How is the vast brain communication system organized? A structural model relates connections to laminar differences between linked areas. The model is based on the principle of systematic structural variation in the cortex, extending from the simplest limbic cortices to eulaminate areas with elaborate lamination. The model accounts for laminar patterns and for the strength and topography of connections between nearby or distant cortices and subcortical structures, exemplified quantitatively for the principal and special prefrontal connections. Widespread connections of limbic areas and focal connections of eulaminate areas yield a broad range of circuit patterns for diverse functions. These diverse pathways innervate excitatory and functionally distinct inhibitory neurons, providing the basis for differential recruitment of areas for flexible behavior. Systematic structural variation likely emerges by timing differences in the development of distinct areas and has important implications for altered connections in diseases of developmental origin.


Article metrics loading...

Loading full text...

Full text loading...


Literature Cited

  1. Abbie AA. 1940. Cortical lamination in the Monotremata. J. Comp. Neurol. 72:429–67 [Google Scholar]
  2. Allman J, McGuinness E. 1988. Visual cortex in primates. See Steklis & Erwin 1988 279–326
  3. Ascoli GA, Alonso-Nanclares L, Anderson SA, Barrionuevo G, Benavides-Piccione R. et al. 2008. Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat. Rev. Neurosci. 9:557–68 [Google Scholar]
  4. Barbas H. 1986. Pattern in the laminar origin of corticocortical connections. J. Comp. Neurol. 252:415–22 [Google Scholar]
  5. Barbas H. 1993. Organization of cortical afferent input to orbitofrontal areas in the rhesus monkey. Neuroscience 56:841–64 [Google Scholar]
  6. Barbas H. 1995. Anatomic basis of cognitive-emotional interactions in the primate prefrontal cortex. Neurosci. Biobehav. Rev. 19:499–510 [Google Scholar]
  7. Barbas H. 2000. Complementary role of prefrontal cortical regions in cognition, memory and emotion in primates. Adv. Neurol. 84:87–110 [Google Scholar]
  8. Barbas H, Blatt GJ. 1995. Topographically specific hippocampal projections target functionally distinct prefrontal areas in the rhesus monkey. Hippocampus 5:511–33 [Google Scholar]
  9. Barbas H, García-Cabezas MA, Zikopoulos B. 2013. Frontal-thalamic circuits associated with language. Brain Lang. 126:49–61 [Google Scholar]
  10. Barbas H, Ghashghaei H, Dombrowski SM, Rempel-Clower NL. 1999. Medial prefrontal cortices are unified by common connections with superior temporal cortices and distinguished by input from memory-related areas in the rhesus monkey. J. Comp. Neurol. 410:343–67 [Google Scholar]
  11. Barbas H, Hilgetag CC, Saha S, Dermon CR, Suski JL. 2005. Parallel organization of contralateral and ipsilateral prefrontal cortical projections in the rhesus monkey. BMC Neurosci. 6:32 [Google Scholar]
  12. Barbas H, Pandya DN. 1989. Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey. J. Comp. Neurol. 286:353–75 [Google Scholar]
  13. Barbas H, Rempel-Clower N. 1997. Cortical structure predicts the pattern of corticocortical connections. Cereb. Cortex 7:635–46 [Google Scholar]
  14. Barone P, Batardiere A, Knoblauch K, Kennedy H. 2000. Laminar distribution of neurons in extrastriate areas projecting to visual areas V1 and V4 correlates with the hierarchical rank and indicates the operation of a distance rule. J. Neurosci. 20:3263–81 [Google Scholar]
  15. Bartos M, Vida I, Jonas P. 2007. Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat. Rev. Neurosci. 8:45–56 [Google Scholar]
