Intrinsic Connections of the Auditory Cortex

  • Mark N. Wallace
  • Jufang He


The patterns of connectivity between cortical neurons define and constrain the basic functional organization of the neocortex. Understanding the local and long distance connections is a prerequisite for developing an integrative description of cortical structure and function. The circuits to which such cells contribute likely control perception and action.


Pyramidal Cell Auditory Cortex Layer Versus Inhibitory Interneuron Apical Dendrite 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



auditory cortex


primary auditory cortex


second auditory cortical area


brain-derived neurotrophic factor


bipolar cell


bitufted cell




cannabinoid receptor Type 1


chandelier cell


double bouquet cell


extraverted multipolar cell


fibroblast growth factor




γ-aminobutyric acid


horizontal bitufted cell


horizontal cell


intrinsic bursting


large basket cell


large multipolar cell




low-threshold spiking


Martinotti cell


medium basket cell


medial geniculate body


medium multipolar cell


nest basket cells




neurogliaform cell




neuron with axonal arcade


pyramidal cell




regular spiking


small basket cell


small multipolar cell




superior temporal gyrus



We thank Alan Palmer for helpful comments.


  1. Alcantara S, Pozas E, Ibanez CF, and Soriano E (2006) BDNF-modulated spatial organization of Cajal-Retzius and GABAergic neurons in the marginal zone plays a role in the development of cortical organization. Cerebral Cortex 16:487–499.CrossRefPubMedGoogle Scholar
  2. Ang Jr ESBC, Haydar TF, Gluncic V, and Rakic P (2003) Four-dimensional migratory coordinates of GABAergic interneurons in the developing mouse cortex. Journal of Neuroscience 23:5805–5815.PubMedGoogle Scholar
  3. Angelucci A, Clasca F, and Sur M (1998) Brainstem inputs to the ferret medial geniculate nucleus and the effect of early deafferentation on novel retinal projections to the auditory thalamus. Journal of Comparative Neurology 400:417–439.CrossRefPubMedGoogle Scholar
  4. Berghuis P, Dobszay MB, Wang XY, Spano S, Ledda F, Sousa KM, Schulte G, Ernfors P, Mackie K, Paratcha G, Hurd YL, and Harkany T (2005) Endocannabinoids regulate interneuron migration and morphogenesis by transactivating the TrkB receptor. Proceedings of the National Academy of Sciences of the United States of America 102:19115–19120.CrossRefPubMedGoogle Scholar
  5. Binzegger T, Douglas RJ, and Martin KAC (2004) A quantitative map of the circuit of cat primary visual cortex. Journal of Neuroscience 24:8441–8453.CrossRefPubMedGoogle Scholar
  6. Buxhoeveden DP and Casanova MF (2002) The minicolumn hypothesis in neuroscience. Brain 125:935–951.CrossRefPubMedGoogle Scholar
  7. Callaway EM (1998) Local circuits in primary visual cortex of the macaque monkey. Annual Review of Neuroscience 21:47–74.CrossRefPubMedGoogle Scholar
  8. Castellani V and Bolz J (1999) Opposing roles for neurotrophin-3 in targeting and collateral formation of distinct sets of developing cortical neurons. Development 126:3335–3345.PubMedGoogle Scholar
  9. Chiry O. Tardif E, Magistretti PJ, and Clarke S (2003) Patterns of calcium-binding proteins support parallel and hierarchical organization of human auditory areas. European Journal of Neuroscience 17:397–410.CrossRefPubMedGoogle Scholar
  10. Clarke S and Rivier F (1998) Compartments within human primary auditory cortex: evidence from cytochrome oxidase and acetylcholinesterase staining. European Journal of Neuroscience 10:741–745.CrossRefPubMedGoogle Scholar
  11. Clemo HR, Keniston L, and Meredith MA (2003) A comparison of the distribution of GABA-ergic neurons in cortices representing different sensory modalities. Journal of Chemical Neuroanatomy 26:51–63.CrossRefPubMedGoogle Scholar
