Dendritic morphology of pyramidal neurons in the chimpanzee neocortex: regional specializations and comparison to humans.

The primate cerebral cortex is characterized by regional variation in the structure of pyramidal neurons, with more complex dendritic arbors and greater spine density observed in prefrontal compared with sensory and motor cortices. Although there are several investigations in humans and other primates, virtually nothing is known about regional variation in the morphology of pyramidal neurons in the cerebral cortex of great apes, humans' closest living relatives. The current study uses the rapid Golgi stain to quantify the dendritic structure of layer III pyramidal neurons in 4 areas of the chimpanzee cerebral cortex: Primary somatosensory (area 3b), primary motor (area 4), prestriate visual (area 18), and prefrontal (area 10) cortex. Consistent with previous studies in humans and macaque monkeys, pyramidal neurons in the prefrontal cortex of chimpanzees exhibit greater dendritic complexity than those in other cortical regions, suggesting that prefrontal cortical evolution in primates is characterized by increased potential for integrative connectivity. Compared with chimpanzees, the pyramidal neurons of humans had significantly longer and more branched dendritic arbors in all cortical regions.

[1]  Federica Amici,et al.  Fission-Fusion Dynamics, Behavioral Flexibility, and Inhibitory Control in Primates , 2013, Current Biology.

[2]  Patrick R Hof,et al.  Neuropil distribution in the cerebral cortex differs between humans and chimpanzees , 2012, The Journal of comparative neurology.

[3]  Christina M. Weaver,et al.  Morphologic evidence for spatially clustered spines in apical dendrites of monkey neocortical pyramidal cells , 2012, The Journal of comparative neurology.

[4]  M. Meredith,et al.  Dendritic spine density in multisensory versus primary sensory cortex , 2012, Synapse.

[5]  M. Hanani Lucifer yellow – an angel rather than the devil , 2011, Journal of cellular and molecular medicine.

[6]  I. Kostović,et al.  Development of prefrontal layer III pyramidal neurons in infants with Down syndrome , 2011 .

[7]  G. Šimić,et al.  Extraordinary neoteny of synaptic spines in the human prefrontal cortex , 2011, Proceedings of the National Academy of Sciences.

[8]  I. Fujita,et al.  Spinogenesis and Pruning in the Anterior Ventral Inferotemporal Cortex of the Macaque Monkey: An Intracellular Injection Study of Layer III Pyramidal Cells , 2011, Front. Neuroanat..

[9]  K. Amunts,et al.  Spatial organization of neurons in the frontal pole sets humans apart from great apes. , 2011, Cerebral cortex.

[10]  Frank J. Yuk,et al.  Evidence for Reduced Experience-Dependent Dendritic Spine Plasticity in the Aging Prefrontal Cortex , 2011, The Journal of Neuroscience.

[11]  K. Christoff,et al.  Clarifying the self: Response to Northoff , 2011, Trends in Cognitive Sciences.

[12]  S. Pääbo,et al.  Rapid metabolic evolution in human prefrontal cortex , 2011, Proceedings of the National Academy of Sciences.

[13]  K. Amunts,et al.  Primate Prefrontal Cortex Evolution: Human Brains Are the Extreme of a Lateralized Ape Trend , 2011, Brain, Behavior and Evolution.

[14]  G. Elston,et al.  Pyramidal Cells in Prefrontal Cortex of Primates: Marked Differences in Neuronal Structure Among Species , 2010, Frontiers in Neuroanatomy.

[15]  Jamie L. Russell,et al.  Cortical Representation of Lateralized Grasping in Chimpanzees (Pan troglodytes): A Combined MRI and PET Study , 2010, PloS one.

[16]  Joshua Kaplan,et al.  Neurolucida Lucivid versus Neurolucida camera: A quantitative and qualitative comparison of three-dimensional neuronal reconstructions , 2010, Journal of Neuroscience Methods.

