Behavioral and Prefrontal Representation of Spatial Proportions in the Monkey

Primate brains are equipped with evolutionarily old and dedicated neural circuits so that they can grasp absolute quantities, such as the number of items or the length of a line. Absolute magnitude, however, is often not informative enough to guide decisions in conflicting social and foraging situations that require an assessment of quantity ratios. We report that rhesus monkeys can discriminate proportions (1:4, 2:4, 3:4, and 4:4) specified by bars differing in lengths and that they can do so at a precision comparable to that shown by humans; the monkeys thus demonstrate an abstract understanding of proportionality. Moreover, neurons in the lateral prefrontal cortex selectively responded to preferred proportions regardless of the exact physical appearance of the stimuli. These results support the hypothesis that nonhuman primates can judge proportions and utilize the underlying information in behaviorally relevant situations.

[1]  J. Tanji,et al.  Numerical representation for action in the parietal cortex of the monkey , 2002, Nature.

[2]  Elizabeth S. Spelke,et al.  Evolutionary and developmental foundations of human knowledge: A case study of mathematics , 2004 .

[3]  Andreas Nieder,et al.  Semantic Associations between Signs and Numerical Categories in the Prefrontal Cortex , 2007, PLoS biology.

[4]  A. Nieder Counting on neurons: the neurobiology of numerical competence , 2005, Nature Reviews Neuroscience.

[5]  D. Harper Competitive foraging in mallards: “Ideal free’ ducks , 1982, Animal Behaviour.

[6]  G. Mandler,et al.  Subitizing: an analysis of its component processes. , 1982, Journal of experimental psychology. General.

[7]  Koleen McCrink,et al.  Ratio Abstraction by 6-Month-Old Infants , 2007, Psychological science.

[8]  Karen Wynn,et al.  Addition and subtraction by human infants , 1992, Nature.

[9]  E. Miller,et al.  Analog Numerical Representations in Rhesus Monkeys: Evidence for Parallel Processing , 2004, Journal of Cognitive Neuroscience.

[10]  Kelly S. Mix,et al.  Early fraction calculation ability. , 1999, Developmental psychology.

[11]  S. Dehaene,et al.  Exact and Approximate Arithmetic in an Amazonian Indigene Group , 2004, Science.

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

[13]  Andreas Nieder,et al.  A parieto-frontal network for visual numerical information in the monkey. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

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

[15]  Stanislas Dehaene,et al.  Arithmetic and the Brain This Review Comes from a Themed Issue on Cognitive Neuroscience Edited the Intraparietal Sulcus and Number Sense Number Sense in the Animal Brain , 2022 .

[16]  C. Gallistel The organization of learning , 1990 .

[17]  Michael N. Shadlen,et al.  Probabilistic reasoning by neurons , 2007, Nature.

[18]  P. Gordon Numerical Cognition Without Words: Evidence from Amazonia , 2004, Science.

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

[20]  Stanislas Dehaene,et al.  Distinct Cerebral Pathways for Object Identity and Number in Human Infants , 2008, PLoS biology.

[21]  Michael J Beran,et al.  Rhesus monkeys (Macaca mulatta) enumerate large and small sequentially presented sets of items using analog numerical representations. , 2007, Journal of experimental psychology. Animal behavior processes.

[22]  Andreas Nieder,et al.  A Labeled-Line Code for Small and Large Numerosities in the Monkey Prefrontal Cortex , 2007, The Journal of Neuroscience.

[23]  Philippe Pinel,et al.  Distributed and Overlapping Cerebral Representations of Number, Size, and Luminance during Comparative Judgments , 2004, Neuron.

[24]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[25]  S. Dehaene,et al.  A Magnitude Code Common to Numerosities and Number Symbols in Human Intraparietal Cortex , 2007, Neuron.

[26]  Catherine Sophian,et al.  Perceptions of proportionality in young children: matching spatial ratios , 2000, Cognition.

[27]  Masaki Tomonaga,et al.  Enumeration of briefly presented items by the chimpanzee (Pan troglodytes) and humans (Homo sapiens) , 2002, Animal learning & behavior.

[28]  E. Miller,et al.  Coding of Cognitive Magnitude Compressed Scaling of Numerical Information in the Primate Prefrontal Cortex , 2003, Neuron.

[29]  Andreas Nieder,et al.  Neuronal population coding of continuous and discrete quantity in the primate posterior parietal cortex , 2007, Proceedings of the National Academy of Sciences.

[30]  David Premack,et al.  Primative mathematical concepts in the chimpanzee: proportionality and numerosity , 1981, Nature.

[31]  J. Tanji,et al.  Role of the lateral prefrontal cortex in executive behavioral control. , 2008, Physiological reviews.

[32]  E. Spelke,et al.  Language and Conceptual Development series Core systems of number , 2004 .

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

[34]  David J. Freedman,et al.  Representation of the Quantity of Visual Items in the Primate Prefrontal Cortex , 2002, Science.

[35]  Susan Carey,et al.  Spontaneous number representation in semi–free–ranging rhesus monkeys , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[36]  Elizabeth M Brannon,et al.  Basic Math in Monkeys and College Students , 2007, PLoS biology.

[37]  永福 智志 The Organization of Learning , 2005, Journal of Cognitive Neuroscience.

[38]  U. Goswami,et al.  Does half a pizza equal half a box of chocolates?: Proportional matching in an analogy task , 2001 .