The Minicolumn and Evolution of the Brain

The minicolumn is generally considered an elementary unit of the neocortex in all mammalian brains. This essential building block has been affected by changes in the circuitry of the cortex during evolution. Researchers believe that enlargement of the cortical surface occurs through the addition of minicolumns rather than of single neurons. Therefore, minicolumns integrate cortical encephalization with organization. Despite these insights, few studies have analyzed the morphometry of the minicolumn to detect subtle but important differences among the brains of diverse mammals. The notion that minicolumns are essentially unchanged across species is challenged by strong evidence to the contrary. Because they are subject to species-specific variation, they can be used as a way to study evolutionary changes. Unfortunately, comparative studies are marred by a lack of standardized techniques, tissue preparation, cortical regions, or anatomical feature studied. However, recent advances in methodology enable standardized, quantified comparisons of minicolumn morphology.

[1]  V. Mountcastle Modality and topographic properties of single neurons of cat's somatic sensory cortex. , 1957, Journal of neurophysiology.

[2]  M. Marín‐padilla Prenatal and early postnatal ontogenesis of the human motor cortex: a golgi study. II. The basket-pyramidal system. , 1970, Brain research.

[3]  G. Bonin,et al.  On columnar arrangement of nerve cells in cerebral cortex. , 1971, Brain research.

[4]  M. Merzenich,et al.  Alterations in mechanoreceptor input to Brodmann's areas 1 and 3 of the postcentral hand area of Macaca mulatta after nerve section and regeneration. , 1972, Brain research.

[5]  T. M. Walsh,et al.  A study of the organization of apical dendrites in the somatic sensory cortex of the rat , 1972, The Journal of comparative neurology.

[6]  P. Rakić Mode of cell migration to the superficial layers of fetal monkey neocortex , 1972, The Journal of comparative neurology.

[7]  M. LeMay,et al.  Human brain--morphologic differences in the hemispheres demonstrable by carotid arteriography. , 1972, The New England journal of medicine.

[8]  H. Burton,et al.  Cytoarchitecture and somatic sensory connectivity of thalamic nuclei other than the ventrobasal complex in the cat , 1974, The Journal of comparative neurology.

[9]  A. Peters,et al.  A study of barrels and pyramidal dendritic clusters in the cerebral cortex. , 1974, Brain research.

[10]  N. Geschwind,et al.  Hemispheric differences in the brains of great apes. , 1975, Brain, behavior and evolution.

[11]  Marjorie LeMay,et al.  MORPHOLOGICAL CEREBRAL ASYMMETRIES OF MODERN MAN, FOSSIL MAN, AND NONHUMAN PRIMATE , 1976, Annals of the New York Academy of Sciences.

[12]  W. Nauta,et al.  Columnar distribution of cortico-cortical fibers in the frontal association, limbic, and motor cortex of the developing rhesus monkey , 1977, Brain Research.

[13]  P. Rakic,et al.  Neuronal migration and contact guidance in the primate telencephalon. , 1978, Postgraduate medical journal.

[14]  V. Mountcastle,et al.  An organizing principle for cerebral function : the unit module and the distributed system , 1978 .

[15]  Cerebral asymmetry in Old World monkeys. , 1978, Acta anatomica.

[16]  D. Folk Cerebral asymmetry in Old World monkeys , 1978 .

[17]  Patrick L. McGeer,et al.  Molecular Neurobiology of the Mammalian Brain , 1978, Springer US.

[18]  H. Seldon Structure of human auditory cortex. II. Axon distributions and morphological correlates of speech perception , 1981, Brain Research.

[19]  A. Cowey,et al.  Vertical organization of neurones accumulating 3H-GABA in visual cortex of rhesus monkey , 1981, Nature.

[20]  H. Seldon Structure of human auditory cortex. I. Cytoarchitectonics and dendritic distributions , 1981, Brain Research.