  16. Benes FM, Vincent SL, Todtenkopf M. 2001. The density of pyramidal and nonpyramidal neurons in anterior cingulate cortex of schizophrenic and bipolar subjects. Biol. Psychiatry 50:395–406 [Google Scholar]
  17. Benowitz LI, Routtenberg A. 1997. GAP-43: an intrinsic determinant of neuronal development and plasticity. Trends Neurosci. 20:84–91 [Google Scholar]
  18. Brodmann K. 1909. Vergleichende Lokalisationslehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues Leipzig, Ger: Verlag von Johann Ambrosius Barth [Google Scholar]
  19. Bullmore E, Sporns O. 2012. The economy of brain network organization. Nat. Rev. Neurosci. 13:336–49 [Google Scholar]
  20. Bunce JG, Zikopoulos B, Feinberg M, Barbas H. 2013. Parallel prefrontal pathways reach distinct excitatory and inhibitory systems in memory-related rhinal cortices. J. Comp. Neurol. 512:4260–83 [Google Scholar]
  21. Buzsáki G, Wang XJ. 2012. Mechanisms of gamma oscillations. Annu. Rev. Neurosci. 35:203–25 [Google Scholar]
  22. Callaway EM. 1998. Local circuits in primary visual cortex of the macaque monkey. Annu. Rev. Neurosci. 21:47–74 [Google Scholar]
  23. Cannon J, McCarthy MM, Lee S, Lee J, Borgers C. et al. 2014. Neurosystems: brain rhythms and cognitive processing. Eur. J. Neurosci. 39:705–19 [Google Scholar]
  24. Canolty RT, Knight RT. 2010. The functional role of cross-frequency coupling. Trends Cogn. Sci. 14:506–15 [Google Scholar]
  25. Carmichael ST, Clugnet MC, Price JL. 1994. Central olfactory connections in the macaque monkey. J. Comp. Neurol. 346:403–34 [Google Scholar]
  26. Carter CS, Braver TS, Barch DM, Botvinick MM, Noll D, Cohen JD. 1998. Anterior cingulate cortex, error detection, and the online monitoring of performance. Science 280:747–49 [Google Scholar]
  27. Cassell MD, Wright DJ. 1986. Topography of projections from the medial prefrontal cortex to the amygdala in the rat. Brain Res. Bull. 17:321–33 [Google Scholar]
  28. Chao LL, Knight RT. 1997. Prefrontal deficits in attention and inhibitory control with aging. Cereb. Cortex 7:63–69 [Google Scholar]
  29. Charvet CJ, Cahalane DJ, Finlay BL. 2013. Systematic, cross-cortex variation in neuron numbers in rodents and primates. Cereb. Cortex 25:147–60 [Google Scholar]
  30. Chudasama Y, Robbins TW. 2003. Dissociable contributions of the orbitofrontal and infralimbic cortex to Pavlovian autoshaping and discrimination reversal learning: further evidence for the functional heterogeneity of the rodent frontal cortex. J. Neurosci. 23:8771–80 [Google Scholar]
  31. Collins CE, Airey DC, Young NA, Leitch DB, Kaas JH. 2010. Neuron densities vary across and within cortical areas in primates. PNAS 107:15927–32 [Google Scholar]
  32. Coogan TA, Burkhalter A. 1990. Conserved patterns of cortico-cortical connections define areal hierarchy in rat visual cortex. Exp. Brain Res. 80:49–53 [Google Scholar]
  33. Crick F. 1984. Function of the thalamic reticular complex: the searchlight hypothesis. PNAS 81:4586–90 [Google Scholar]
  34. Damasio AR. 1994. Descartes' Error: Emotion, Reason, and the Human Brain New York: Putnam [Google Scholar]
  35. Dart RA. 1934. The dual structure of the neopallium: its history and significance. J. Anat. 69:3–19 [Google Scholar]
  36. DeFelipe J. 1997. Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28K, parvalbumin and calretinin in the neocortex. J. Chem. Neuroanat. 14:1–19 [Google Scholar]
  37. DeFelipe J. 2002. Cortical interneurons: from Cajal to 2001. Prog. Brain Res. 136:215–38 [Google Scholar]
  38. DeFelipe J, López-Cruz PL, Benavides-Piccione R, Bielza C, Larrañaga P. et al. 2013. New insights into the classification and nomenclature of cortical GABAergic interneurons. Nat. Rev. Neurosci. 14:202–16 [Google Scholar]