  12. Cline H (2003) Sperry and Hebb: oil and vinegar? Trends in Neurosciences 26:655–661.CrossRefPubMedGoogle Scholar
  13. Dean C and Dresbach T (2006) Neuroligins and neurexins: linking cell adhesion, synapse formation and cognitive function. Trends in Neurosciences 29:21–29.CrossRefPubMedGoogle Scholar
  14. DeFelipe J (2002a) Cortical interneurons: from Cajal to 2001. Progress in Brain Research 136:215–238.CrossRefPubMedGoogle Scholar
  15. DeFelipe J, Alonso-Nanclares L, and Arellano JI (2002b) Microstructure of the neocortex: comparative aspects. Journal of Neurocytology 31:299–316.CrossRefPubMedGoogle Scholar
  16. DeFelipe J, Hendry SHC, Hashikawa T, Molinari M, and Jones EG (1990) A microcolumnar structure of monkey cerebral cortex revealed by immunocytochemical studies of double bouquet cell axons. Neuroscience 37:655–673.CrossRefPubMedGoogle Scholar
  17. del Rio MR and DeFelipe J (1995) A light and electron microscopic study of calbindin D-28 k immunoreactive double bouquet cells in the human temporal cortex. Brain Research 690:133–140.CrossRefPubMedGoogle Scholar
  18. Douglas RJ and Martin KAC (2004) Neuronal circuits of the neocortex. Annual Review of Neuroscience 27:419–451.CrossRefPubMedGoogle Scholar
  19. Eder M, Rammes G, Zieglgansberger W, and Dodt H-U (2001) GABAA and GABAB receptors on neocortical neurons are differentially distributed. European Journal of Neuroscience 13:1065–1069.CrossRefPubMedGoogle Scholar
  20. Ehret G (1997) The auditory cortex. Journal of Comparative Physiology (A) 181:547–557.CrossRefGoogle Scholar
  21. Feldman ML and Peters A (1974) A study of barrels and pyramidal dendritic clusters in the cerebral cortex. Brain Research 77:55–76.CrossRefPubMedGoogle Scholar
  22. Fitzpatrick DC and Henson OW Jr (1994) Cell types in the mustached bat auditory cortex. Brain Behavior and Evolution 43:79–91.CrossRefGoogle Scholar
  23. Foeller E, Vater M, and Kössl M (2001) Laminar analysis of inhibition in the gerbil primary auditory cortex. Journal of the Association for Research in Otolaryngology 2:279–296.PubMedGoogle Scholar
  24. Fukuchi-Shimogori T and Grove EA (2001) Neocortex patterning by the secreted signaling molecule FGF8. Science 294:1071–1074.CrossRefPubMedGoogle Scholar
  25. Galuske RAW, Schlote W, Bratzke H, and Singer W (2000) Interhemispheric asymmetries of the modular structure in human temporal cortex. Science 289:1946–1949.CrossRefPubMedGoogle Scholar
  26. Gao W-J and Pallas SL (1999) Cross-modal reorganization of horizontal connectivity in auditory cortex without altering thalamocortical projections. Journal of Neuroscience 19:7940–7950.PubMedGoogle Scholar
  27. Gillespie DC, Kim G, and Kandler K (2005) Inhibitory synapses in the developing auditory system are glutamatergic. Nature Neuroscience 8:332–338.CrossRefPubMedGoogle Scholar
  28. Hackett TA, Preuss TM, and Kaas JH (2001) Architectonic identification of the core region in auditory cortex of macaques, chimpanzees, and humans. Journal of Comparative Neurology 441:197–222.CrossRefPubMedGoogle Scholar
  29. He J (2003) Slow oscillation in non-lemniscal auditory thalamus. Journal of Neuroscience 23:8281–8290.PubMedGoogle Scholar
  30. He JF and Hu B (2002) Differential distribution of burst and single-spike responses in auditory thalamus. Journal of Neurophysiology 88:2152–2156.CrossRefPubMedGoogle Scholar
  31. Hefti BJ and Smith PH (2000) Anatomy, physiology, and synaptic responses of rat layer V auditory cortical cells and effects of intracellular GABAA blockade. Journal of Neurophysiology 83:2626–2638.PubMedGoogle Scholar