[21]  H. Seldon Structure of human auditory cortex. III. Statistical analysis of dendritic trees , 1982, Brain Research.

[22]  P. Goldman-Rakic,et al.  Interdigitation of contralateral and ipsilateral columnar projections to frontal association cortex in primates. , 1982, Science.

[23]  N. Geschwind,et al.  Asymmetries of the Brains and Skulls of Nonhuman Primates , 1982 .

[24]  A. Schleicher,et al.  Quantitative Cytoarchitectonics of the Cerebral Cortices of Several Prosimian Species , 1982 .

[25]  J. Szentágothai The modular architectonic principle of neural centers. , 1983, Reviews of physiology, biochemistry and pharmacology.

[26]  I. Kostović,et al.  Prenatal and perinatal development of radial cell columns in the human auditory cortex. , 1984, Acta oto-laryngologica.

[27]  Jelena Krmpoti Nemani,et al.  Prenatal and perinatal development of radial cell columns in the human auditory cortex. , 1984 .

[28]  D. Hubel,et al.  Specificity of intrinsic connections in primate primary visual cortex , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  E. G. Jones,et al.  Vertical organization of gamma-aminobutyric acid-accumulating intrinsic neuronal systems in monkey cerebral cortex , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  H. Seldon,et al.  The Anatomy of Speech Perception , 1985 .

[31]  M. Jacobson,et al.  Architecture of apical dendrites in the murine neocortex: Dual apical dendritic systems , 1986, Neuroscience.

[32]  M. Alexander,et al.  Principles of Neural Science , 1981 .

[33]  A. Peters,et al.  The neuronal composition of area 17 of rat visual cortex. IV. The organization of pyramidal cells , 1987, The Journal of comparative neurology.

[34]  M. Cynader,et al.  Surface organization of orientation and direction selectivity in cat area 18 , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  B. Whitsel,et al.  A combined 2‐deoxyglucose and neurophysiological study of primate somatosensory cortex , 1987, The Journal of comparative neurology.

[36]  ML Schwartz,et al.  Periodicity of GABA-containing cells in primate prefrontal cortex , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[37]  J. S. McCasland,et al.  High‐resolution 2‐deoxyglucose mapping of functional cortical columns in mouse barrel cortex , 1988, The Journal of comparative neurology.

[38]  B. Whitsel,et al.  Spatial organization of the peripheral input to area 1 cell columns. II. The forelimb representation achieved by a mosaic of segregates , 1988, Brain Research Reviews.

[39]  B. Whitsel,et al.  Spatial organization of the peripheral input to area 1 cell columns. I. the detection of ‘segregates’ , 1988, Brain Research Reviews.

[40]  E. G. Jones,et al.  Synapses of double bouquet cells in monkey cerebral cortex visualized by calbindin immunoreactivity , 1989, Brain Research.

[41]  W. Singer,et al.  Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties , 1989, Nature.

[42]  R Llinás,et al.  Intrinsic electrical properties of nerve cells and their role in network oscillation. , 1990, Cold Spring Harbor symposia on quantitative biology.

[43]  N. Swindale Is the cerebral cortex modular? , 1990, Trends in Neurosciences.

[44]  E. Leise Modular construction of nervous systems: A basic principle of design for invertebrates and vertebrates , 1990, Brain Research Reviews.

[45]  M. Diamond,et al.  Demonstration of discrete place‐defined columns—segregates—in the cat SI , 1990, The Journal of comparative neurology.

[46]  T. Deacon Rethinking mammalian brain evolution , 1990 .

[47]  E. G. Jones,et al.  A microcolumnar structure of monkey cerebral cortex revealed by immunocytochemical studies of double bouquet cell axons , 1990, Neuroscience.

[48]  J L Ringo,et al.  Neuronal interconnection as a function of brain size. , 1991, Brain, behavior and evolution.