  39. Dermon CR, Barbas H. 1994. Contralateral thalamic projections predominantly reach transitional cortices in the rhesus monkey. J. Comp. Neurol. 344:508–31 [Google Scholar]
  40. Dombrowski SM, Hilgetag CC, Barbas H. 2001. Quantitative architecture distinguishes prefrontal cortical systems in the rhesus monkey. Cereb. Cortex 11:975–88 [Google Scholar]
  41. Douglas RJ, Martin KA. 2004. Neuronal circuits of the neocortex. Annu. Rev. Neurosci. 27:419–51 [Google Scholar]
  42. Elston GN, Benavides-Piccione R, DeFelipe J. 2001. The pyramidal cell in cognition: a comparative study in human and monkey. J. Neurosci. 21:RC163 [Google Scholar]
  43. Fell J, Axmacher N. 2011. The role of phase synchronization in memory processes. Nat. Rev. Neurosci. 12:105–18 [Google Scholar]
  44. Felleman DJ, Van Essen DC. 1991. Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1:1–47 [Google Scholar]
  45. Funahashi S, Kubota K. 1994. Working memory and prefrontal cortex. Neurosci. Res. 21:1–11 [Google Scholar]
  46. Fuster JM. 1989. The Prefrontal Cortex New York: Raven Press [Google Scholar]
  47. Gabbott PLA, Bacon SJ. 1996. Local circuit neurons in the medial prefrontal cortex (areas 24a,b,c, 25 and 32) in the monkey: II. Quantitative areal and laminar distributions. J. Comp. Neurol. 364:609–36 [Google Scholar]
  48. Gabbott PLA, Warner TA, Jays PR, Salway P, Busby SJ. 2005. Prefrontal cortex in the rat: projections to subcortical autonomic, motor, and limbic centers. J. Comp. Neurol. 492:145–77 [Google Scholar]
  49. García-Cabezas MA, Barbas H. 2014. A direct anterior cingulate pathway to the primate primary olfactory cortex may control attention to olfaction. Brain Struct. Funct. 219:1735–54 [Google Scholar]
  50. García-Cabezas MA, Martínez-Sánchez P, Sánchez-González MA, Garzón M, Cavada C. 2009. Dopamine innervation in the thalamus: monkey versus rat. Cereb. Cortex 19:424–34 [Google Scholar]
  51. Ghashghaei HT, Barbas H. 2001. Neural interaction between the basal forebrain and functionally distinct prefrontal cortices in the rhesus monkey. Neuroscience 103:593–614 [Google Scholar]
  52. Ghashghaei HT, Barbas H. 2002. Pathways for emotions: interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey. Neuroscience 115:1261–79 [Google Scholar]
  53. Ghashghaei HT, Hilgetag CC, Barbas H. 2007. Sequence of information processing for emotions based on the anatomic dialogue between prefrontal cortex and amygdala. NeuroImage 34:905–23 [Google Scholar]
  54. Giguere M, Goldman-Rakic PS. 1988. Mediodorsal nucleus: areal, laminar, and tangential distribution of afferents and efferents in the frontal lobe of rhesus monkeys. J. Comp. Neurol. 277:195–213 [Google Scholar]
  55. Godlove DC, Maier A, Woodman GF, Schall JD. 2014. Microcircuitry of agranular frontal cortex: testing the generality of the canonical cortical microcircuit. J. Neurosci. 34:5355–69 [Google Scholar]
  56. Goldman-Rakic PS. 1988. Topography of cognition: parallel distributed networks in primate association cortex. Annu. Rev. Neurosci. 11:137–56 [Google Scholar]
  57. Goulas A, Uylings HB, Stiers P. 2014. Mapping the hierarchical layout of the structural network of the macaque prefrontal cortex. Cereb. Cortex 24:1178–94 [Google Scholar]
  58. Graybiel AM. 2008. Habits, rituals, and the evaluative brain. Annu. Rev. Neurosci. 31:359–87 [Google Scholar]
  59. Greengard P. 2001. The neurobiology of slow synaptic transmission. Science 294:1024–30 [Google Scholar]
  60. Groenewegen HJ, Uylings HB. 2000. The prefrontal cortex and the integration of sensory, limbic and autonomic information. Prog. Brain Res. 126:3–28 [Google Scholar]