  32. Hefti BJ and Smith PH (2003) Distribution and kinetic properties of GABAergic inputs to layer V pyramidal cells in rat auditory cortex. Journal of the Association for Research in Otolaryngology 4:106–121.CrossRefPubMedGoogle Scholar
  33. Hendry SHC and Jones EG (1991) GABA neuronal subpopulation in cat primary auditory cortex: co-localization with calcium binding proteins. Brain Research 543:45–55.CrossRefPubMedGoogle Scholar
  34. Hestrin S and Galarreta M (2005) Electrical synapses define networks of neocortical GABAergic neurons. Trends in Neurosciences 28:304–309.CrossRefPubMedGoogle Scholar
  35. Horton JC and Adams DL (2005) The cortical column: a structure without a function. Philosophical Transactions of the Royal Society B 360:837–862.CrossRefGoogle Scholar
  36. Issa NP (2003) Inhibitory circuits in sensory maps develop through excitation. Trends in Neurosciences 26:456–458.CrossRefPubMedGoogle Scholar
  37. Jones EG (2000) Microcolumns in the cerebral cortex. Proceedings of the National Academy of Sciences of the United States of America 97:5019–5021.CrossRefPubMedGoogle Scholar
  38. Kawaguchi Y and Kubota Y (1997) GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cerebral Cortex 7:476–486.CrossRefPubMedGoogle Scholar
  39. Kozloski J, Hamzei-Sichani F, and Yuste R (2001) Stereotyped position of local synaptic targets in neocortex. Science 293:868–872.CrossRefPubMedGoogle Scholar
  40. Letinic K, Zoncu R, and Rakic P (2002) Origin of GABAergic neurons in the human neocortex. Nature 417:645–649.CrossRefPubMedGoogle Scholar
  41. Linden JF and Schreiner CE.(2003) Columnar transformations in auditory cortex? A comparison to visual and somatosensory cortices. Cerebral Cortex 13:83–89.CrossRefPubMedGoogle Scholar
  42. Maravall M, Koh IYY, Lindquist WB, and Svoboda K (2004) Experience-dependent changes in basal dendritic branching of layer 2/3 pyramidal neurons during a critical period for developmental plasticity in rat barrel cortex. Cerebral Cortex 14:655–664.CrossRefPubMedGoogle Scholar
  43. Margrie TW, Meyer AH, Caputi A, Monyer H, Hasan MT, Schaefer AT, Denk W, and Brecht M (2003) Targeted whole-cell recordings in the mammalian brain in vivo. Neuron 39:911–918.CrossRefPubMedGoogle Scholar
  44. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, and Wu C (2004) Interneurons of the neocortical inhibitory system. Nature Reviews Neuroscience 5:793–807.CrossRefPubMedGoogle Scholar
  45. McMullen NT and de Venecia RK (1993) Thalamocortical patches in auditory neocortex. Brain Research 620:317–322.CrossRefPubMedGoogle Scholar
  46. Meyer G, Gonzalez-Hernandez TH, and Ferres-Torres R (1989) The spiny stellate neurons in layer IV of the human auditory cortex. A Golgi study. Neuroscience 33:489–498.CrossRefPubMedGoogle Scholar
  47. Miller LM, Escabí MA, Read HL, and Schreiner CE (2001) Functional convergence of response properties in the auditory thalamocortical system. Neuron 32:151–160.CrossRefPubMedGoogle Scholar
  48. Mitani A, Shimokouchi M, Itoh K, Nomura S, Kudo M, and Mizuno N (1985) Morphology and laminar organization of electrophysiologically identified neurons in the primary auditory cortex in the cat. Journal of Comparative Neurology 235:430–447.CrossRefPubMedGoogle Scholar
  49. Morel A, Garraghty PE, and Kaas JH (1993) Tonotopic organization, architectonic fields, and connections of auditory cortex in macaque monkeys. Journal of Comparative Neurology 335:437–459.CrossRefPubMedGoogle Scholar
  50. Morel A and Kaas JH (1992) Subdivisions and connections of auditory cortex in owl monkeys. Journal of Comparative Neurology 318:27–63.CrossRefPubMedGoogle Scholar
  51. Mountcastle VB (1997) The columnar organization of the neocortex. Brain 120:701–722.CrossRefPubMedGoogle Scholar