[49]  A. Peters,et al.  Organization of pyramidal neurons in area 17 of monkey visual cortex , 1991, The Journal of comparative neurology.

[50]  B L Whitsel,et al.  Mechanisms underlying somatosensory cortical dynamics: I. In vivo studies. , 1992, Cerebral cortex.

[51]  Minami Ito,et al.  Columns for visual features of objects in monkey inferotemporal cortex , 1992, Nature.

[52]  J. DeFelipe,et al.  The pyramidal neuron of the cerebral cortex: Morphological and chemical characteristics of the synaptic inputs , 1992, Progress in Neurobiology.

[53]  R. Yuste,et al.  Neuronal domains in developing neocortex. , 1992, Science.

[54]  B L Whitsel,et al.  Mechanisms underlying somatosensory cortical dynamics: II. In vitro studies. , 1992, Cerebral cortex.

[55]  D. Purves,et al.  Iterated patterns of brain circuitry (or how the cortex gets its spots) , 1992, Trends in Neurosciences.

[56]  J. Kaas The functional organization of somatosensory cortex in primates. , 1993, Annals of anatomy = Anatomischer Anzeiger : official organ of the Anatomische Gesellschaft.

[57]  J. B. Levitt,et al.  Comparison of intrinsic connectivity in different areas of macaque monkey cerebral cortex. , 1993, Cerebral cortex.

[58]  A. Peters,et al.  Neuronal organization in area 17 of cat visual cortex. , 1993, Cerebral cortex.

[59]  C. Beaulieu,et al.  Numerical data on neocortical neurons in adult rat, with special reference to the GABA population , 1993, Brain Research.

[60]  A Keller,et al.  Intrinsic synaptic organization of the motor cortex. , 1993, Cerebral cortex.

[61]  B L Whitsel,et al.  Minicolumnar activation patterns in cat and monkey SI cortex. , 1993, Cerebral cortex.

[62]  E. White,et al.  Cortical modules in the posteromedial barrel subfield (Sml) of the mouse , 1993, The Journal of comparative neurology.

[63]  S. Shamma,et al.  Organization of response areas in ferret primary auditory cortex. , 1993, Journal of neurophysiology.

[64]  A. Peters,et al.  Numerical relationships between geniculocortical afferents and pyramidal cell modules in cat primary visual cortex. , 1993, Cerebral cortex.

[65]  J. Deuchars,et al.  Temporal and spatial properties of local circuits in neocortex , 1994, Trends in Neurosciences.

[66]  D. Kelly,et al.  Minicolumnar organization within somatosensory cortical segregates: II. Emergent functional properties. , 1994, Cerebral cortex.

[67]  Hans-Ulrich Dodt,et al.  Changes in intrinsic optical signal of rat neocortical slices following afferent stimulation , 1994, Neuroscience Letters.

[68]  D. Kelly,et al.  Minicolumnar organization within somatosensory cortical segregates: I. Development of afferent connections. , 1994, Cerebral cortex.

[69]  L. Krubitzer The organization of neocortex in mammals: are species differences really so different? , 1995, Trends in Neurosciences.

[70]  H. Sompolinsky,et al.  Theory of orientation tuning in visual cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[71]  P. Rakic,et al.  Radial and horizontal deployment of clonally related cells in the primate neocortex: Relationship to distinct mitotic lineages , 1995, Neuron.

[72]  P. Goldman-Rakic,et al.  Intrinsic circuit organization of the major layers and sublayers of the dorsolateral prefrontal cortex in the rhesus monkey , 1995, The Journal of comparative neurology.

[73]  S. Nelson,et al.  An emergent model of orientation selectivity in cat visual cortical simple cells , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[74]  P. Goldman-Rakic,et al.  Abnormally high neuronal density in the schizophrenic cortex. A morphometric analysis of prefrontal area 9 and occipital area 17. , 1995, Archives of general psychiatry.