  61. Haber SN. 2003. The primate basal ganglia: parallel and integrative networks. J. Chem. Neuroanat. 26:317–30 [Google Scholar]
  62. Hasselmo ME, Sarter M. 2011. Modes and models of forebrain cholinergic neuromodulation of cognition. Neuropsychopharmacology 36:52–73 [Google Scholar]
  63. Hegde J, Felleman DJ. 2007. Reappraising the functional implications of the primate visual anatomical hierarchy. Neuroscientist 13:416–21 [Google Scholar]
  64. Hilgetag CC, Grant S. 2010. Cytoarchitectural differences are a key determinant of laminar projection origins in the visual cortex. NeuroImage 51:1006–17 [Google Scholar]
  65. Hilgetag CC, Medalla M, Barbas H. 2008. Relationship of connection patterns to the architecture of the primate visual cortex. Soc. Neurosci. Meet. Plann. Abstr. 38 [Google Scholar]
  66. Hilgetag CC, O'Neill MA, Young MP. 1996. Indeterminate organization of the visual system. Science 271:776–77 [Google Scholar]
  67. Höistad M, Barbas H. 2008. Sequence of information processing for emotions through pathways linking temporal and insular cortices with the amygdala. NeuroImage 40:1016–33 [Google Scholar]
  68. Hubel DH, Wiesel TN. 1968. Receptive fields and functional architecture of monkey striate cortex. J. Physiol. 195:215–43 [Google Scholar]
  69. Insausti R, Munoz M. 2001. Cortical projections of the non-entorhinal hippocampal formation in the cynomolgus monkey (Macaca fascicularis). Eur. J. Neurosci. 14:435–51 [Google Scholar]
  70. Isaacson JS, Scanziani M. 2011. How inhibition shapes cortical activity. Neuron 72:231–43 [Google Scholar]
  71. Jones EG. 2007. The Thalamus New York: Cambridge Univ. Press [Google Scholar]
  72. Jones EG. 2009. The origins of cortical interneurons: mouse versus monkey and human. Cereb. Cortex 19:1953–56 [Google Scholar]
  73. Jongen-Relo AL, Amaral DG. 1998. Evidence for a GABAergic projection from the central nucleus of the amygdala to the brainstem of the macaque monkey: a combined retrograde tracing and in situ hybridization study. Eur. J. Neurosci. 10:2924–33 [Google Scholar]
  74. Kaas JH. 2008. The evolution of the complex sensory and motor systems of the human brain. Brain Res. Bull. 75:384–90 [Google Scholar]
  75. Kapfhammer JP, Schwab ME. 1994. Inverse patterns of myelination and GAP-43 expression in the adult CNS: neurite growth inhibitors as regulators of neuronal plasticity?. J. Comp. Neurol. 340:194–206 [Google Scholar]
  76. Kawaguchi Y, Kubota Y. 1997. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb. Cortex 7:476–86 [Google Scholar]
  77. Krubitzer L. 2009. In search of a unifying theory of complex brain evolution. Ann. N. Y. Acad. Sci. 1156:44–67 [Google Scholar]
  78. Lindquist KA, Wager TD, Kober H, Bliss-Moreau E, Barrett LF. 2012. The brain basis of emotion: a meta-analytic review. Behav. Brain Sci. 35:121–43 [Google Scholar]
  79. Lorente de Nó R. 1938. The cerebral cortex: architecture, intracortical connections and motor projections. Physiology of the Nervous System JF Fulton 291–325 London: Oxford Univ. Press [Google Scholar]
  80. Marin-Padilla M. 1970. Prenatal and early postnatal ontogenesis of the human motor cortex: a Golgi study. I. The sequential development of the cortical layers. Brain Res. 23:167–83 [Google Scholar]
  81. Markov NT, Vezoli J, Chameau P, Falchier A, Quilodran R. et al. 2014. Anatomy of hierarchy: feedforward and feedback pathways in macaque visual cortex. J. Comp. Neurol. 522:225–59 [Google Scholar]
  82. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C. 2004. Interneurons of the neocortical inhibitory system. Nat. Rev. Neurosci. 5:793–807 [Google Scholar]
