A parieto-frontal network for visual numerical information in the monkey.

Recent electrophysiological studies in monkeys have implicated the prefrontal cortex (PFC) and posterior parietal cortex (PPC) in numerical judgments. The functional organization and respective contributions of these (and other) cortical areas, however, are unknown; their neural activity during numerical judgments has not been directly compared. We surveyed activity in the PPC and the anterior inferior temporal cortex while monkeys performed a visual numerosity judgment task and compared it with a population of PFC neurons. In the PPC, the proportion of numerosity-selective neurons was highest in the fundus of the intraparietal sulcus; only few numerosity-selective neurons were found in other PPC areas or the anterior inferior temporal cortex. Further, neurons in the fundus of the intraparietal sulcus responded and conveyed numerosity earlier than PFC neurons, suggesting that numerosity information flows from the PPC to the lateral PFC. This finding suggests a parieto-frontal network for numerosity in monkeys and establishes homologies between the monkey and human brain.

[1]  P. MacNeilage,et al.  Numerical representations in primates. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[2]  Keiji Tanaka,et al.  Inferotemporal cortex and object vision. , 1996, Annual review of neuroscience.

[3]  D G Gadian,et al.  Calculation difficulties in children of very low birthweight: a neural correlate. , 2001, Brain : a journal of neurology.

[4]  Leslie G. Ungerleider,et al.  Projections from inferior temporal cortex to prefrontal cortex via the uncinate fascicle in rhesus monkeys , 2004, Experimental Brain Research.

[5]  David Nicholl Principles of Frontal Lobe Function DT Stuss RT Knight , 2003, The Lancet Neurology.

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

[7]  David J. Freedman,et al.  A Comparison of Primate Prefrontal and Inferior Temporal Cortices during Visual Categorization , 2003, The Journal of Neuroscience.

[8]  J. Fuster,et al.  From perception to action: temporal integrative functions of prefrontal and parietal neurons. , 1999, Cerebral cortex.

[9]  P. Goldman-Rakic,et al.  Inactivation of parietal and prefrontal cortex reveals interdependence of neural activity during memory-guided saccades. , 2000, Journal of neurophysiology.

[10]  S. Dehaene,et al.  Abstract representations of numbers in the animal and human brain , 1998, Trends in Neurosciences.

[11]  K. Zilles,et al.  Polymodal Motion Processing in Posterior Parietal and Premotor Cortex A Human fMRI Study Strongly Implies Equivalencies between Humans and Monkeys , 2001, Neuron.

[12]  D. LeBihan,et al.  Modulation of Parietal Activation by Semantic Distance in a Number Comparison Task , 2001, NeuroImage.

[13]  R. Romo,et al.  Timing and neural encoding of somatosensory parametric working memory in macaque prefrontal cortex. , 2003, Cerebral cortex.

[14]  G. Orban,et al.  How well do response changes of striate neurons signal differences in orientation: a study in the discriminating monkey , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  Paul Bloom,et al.  Enumeration of collective entities by 5-month-old infants , 2002, Cognition.

[16]  J. Fuster,et al.  Effects of cooling parietal cortex on prefrontal units in delay tasks , 1989, Brain Research.

[17]  D. M. Green,et al.  Signal detection theory and psychophysics , 1966 .

[18]  A. Kleinschmidt,et al.  A Supramodal Number Representation in Human Intraparietal Cortex , 2003, Neuron.

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

[20]  E. J. Capaldi,et al.  The Development of numerical competence : animal and human models , 1993 .

[21]  E. Spelke,et al.  Sources of mathematical thinking: behavioral and brain-imaging evidence. , 1999, Science.

[22]  R. Romo,et al.  Neuronal correlates of parametric working memory in the prefrontal cortex , 1999, Nature.

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

[24]  D. Stuss,et al.  Principles of frontal lobe function , 2002 .

[25]  J. Movshon,et al.  The statistical reliability of signals in single neurons in cat and monkey visual cortex , 1983, Vision Research.

[26]  K. Priftis,et al.  Brain damage: Neglect disrupts the mental number line , 2002, Nature.

[27]  E. Spelke,et al.  Large number discrimination in 6-month-old infants , 2000, Cognition.

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

[29]  S. Dehaene,et al.  Language and calculation within the parietal lobe: a combined cognitive, anatomical and fMRI study , 2000, Neuropsychologia.

[30]  R. Andersen,et al.  Magnetic resonance image-guided implantation of chronic recording electrodes in the macaque intraparietal sulcus , 2003, Journal of Neuroscience Methods.

[31]  Richard F. Thompson,et al.  Number Coding in Association Cortex of the Cat , 1970, Science.

[32]  D. Wilkin,et al.  Neuron , 2001, Brain Research.

[33]  D. V. van Essen,et al.  Corticocortical connections of visual, sensorimotor, and multimodal processing areas in the parietal lobe of the macaque monkey , 2000, The Journal of comparative neurology.

[34]  M. Goldberg,et al.  Ventral intraparietal area of the macaque: anatomic location and visual response properties. , 1993, Journal of neurophysiology.

[35]  M. Goldberg,et al.  Ventral intraparietal area of the macaque: congruent visual and somatic response properties. , 1998, Journal of neurophysiology.