[75]  W. Singer,et al.  Stimulus dependent intercolumnar synchronization of single unit responses in cat area 17. , 1995, Neuroreport.

[76]  A. Schleicher,et al.  Quantitative analysis of the columnar arrangement of neurons in the human cingulate cortex , 1995, The Journal of comparative neurology.

[77]  Paul Leonard Gabbott,et al.  The organisation of dendritic bundles in the prelimbic cortex (area 32) of the rat , 1996, Brain Research.

[78]  Trichur Raman Vidyasagar,et al.  Multiple mechanisms underlying the orientation selectivity of visual cortical neurones , 1996, Trends in Neurosciences.

[79]  I Fujita,et al.  Intrinsic connections in the macaque inferior temporal cortex , 1996, The Journal of comparative neurology.

[80]  D J Simons,et al.  Spatial gradients and inhibitory summation in the rat whisker barrel system. , 1996, Journal of neurophysiology.

[81]  M. Gazzaniga,et al.  Acetylcholinesterase staining in human auditory and language cortices: regional variation of structural features. , 1996, Cerebral cortex.

[82]  A. Peters,et al.  Myelinated axons and the pyramidal cell modules in monkey primary visual cortex , 1996, The Journal of comparative neurology.

[83]  K. Holthoff,et al.  Intrinsic optical signals in rat neocortical slices measured with near- infrared dark-field microscopy reveal changes in extracellular space , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[84]  D. Kiper,et al.  Growth of Callosal Terminal Arbors in Primary Visual Areas of the Cat , 1996, The European journal of neuroscience.

[85]  R. Pascher,et al.  Heterogeneity in the columnar number of neurons in different neocortical areas in the rat , 1996, Neuroscience Letters.

[86]  S. Juliano,et al.  Development of local connections in ferret somatosensory cortex , 1996, The Journal of comparative neurology.

[87]  A. Grinvald,et al.  Functional Organization for Direction of Motion and Its Relationship to Orientation Maps in Cat Area 18 , 1996, The Journal of Neuroscience.

[88]  The spread of excitation in neocortical columns visualized with infrared-darkfield videomicroscopy. , 1996, Neuroreport.

[89]  Keiji Tanaka,et al.  Columnar Organization in the Inferotemporal Cortex , 1997 .

[90]  R. Shapley,et al.  New perspectives on the mechanisms for orientation selectivity , 1997, Current Opinion in Neurobiology.

[91]  Javier DeFelipe,et al.  Double bouquet cell axons in the human temporal neocortex: relationship to bundles of myelinated axons and colocalization of calretinin and calbindin D-28k immunoreactivities , 1997, Journal of Chemical Neuroanatomy.

[92]  V. Mountcastle The columnar organization of the neocortex. , 1997, Brain : a journal of neurology.

[93]  Ikuo Taniguchi,et al.  The columnar and layer-specific response properties of neurons in the primary auditory cortex of Mongolian gerbils , 1997, Hearing Research.

[94]  K. Zilles,et al.  Neurobiological bases of behavioral development in the first year. , 1997, Neuropediatrics.

[95]  A. Peters,et al.  The organization of double bouquet cells in monkey striate cortex , 1997, Journal of neurocytology.

[96]  L. Gustafsson Inadequate cortical feature maps: A neural circuit theory of autism , 1997, Biological Psychiatry.

[97]  B L Whitsel,et al.  Optical imaging in vitro provides evidence for the minicolumnar nature of cortical response , 1997, Neuroreport.

[98]  A. Grinvald,et al.  Spatial Relationships among Three Columnar Systems in Cat Area 17 , 1997, The Journal of Neuroscience.

[99]  A. Braun,et al.  Asymmetry of chimpanzee planum temporale: humanlike pattern of Wernicke's brain language area homolog. , 1998, Science.

[100]  W. Shankle,et al.  Constructing the human cerebral cortex during infancy and childhood: Types and numbers of cortical columns and numbers of neurons in such columns at different age‐points , 1998, Acta paediatrica Japonica : Overseas edition.