  83. Massi L, Lagler M, Hartwich K, Borhegyi Z, Somogyi P, Klausberger T. 2012. Temporal dynamics of parvalbumin-expressing axo-axonic and basket cells in the rat medial prefrontal cortex in vivo. J. Neurosci. 32:16496–502 [Google Scholar]
  84. McDonald AJ. 1998. Cortical pathways to the mammalian amygdala. Prog. Neurobiol. 55:257–332 [Google Scholar]
  85. Medalla M, Barbas H. 2006. Diversity of laminar connections linking periarcuate and lateral intraparietal areas depends on cortical structure. Eur. J. Neurosci. 23:161–79 [Google Scholar]
  86. Medalla M, Barbas H. 2009. Synapses with inhibitory neurons differentiate anterior cingulate from dorsolateral prefrontal pathways associated with cognitive control. Neuron 61:609–20 [Google Scholar]
  87. Medalla M, Barbas H. 2010. Anterior cingulate synapses in prefrontal areas 10 and 46 suggest differential influence in cognitive control. J. Neurosci. 30:16068–81 [Google Scholar]
  88. Medalla M, Barbas H. 2014. Specialized prefrontal “auditory fields”: organization of primate prefrontal-temporal pathways. Front. Neurosci. 8:77 [Google Scholar]
  89. Medalla M, Lera P, Feinberg M, Barbas H. 2007. Specificity in inhibitory systems associated with prefrontal pathways to temporal cortex in primates. Cereb. Cortex 17:Suppl. 1i136–50 [Google Scholar]
  90. Meskenaite V. 1997. Calretinin-immunoreactive local circuit neurons in area 17 of the cynomolgus monkey, Macaca fascicularis. J. Comp. Neurol. 379:113–32 [Google Scholar]
  91. Mesulam M. 2008. Representation, inference, and transcendent encoding in neurocognitive networks of the human brain. Ann. Neurol. 64:367–78 [Google Scholar]
  92. Miller EK, Cohen JD. 2001. An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 24:167–202 [Google Scholar]
  93. Morecraft RJ, Geula C, Mesulam MM. 1992. Cytoarchitecture and neural afferents of orbitofrontal cortex in the brain of the monkey. J. Comp. Neurol. 323:341–58 [Google Scholar]
  94. Mountcastle VB. 1957. Modality and topographic properties of single neurons of cat's somatic sensory cortex. J. Neurophysiol. 20:408–34 [Google Scholar]
  95. Mountcastle VB. 1997. The columnar organization of the neocortex. Brain 120:Pt. 4701–22 [Google Scholar]
  96. Nauta WJH. 1971. The problem of the frontal lobe: a reinterpretation. J. Psychiatr. Res. 8:167–87 [Google Scholar]
  97. Nauta WJH. 1972. Neural associations of the frontal cortex. Acta Neurobiol. Exp. 32:125–40 [Google Scholar]
  98. Nauta WJH. 1979. Expanding borders of the limbic system concept. Functional Neurosurgery T Rasmussen, R Marino 7–23 New York: Raven Press [Google Scholar]
  99. Nauta WJH, Haymaker W. 1969. Hypothalamic nuclei and fiber connections. The Hypothalamus W Haymaker, E Anderson, WJH Nauta 136–209 Springfield, IL: Thomas [Google Scholar]
  100. O'Kusky J, Colonnier M. 1982. A laminar analysis of the number of neurons, glia, and synapses in the visual cortex (area 17) of adult macaque monkeys. J. Comp. Neurol. 210:278–90 [Google Scholar]
  101. Pandya DN, Seltzer B, Barbas H. 1988. Input-output organization of the primate cerebral cortex. See Steklis & Erwin 1988 39–80
  102. Pessoa L. 2013. The Cognitive-Emotional Brain Cambridge, MA: MIT Press [Google Scholar]
  103. Petersen CC. 2007. The functional organization of the barrel cortex. Neuron 56:339–55 [Google Scholar]
  104. Petrides M. 2000. Frontal lobes and memory. Handbook of Neuropsychology F Boller, J Grafman 67–84 Amsterdam: Elsevier Sci. [Google Scholar]
  105. Pinto A, Sesack SR. 2008. Ultrastructural analysis of prefrontal cortical inputs to the rat amygdala: spatial relationships to presumed dopamine axons and D1 and D2 receptors. Brain Struct. Funct. 213:159–75 [Google Scholar]