  52. Mountcastle VB (2003) Introduction. Cerebral Cortex 13:2–4.CrossRefPubMedGoogle Scholar
  53. Nelken I (2004) Processing of complex stimuli and natural scenes in the auditory cortex. Current Opinion in Neurobiology 14:474–480.CrossRefPubMedGoogle Scholar
  54. Ojima H, Honda CN, and Jones EG (1991) Patterns of axon collateralization of identified supragranular pyramidal neurons in the cat auditory cortex. Cerebral Cortex 1:80–94.CrossRefPubMedGoogle Scholar
  55. Ojima H, Honda CN, and Jones EG (1992) Characteristics of intracellularly injected infragranular pyramidal neurons in cat primary auditory cortex. Cerebral Cortex 2:197–216.CrossRefPubMedGoogle Scholar
  56. Peters A (2002) Examining neocortical circuits: some background and facts. Journal of Neurocytology 31:183–193.CrossRefPubMedGoogle Scholar
  57. Peters A and Sethares C (1997) The organization of double bouquet cells in monkey striate cortex. Journal of Neurocytology 26:779–797.CrossRefPubMedGoogle Scholar
  58. Polleux F, Whitford KL, Dijkhuizen PA, Vitalis T, and Ghosh A (2002) Control of cortical interneuron migration by neurotrophins and P13-kinase signaling. Development 129:3147–3160.PubMedGoogle Scholar
  59. Price DJ, Kennedy H, Dehay C, Zhou L, Mercier M, Jossin Y, Goffinet AM, Tissir F, Blakey D, and Molnar Z (2006) The development of cortical connections. European Journal of Neuroscience 23:910–920.CrossRefPubMedGoogle Scholar
  60. Prieto JJ, Peterson BA, and Winer JA (1994a) Morphology and spatial distribution of GABAergic neurons in cat primary auditory cortex (AI). Journal of Comparative Neurology 344:349–382.CrossRefPubMedGoogle Scholar
  61. Prieto JJ, Peterson BA, and Winer JA (1994b) Laminar distribution and neuronal targets of GABAergic axon terminals in cat primary auditory cortex (AI). Journal of Comparative Neurology 344:383–402.CrossRefPubMedGoogle Scholar
  62. Prieto JJ and Winer JA (1999) Layer VI in cat primary auditory cortex: Golgi study and sublaminar origins of projection neurons. Journal of Comparative Neurology 404:332–358.CrossRefPubMedGoogle Scholar
  63. Rakic P (1995) A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution. Trends in Neurosciences 18:383–388.CrossRefPubMedGoogle Scholar
  64. Read HL, Winer JA, and Schreiner CE (2001) Modular organization of intrinsic connections associated with spectral tuning in cat auditory cortex. Proceedings of the National Academy of Sciences of the United States of America 98:8042–8047.CrossRefGoogle Scholar
  65. Rockland KS and Ichinohe N (2004) Some thoughts on cortical minicolumns. Experimental Brain Research 158:265–277.CrossRefGoogle Scholar
  66. Roe AW, Pallas SL, Kwon YH, and Sur M (1992) Visual projections routed to the auditory pathway in ferrets: receptive fields of visual neurons in primary auditory cortex. Journal of Neuroscience 12:3651–3664.PubMedGoogle Scholar
  67. Rouiller EM and de Ribaupierre F (1990) Arborization of corticothalamic axons in the auditory thalamus of the cat: a PHA-L tracing study. Neuroscience Letters 108:29–35.CrossRefPubMedGoogle Scholar
  68. Sherrington CS (1933) The Brain and Its Mechanism. Cambridge University Press, London.Google Scholar
  69. Sincich LC, Adams DL, and Horton JC (2003) Complete flatmounting of the macaque cerebral cortex. Visual Neuroscience 20:663–686.CrossRefPubMedGoogle Scholar
  70. Smith PH and Populin LC (2001) Fundamental differences between the thalamocortical recipient layers of the cat auditory and visual cortices. Journal of Comparative Neurology 436:508–519.CrossRefPubMedGoogle Scholar
  71. Sur M, Angelucci A, and Sharma J (1999) Rewiring cortex: the role of patterned activity in development and plasticity of neocortical circuits. Journal of Neurobiology 41:33–43.CrossRefPubMedGoogle Scholar
