patterns , 2009, Current Biology.

[3]  J. Cantlon,et al.  Neural Tuning to Numerosity Relates to Perceptual Tuning in 3–6-Year-Old Children , 2017, The Journal of Neuroscience.

[4]  Philippe Pinel,et al.  Tuning Curves for Approximate Numerosity in the Human Intraparietal Sulcus , 2004, Neuron.

[5]  M. Srinivasan,et al.  Evidence for counting in insects , 2008, Animal Cognition.

[6]  Julie Castronovo,et al.  Superior numerical abilities following early visual deprivation , 2013, Cortex.

[7]  O. Güntürkün The avian ‘prefrontal cortex’ and cognition , 2005, Current Opinion in Neurobiology.

[8]  J D Delius,et al.  Pigeons (Columba livia) learn to link numerosities with symbols. , 2001, Journal of comparative psychology.

[9]  Andreas Nieder,et al.  Neurons in the Endbrain of Numerically Naive Crows Spontaneously Encode Visual Numerosity , 2018, Current Biology.

[10]  Brian Butterworth,et al.  Evidence for Two Numerical Systems That Are Similar in Humans and Guppies , 2012, PloS one.

[11]  G. Vallortigara,et al.  Quantity discrimination by zebrafish (Danio rerio). , 2015, Journal of comparative psychology.

[12]  Numerical discrimination by frogs (Bombina orientalis) , 2014, Animal Cognition.

[13]  Andreas Nieder,et al.  Compressed Scaling of Abstract Numerosity Representations in Adult Humans and Monkeys , 2009, Journal of Cognitive Neuroscience.

[14]  E. J. Carter,et al.  Functional Imaging of Numerical Processing in Adults and 4-y-Old Children , 2006, PLoS biology.

[15]  Harlene Hayne,et al.  Pigeons on Par with Primates in Numerical Competence , 2011, Science.

[16]  Andreas Nieder,et al.  Sensory and Working Memory Representations of Small and Large Numerosities in the Crow Endbrain , 2016, The Journal of Neuroscience.

[17]  Andreas Nieder,et al.  Associative learning rapidly establishes neuronal representations of upcoming behavioral choices in crows , 2015, Proceedings of the National Academy of Sciences.

[18]  Michael Andres,et al.  Mode-dependent and mode-independent representations of numerosity in the right intraparietal sulcus , 2010, NeuroImage.

[19]  Andreas Nieder,et al.  A Brain for Numbers: The Biology of the Number Instinct , 2019 .

[20]  J. Cantlon,et al.  Shared System for Ordering Small and Large Numbers in Monkeys and Humans , 2006, Psychological science.

[21]  Andreas Nieder,et al.  Inside the corvid brain—probing the physiology of cognition in crows , 2017, Current Opinion in Behavioral Sciences.

[22]  A. Foá,et al.  Quantity Discrimination in Trained Lizards (Podarcis sicula) , 2018, Front. Psychol..

[23]  A. Nieder The neuronal code for number , 2016, Nature Reviews Neuroscience.

[24]  Giorgio Vallortigara,et al.  Arithmetic in newborn chicks , 2009, Proceedings of the Royal Society B: Biological Sciences.

[25]  E. Spelke,et al.  The construction of large number representations in adults , 2003, Cognition.

[26]  Helen M. Ditz,et al.  Neurons selective to the number of visual items in the corvid songbird endbrain , 2015, Proceedings of the National Academy of Sciences.

[27]  B. P. Klein,et al.  Topographic Representation of Numerosity in the Human Parietal Cortex , 2013, Science.

[28]  Jair E. Garcia,et al.  Numerical ordering of zero in honey bees , 2018, Science.

[29]  Chih-Jen Lin,et al.  LIBSVM: A library for support vector machines , 2011, TIST.

[30]  A. Reiner,et al.  The expression of tyrosine hydroxylase and DARPP‐32 in the house crow (Corvus splendens) brain , 2019, The Journal of comparative neurology.

[31]  Á. Miklósi,et al.  Role of mental representations in quantity judgments by jackdaws (Corvus monedula). , 2014, Journal of comparative psychology.

[32]  G. Vallortigara,et al.  Continuous and discrete quantity discrimination in tortoises , 2018, bioRxiv.

[33]  Giorgio Vallortigara,et al.  Discrimination of small numerosities in young chicks. , 2008, Journal of experimental psychology. Animal behavior processes.

[34]  Elena Rusconi,et al.  A brain for numbers , 2009, Cortex.

[35]  Hilary Barth,et al.  Abstract number and arithmetic in preschool children. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[36]  Masato Aoyama,et al.  Spontaneous discrimination of food quantities in the jungle crow, Corvus macrorhynchos , 2014, Animal Behaviour.

[37]  Andreas Nieder,et al.  Numerosity representations in crows obey the Weber–Fechner law , 2016, Proceedings of the Royal Society B: Biological Sciences.

[38]  Bronwen L. Aken,et al.  The draft genomes of soft–shell turtle and green sea turtle yield insights into the development and evolution of the turtle–specific body plan , 2013, Nature Genetics.

[39]  C. Packer,et al.  Roaring and numerical assessment in contests between groups of female lions, Panthera leo , 1994, Animal Behaviour.

[40]  Byron M. Yu,et al.  Dimensionality reduction for large-scale neural recordings , 2014, Nature Neuroscience.

[41]  Andreas Nieder,et al.  Temporal and Spatial Enumeration Processes in the Primate Parietal Cortex , 2006, Science.

[42]  Xavier Seron,et al.  Numerical estimation in blind subjects: evidence of the impact of blindness and its following experience. , 2007, Journal of experimental psychology. Human perception and performance.

[43]  R. Jaeger,et al.  Salamanders (Plethodon cinereus) go for more: rudiments of number in an amphibian , 2003, Animal Cognition.

[44]  Maximilian E. Kirschhock,et al.  Neuronal Correlates of Spatial Working Memory in the Endbrain of Crows , 2019, Current Biology.

[45]  N. M. Brooke,et al.  A molecular timescale for vertebrate evolution , 1998, Nature.

[46]  A. Nieder,et al.  Cross-Modal Associative Mnemonic Signals in Crow Endbrain Neurons , 2015, Current Biology.

[47]  Florian Mormann,et al.  Single Neurons in the Human Brain Encode Numbers , 2018, Neuron.

[48]  Andreas Nieder,et al.  The Number Domain— Can We Count on Parietal Cortex? , 2004, Neuron.

[49]  H S Terrace,et al.  Ordering of the numerosities 1 to 9 by monkeys. , 1998, Science.

[50]  K. Burns,et al.  Adaptive numerical competency in a food-hoarding songbird , 2008, Proceedings of the Royal Society B: Biological Sciences.