  106. Porrino LJ, Crane AM, Goldman-Rakic PS. 1981. Direct and indirect pathways from the amygdala to the frontal lobe in rhesus monkeys. J. Comp. Neurol. 198:121–36 [Google Scholar]
  107. Price JL. 2003. Comparative aspects of amygdala connectivity. Ann. N. Y. Acad. Sci. 985:50–58 [Google Scholar]
  108. Raizada RD, Grossberg S. 2003. Towards a theory of the laminar architecture of cerebral cortex: computational clues from the visual system. Cereb. Cortex 13:100–13 [Google Scholar]
  109. Rakic P. 2002. Neurogenesis in adult primate neocortex: an evaluation of the evidence. Nat. Rev. Neurosci. 3:65–71 [Google Scholar]
  110. Rakic P. 2009. Evolution of the neocortex: a perspective from developmental biology. Nat. Rev. Neurosci. 10:724–35 [Google Scholar]
  111. Ray RD, Zald DH. 2012. Anatomical insights into the interaction of emotion and cognition in the prefrontal cortex. Neurosci. Biobehav. Rev. 36:479–501 [Google Scholar]
  112. Rempel-Clower NL, Barbas H. 1998. Topographic organization of connections between the hypothalamus and prefrontal cortex in the rhesus monkey. J. Comp. Neurol. 398:393–419 [Google Scholar]
  113. Rempel-Clower NL, Barbas H. 2000. The laminar pattern of connections between prefrontal and anterior temporal cortices in the rhesus monkey is related to cortical structure and function. Cereb. Cortex 10:851–65 [Google Scholar]
  114. Robbins TW, Arnsten AFT. 2009. The neuropsychopharmacology of fronto-executive function: monoaminergic modulation. Annu. Rev. Neurosci. 32:267–87 [Google Scholar]
  115. Rockel AJ, Hiorns RW, Powell TP. 1980. The basic uniformity in structure of the neocortex. Brain 103:221–44 [Google Scholar]
  116. Rockland KS, Pandya DN. 1979. Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey. Brain Res. 179:3–20 [Google Scholar]
  117. Romanski LM, Averbeck BB. 2009. The primate cortical auditory system and neural representation of conspecific vocalizations. Annu. Rev. Neurosci. 32:315–46 [Google Scholar]
  118. Rosene DL, Van Hoesen GW. 1977. Hippocampal efferents reach widespread areas of cerebral cortex and amygdala in the rhesus monkey. Science 198:315–17 [Google Scholar]
  119. Saha S, Batten TF, Henderson Z. 2000. A GABAergic projection from the central nucleus of the amygdala to the nucleus of the solitary tract: a combined anterograde tracing and electron microscopic immunohistochemical study. Neuroscience 99:613–26 [Google Scholar]
  120. Salzman CD, Fusi S. 2010. Emotion, cognition, and mental state representation in amygdala and prefrontal cortex. Annu. Rev. Neurosci. 33:173–202 [Google Scholar]
  121. Sanides F. 1970. Functional architecture of motor and sensory cortices in primates in the light of a new concept of neocortex evolution. The Primate Brain: Advances in Primatology CR Noback, W Montagna 137–208 New York: Appleton-Century-Crofts Educational Division/Meredith Corporation [Google Scholar]
  122. Schmahmann JD, Pandya DN. 2008. Disconnection syndromes of basal ganglia, thalamus, and cerebrocerebellar systems. Cortex 44:1037–66 [Google Scholar]
  123. Schroeder CE, Lakatos P. 2009. Low-frequency neuronal oscillations as instruments of sensory selection. Trends Neurosci. 32:9–18 [Google Scholar]
  124. Sesack SR, Deutch AY, Roth RH, Bunney BS. 1989. Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin. J. Comp. Neurol. 290:213–42 [Google Scholar]
  125. Shepherd GM. 2011. The microcircuit concept applied to cortical evolution: from three-layer to six-layer cortex. Front. Neuroanat. 5:30 [Google Scholar]
  126. Sherman SM, Guillery RW. 1996. Functional organization of thalamocortical relays. J. Neurophysiol. 76:1367–95 [Google Scholar]