[101]  J. Rilling,et al.  Planum temporale asymmetries in great apes as revealed by magnetic resonance imaging (MRI) , 1998, Neuroreport.

[102]  E. Callaway,et al.  Cytochrome-oxidase blobs and intrinsic horizontal connections of layer 2/3 pyramidal neurons in primate V1 , 1998, Visual Neuroscience.

[103]  B. Anderson,et al.  Anatomic asymmetries of the posterior superior temporal lobes: a postmortem study. , 1999, Neuropsychiatry, neuropsychology, and behavioral neurology.

[104]  H. Sato,et al.  Temporal Characteristics of Response Integration Evoked by Multiple Whisker Stimulations in the Barrel Cortex of Rats , 1999, The Journal of Neuroscience.

[105]  J. Pettigrew,et al.  Morphology of Pyramidal Neurones in Cytochrome Oxidase Modules of the S-I Bill Representation of the Platypus , 1999, Brain, Behavior and Evolution.

[106]  W Singer,et al.  Matching the modules: cortical maps and long-range intrinsic connections in visual cortex during development. , 1999, Journal of neurobiology.

[107]  Neurobiological bases of behavioral development in the second year. , 1999, Neuropediatrics.

[108]  L. C. Katz,et al.  Development of ocular dominance columns in the absence of retinal input , 1999, Nature Neuroscience.

[109]  W. G. Sannita,et al.  Synchronized ∼15.0–35.0Hz oscillatory response to spatially modulated visual patterns in man , 1999, Neuroscience.

[110]  L. Acsády,et al.  Postsynaptic targets of somatostatin-immunoreactive interneurons in the rat hippocampus , 1999, Neuroscience.

[111]  J. DeFelipe Chandelier cells and epilepsy. , 1999, Brain : a journal of neurology.

[112]  A. Keller,et al.  Thalamic-Evoked Synaptic Interactions in Barrel Cortex Revealed by Optical Imaging , 2000, The Journal of Neuroscience.

[113]  P. Jonas,et al.  Distal initiation and active propagation of action potentials in interneuron dendrites. , 2000, Science.

[114]  W. Singer,et al.  Interhemispheric asymmetries of the modular structure in human temporal cortex. , 2000, Science.

[115]  Functional neuroimaging in child psychiatry: Brain development and evolution , 2000 .

[116]  J. Lübke,et al.  Columnar Organization of Dendrites and Axons of Single and Synaptically Coupled Excitatory Spiny Neurons in Layer 4 of the Rat Barrel Cortex , 2000, The Journal of Neuroscience.

[117]  D. Buxhoeveden,et al.  Comparative lateralisation patterns in the language area of human, chimpanzee, and rhesus monkey brains , 2000, Laterality.

[118]  R. Miles,et al.  Diversity in Inhibition , 2000, Science.

[119]  G. Elston,et al.  Pyramidal Cells, Patches, and Cortical Columns: a Comparative Study of Infragranular Neurons in TEO, TE, and the Superior Temporal Polysensory Area of the Macaque Monkey , 2000, The Journal of Neuroscience.

[120]  Andrew Switala,et al.  Reduced interneuronal space in schizophrenia , 2000, Biological Psychiatry.

[121]  L. C. Katz,et al.  Early development of ocular dominance columns. , 2000, Science.

[122]  H. Kennedy,et al.  Non-uniformity of neocortex: areal heterogeneity of NADPH-diaphorase reactive neurons in adult macaque monkeys. , 2000, Cerebral cortex.

[123]  H. Stanley,et al.  Description of microcolumnar ensembles in association cortex and their disruption in Alzheimer and Lewy body dementias. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

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

[125]  H. Markram,et al.  Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. , 2000, Science.