[17]  Brian Hare,et al.  Bonobos Exhibit Delayed Development of Social Behavior and Cognition Relative to Chimpanzees , 2010, Current Biology.

[18]  M. Kilgard,et al.  Effect of the environment on the dendritic morphology of the rat auditory cortex , 2010, Synapse.

[19]  W. Gan,et al.  Stably maintained dendritic spines are associated with lifelong memories , 2009, Nature.

[20]  Patrick J Coskren,et al.  The electrotonic structure of pyramidal neurons contributing to prefrontal cortical circuits in macaque monkeys is significantly altered in aging. , 2009, Cerebral cortex.

[21]  I. Fujita,et al.  Spinogenesis and Pruning Scales across Functional Hierarchies , 2009, The Journal of Neuroscience.

[22]  M. Tomasello,et al.  Does the chimpanzee have a theory of mind? 30 years later , 2008, Trends in Cognitive Sciences.

[23]  Milos Judas,et al.  Lifespan alterations of basal dendritic trees of pyramidal neurons in the human prefrontal cortex: a layer-specific pattern. , 2008, Cerebral cortex.

[24]  Douglas B. Ehlenberger,et al.  Repeated stress alters dendritic spine morphology in the rat medial prefrontal cortex , 2008, The Journal of comparative neurology.

[25]  N. Spruston Pyramidal neurons: dendritic structure and synaptic integration , 2008, Nature Reviews Neuroscience.

[26]  M. Cáceres,et al.  Increased cortical expression of two synaptogenic thrombospondins in human brain evolution. , 2007, Cerebral cortex.

[27]  D. Premack Human and animal cognition: Continuity and discontinuity , 2007, Proceedings of the National Academy of Sciences.

[28]  V. Casagrande Faculty Opinions recommendation of Increased cortical expression of two synaptogenic thrombospondins in human brain evolution. , 2007 .

[29]  H. Reichert,et al.  Evolution of Nervous Systems , 2007 .

[30]  J. Kaas,et al.  Specializations of the granular prefrontal cortex of primates: implications for cognitive processing. , 2006, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[31]  G. Elston,et al.  Specialization in pyramidal cell structure in the sensory-motor cortex of the Chacma baboon (Papio ursinus) with comparative notes on macaque and vervet monkeys. , 2005, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[32]  Bob Jacobs,et al.  Regional Dendritic Variation in Neonatal Human Cortex: A Quantitative Golgi Study , 2005, Developmental Neuroscience.

[33]  Jon H. Kaas,et al.  Regional Specialization in Pyramidal Cell Structure in the Visual Cortex of the Galago: An Intracellular Injection Study of Striate and Extrastriate Areas with Comparative Notes on New World and Old World Monkeys , 2005, Brain, Behavior and Evolution.

[34]  G. Elston,et al.  A study of pyramidal cell structure in the cingulate cortex of the macaque monkey with comparative notes on inferotemporal and primary visual cortex. , 2004, Cerebral cortex.

[35]  Wenbo Xu,et al.  Sister grouping of chimpanzees and humans as revealed by genome-wide phylogenetic analysis of brain gene expression profiles. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[36]  G. Elston Cortex, cognition and the cell: new insights into the pyramidal neuron and prefrontal function. , 2003, Cerebral cortex.

[37]  N. Kasthuri,et al.  Long-term dendritic spine stability in the adult cortex , 2002, Nature.

[38]  G. Elston,et al.  The Pyramidal Cell in Cognition: A Comparative Study in Human and Monkey , 2001, The Journal of Neuroscience.

[39]  J. Jacobs,et al.  Regional dendritic and spine variation in human cerebral cortex: a quantitative golgi study. , 2001, Cerebral cortex.

[40]  G. V. Van Hoesen,et al.  Prefrontal cortex in humans and apes: a comparative study of area 10. , 2001, American journal of physical anthropology.

[41]  Mark A. Changizi,et al.  Principles underlying mammalian neocortical scaling , 2001, Biological Cybernetics.