  127. Sohal VS, Zhang F, Yizhar O, Deisseroth K. 2009. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459:698–702 [Google Scholar]
  128. Steklis HD, Erwin J. 1988. Comparative Primate Biology 4 Neurosciences New York: Alan R. Liss [Google Scholar]
  129. Timbie C, Barbas H. 2014. Specialized pathways from the primate amygdala to posterior orbitofrontal cortex. J. Neurosci. 34:8106–18 [Google Scholar]
  130. Tognoli E, Kelso JA. 2014. The metastable brain. Neuron 81:35–48 [Google Scholar]
  131. Turner BH, Mishkin M, Knapp M. 1980. Organization of the amygdalopetal projections from modality-specific cortical association areas in the monkey. J. Comp. Neurol. 191:515–43 [Google Scholar]
  132. Uylings HB, Groenewegen HJ, Kolb B. 2003. Do rats have a prefrontal cortex?. Behav. Brain Res. 146:3–17 [Google Scholar]
  133. Vertes RP. 2004. Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 51:32–58 [Google Scholar]
  134. Vertes RP. 2006. Interactions among the medial prefrontal cortex, hippocampus and midline thalamus in emotional and cognitive processing in the rat. Neuroscience 142:1–20 [Google Scholar]
  135. Vogt BA, Hof PR, Zilles K, Vogt LJ, Herold C, Palomero-Gallagher N. 2013. Cingulate area 32 homologies in mouse, rat, macaque and human: cytoarchitecture and receptor architecture. J. Comp. Neurol. 521:4189–204 [Google Scholar]
  136. Vogt BA, Pandya DN. 1987. Cingulate cortex of the rhesus monkey: II. Cortical afferents. J. Comp. Neurol. 262:271–89 [Google Scholar]
  137. von Economo C. 2009 (1927). Cellular Structure of the Human Cerebral Cortex transl./ed. LC Thriarhou Basel, Switz.: Karger [Google Scholar]
  138. Wang XJ, Tegner J, Constantinidis C, Goldman-Rakic PS. 2004. Division of labor among distinct subtypes of inhibitory neurons in a cortical microcircuit of working memory. PNAS 101:1368–73 [Google Scholar]
  139. Wonders CP, Anderson SA. 2006. The origin and specification of cortical interneurons. Nat. Rev. Neurosci. 7:687–96 [Google Scholar]
  140. Woodruff A, Yuste R. 2008. Of mice and men, and chandeliers. PLOS Biol. 6:e243 [Google Scholar]
  141. Xu X, Roby KD, Callaway EM. 2010. Immunochemical characterization of inhibitory mouse cortical neurons: three chemically distinct classes of inhibitory cells. J. Comp. Neurol. 518:389–404 [Google Scholar]
  142. Yakovlev PI. 1948. Motility, behavior and the brain: stereodynamic organization and neurocoordinates of behavior. J. Nerv. Ment. Dis. 107:313–35 [Google Scholar]
  143. Yeterian EH, Pandya DN, Tomaiuolo F, Petrides M. 2012. The cortical connectivity of the prefrontal cortex in the monkey brain. Cortex 48:58–81 [Google Scholar]
  144. Zaborszky L, Csordas A, Mosca K, Kim J, Gielow MR. et al. 2013. Neurons in the basal forebrain project to the cortex in a complex topographic organization that reflects corticocortical connectivity patterns: an experimental study based on retrograde tracing and 3D reconstruction. Cereb. Cortex 25:118–37 [Google Scholar]
  145. Zikopoulos B, Barbas H. 2007a. Circuits for multisensory integration and attentional modulation through the prefrontal cortex and the thalamic reticular nucleus in primates. Rev. Neurosci. 18:417–38 [Google Scholar]
  146. Zikopoulos B, Barbas H. 2007b. Parallel driving and modulatory pathways link the prefrontal cortex and thalamus. PLOS ONE 2:e848 [Google Scholar]
  147. Zikopoulos B, Barbas H. 2010. Changes in prefrontal axons may disrupt the network in autism. J. Neurosci. 30:14595–609 [Google Scholar]
  148. Zikopoulos B, Barbas H. 2012. Pathways for emotions and attention converge on the thalamic reticular nucleus in primates. J. Neurosci. 32:5338–50 [Google Scholar]

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error