[126]  E. G. Jones,et al.  Microcolumns in the cerebral cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[127]  A Grinvald,et al.  Long-Term Optical Imaging and Spectroscopy Reveal Mechanisms Underlying the Intrinsic Signal and Stability of Cortical Maps in V1 of Behaving Monkeys , 2000, The Journal of Neuroscience.

[128]  Andrew E. Switala,et al.  Quantitative analysis of cell columns in the cerebral cortex , 2000, Journal of Neuroscience Methods.

[129]  Evolutionary Anatomy of the Primate Cerebral Cortex: Neocortical expansion and elaboration during primate evolution: a view from neuroembryology , 2001 .

[130]  K. Gibson,et al.  Evolutionary Anatomy of the Primate Cerebral Cortex: Bigger is better: primate brain size in relationship to cognition , 2001 .

[131]  A. Agmon,et al.  Diverse Types of Interneurons Generate Thalamus-Evoked Feedforward Inhibition in the Mouse Barrel Cortex , 2001, The Journal of Neuroscience.

[132]  A. Agmon,et al.  Vertical bias in dendritic trees of non-pyramidal neocortical neurons expressing GAD67-GFP in vitro. , 2001, Cerebral cortex.

[133]  P. Goldman-Rakic,et al.  Prefrontal Microcircuits: Membrane Properties and Excitatory Input of Local, Medium, and Wide Arbor Interneurons , 2001, The Journal of Neuroscience.

[134]  R. Yuste,et al.  Stereotyped position of local synaptic targets in neocortex. , 2001, Science.

[135]  P. Goldman-Rakic,et al.  Coding Specificity in Cortical Microcircuits: A Multiple-Electrode Analysis of Primate Prefrontal Cortex , 2001, The Journal of Neuroscience.

[136]  Pasko Rakic,et al.  Telencephalic origin of human thalamic GABAergic neurons , 2001, Nature Neuroscience.

[137]  J. Budd,et al.  Local lateral connectivity of inhibitory clutch cells in layer 4 of cat visual cortex (area 17) , 2001, Experimental Brain Research.

[138]  D. Buxhoeveden,et al.  Lateralization of Minicolumns in Human Planum temporale Is Absent in Nonhuman Primate Cortex , 2001, Brain, Behavior and Evolution.

[139]  M Litaker,et al.  Morphological differences between minicolumns in human and nonhuman primate cortex. , 2001, American journal of physical anthropology.

[140]  S. Schultz Principles of Neural Science, 4th ed. , 2001 .

[141]  Michel A. Hofman,et al.  Evolutionary Anatomy of the Primate Cerebral Cortex: Brain evolution in hominids: are we at the end of the road? , 2001 .

[142]  D. Buxhoeveden,et al.  Asperger's Syndrome and Cortical Neuropathology , 2002, Journal of child neurology.

[143]  Lawrence C Katz,et al.  Ocular dominance development revisited , 2002, Current Opinion in Neurobiology.

[144]  K. Fleischhauer,et al.  Morphological characteristics of neocortical laminae when studied in tangential semithin sections through the visual cortex of the rabbit , 2004, Anatomy and Embryology.

[145]  C. Schmolke The ontogeny of dendrite bundles in rabbit visual cortex , 2004, Anatomy and Embryology.

[146]  Otto D. Creutzfeldt,et al.  Generality of the functional structure of the neocortex , 1977, Naturwissenschaften.

[147]  H. Petsche,et al.  Vertical bundles of dendrites in the neocortex , 2004, Zeitschrift für Anatomie und Entwicklungsgeschichte.

[148]  L. Garey,et al.  Neuronal architecture of the human temporal cortex , 2004, Anatomy and Embryology.

[149]  D. Buxhoeveden,et al.  The linear organization of cell columns in human and nonhuman anthropoid Tpt cortex , 1996, Anatomy and Embryology.

[150]  C. Viebahn,et al.  Dendrite bundles in lamina II/III of the rabbit neocortex , 2004, Anatomy and Embryology.