[42]  M. Tomasello,et al.  Do chimpanzees know what conspecifics know? , 2001, Animal Behaviour.

[43]  G. Elston Pyramidal Cells of the Frontal Lobe: All the More Spinous to Think With , 2000, The Journal of Neuroscience.

[44]  M G Rosa,et al.  Cellular heterogeneity in cerebral cortex: A study of the morphology of pyramidal neurones in visual areas of the marmoset monkey , 1999, The Journal of comparative neurology.

[45]  G. Elston,et al.  Cortical integration in the visual system of the macaque monkey: large-scale morphological differences in the pyramidal neurons in the occipital, parietal and temporal lobes , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[46]  A. Whiten,et al.  Cultures in chimpanzees , 1999, Nature.

[47]  D. Rumbaugh,et al.  Delay of gratification in chimpanzees (Pan troglodytes). , 1999, Developmental psychobiology.

[48]  E. Miller,et al.  The Prefrontal Cortex Complex Neural Properties for Complex Behavior , 1999, Neuron.

[49]  G. Elston,et al.  Morphological variation of layer III pyramidal neurones in the occipitotemporal pathway of the macaque monkey visual cortex. , 1998, Cerebral cortex.

[50]  de Brabander,et al.  Layer‐specific dendritic regression of pyramidal cells with ageing in the human prefrontal cortex , 1998, The European journal of neuroscience.

[51]  T. Deacon The Symbolic Species: The Co-evolution of Language and the Brain , 1998 .

[52]  B. Jacobs,et al.  Life‐span dendritic and spine changes in areas 10 and 18 of human cortex: A quantitative golgi study , 1997, The Journal of comparative neurology.

[53]  G. Elston,et al.  The occipitoparietal pathway of the macaque monkey: comparison of pyramidal cell morphology in layer III of functionally related cortical visual areas. , 1997, Cerebral cortex.

[54]  J. Fuster The Prefrontal Cortex , 1997 .

[55]  S C Rao,et al.  Integration of what and where in the primate prefrontal cortex. , 1997, Science.

[56]  B. Anderson,et al.  Age and hemisphere effects on dendritic structure. , 1996, Brain : a journal of neurology.

[57]  D. Tank,et al.  Dendritic Integration in Mammalian Neurons, a Century after Cajal , 1996, Neuron.

[58]  H. Uylings,et al.  Morphometric dendritic field analysis of pyramidal neurons in the human prefrontal cortex: relation to section thickness , 1996, Journal of Neuroscience Methods.

[59]  P Andersen,et al.  An increase in dendritic spine density on hippocampal CA1 pyramidal cells following spatial learning in adult rats suggests the formation of new synapses. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[60]  M. Koenderink,et al.  Postnatal maturation of the layer III pyramidal neurons in the human prefrontal cortex: a quantitative Golgi analysis , 1994, Brain Research.

[61]  Body and brain. , 1994, Journal of the Royal Society of Medicine.

[62]  A. Scheibel,et al.  A quantitative dendritic analysis of wernicke's area in humans. I. Lifespan changes , 1993, The Journal of comparative neurology.

[63]  A. Scheibel,et al.  A quantitative dendritic analysis of wernicke's area in humans. II. Gender, hemispheric, and environmental factors , 1993, The Journal of comparative neurology.

[64]  Richard W. Byrne,et al.  Cognitive Evolution in Primates: Evidence from Tactical Deception , 1992 .

[65]  D. Purves Body and Brain: A Trophic Theory of Neural Connections , 1988 .

[66]  A. Scheibel,et al.  Chapter 4 – The Methods of Golgi , 1978 .

[67]  R. Robertson Neuroanatomical Research Techniques , 1978 .

[68]  M. Diamond,et al.  Extensive cortical depth measurements and neuron size increases in the cortex of environmentally enriched rats , 1967 .

[69]  T. Serwold,et al.  Dendrite growth increased by visual activity requires NMDA receptor and Rho GTPases , 2022 .