  72. Sur M and Rubenstein JLR (2005) Patterning and plasticity of the cerebral cortex. Science 310:805–810.CrossRefPubMedGoogle Scholar
  73. Szabadics J, Varga C, Molnar G, Olah S, Barzo P, and Tamas G (2006) Excitatory effect of GABAergic axo-axonic cells in cortical microcircuits Science 311:233–235.CrossRefPubMedGoogle Scholar
  74. Thomson AM and Bannister AP (1998) Postsynaptic pyramidal target selection by descending layer III pyramidal axons: dual intracellular recordings and biocytin filling in slices of rat neocortex. Neuroscience 84:669–683.CrossRefPubMedGoogle Scholar
  75. Thomson AM and Bannister AP (2003) Interlaminar connections in the neocortex. Cerebral Cortex 13:5–14.CrossRefPubMedGoogle Scholar
  76. Thomson AM and Morris OT (2002) Selectivity in the inter-laminar connections made by neocortical neurones. Journal of Neurocytology 31:239–246.CrossRefPubMedGoogle Scholar
  77. Valcanis H and Tan S-S (2003) Layer specification of transplanted interneurons in developing mouse neocortex. Journal of Neuroscience 23:5113–5122.PubMedGoogle Scholar
  78. Viebahn C (1990) Correlation between differences in the structure of dendrite bundles and cytoarchitectonic patterns in the cerebral cortex of the rabbit. Journal für Hirnforschung 31:645–652.PubMedGoogle Scholar
  79. Wallace, M.N. and Bajwa, S. (1991) Patchy intrinsic connections of the ferret primary auditory cortex. Neuroreport 2:417–420.CrossRefPubMedGoogle Scholar
  80. Wallace MN, Johnston PW, and Palmer AR (2002) Histochemical identification of cortical areas in the auditory region of the human brain. Experimental Brain Research 143:499–508.CrossRefGoogle Scholar
  81. Wallace MN, Kitzes LM, and Jones EG (1991) Intrinsic inter- and intralaminar connections and their relationship to the tonotopic map in cat primary auditory cortex. Experimental Brain Research 86:527–544.Google Scholar
  82. Watts J and Thomson AM (2005) Excitatory and inhibitory connections show selectivity in the neocortex. Journal of Physiology 562:89–97.CrossRefPubMedGoogle Scholar
  83. White EL (2002) Specificity of cortical synaptic connectivity: emphasis on perspectives gained from quantitative electron microscopy. Journal of Neurocytology 31:195–202.CrossRefPubMedGoogle Scholar
  84. Winer JA (1992) The functional architecture of the medial geniculate body and the primary auditory cortex. In: Webster DB, Popper AN, and Fay RR (eds). Springer Handbook of Auditory Research, volume 1, The Mammalian Auditory Pathway: Neuroanatomy. Springer, New York, pp. 222–409.Google Scholar
  85. Winer JA, Larue DT, and Huang CL (1999) Two systems of giant axon terminals in the cat medial geniculate body: convergence of cortical and GABAergic inputs. Journal of Comparative Neurology 413:181–197.CrossRefPubMedGoogle Scholar
  86. Winer JA and Prieto JJ (2001) Layer V in cat primary auditory cortex (AI): cellular architecture and identification of projection neurons. Journal of Comparative Neurology 434:379–412.CrossRefPubMedGoogle Scholar
  87. Woo NH and Lu B (2006) Regulation of cortical interneurons by neurotrophins: from development to cognitive disorders. Neuroscientist 12:43–56.CrossRefPubMedGoogle Scholar
  88. Xu Q, Cobos I, de la Cruz E, Rubenstein JL, and Anderson SA (2004) Origins of cortical interneuron subtypes. Journal of Neuroscience 24:2612–2622.CrossRefPubMedGoogle Scholar
  89. Yanez IB, Munoz A, Contreras J, Gonzalez J, Rodriguez-Veiga E, and DeFelipe J (2005) Double bouquet cell in the human cerebral cortex and a comparison with other mammals. Journal of Comparative Neurology 486:344–360.CrossRefPubMedGoogle Scholar
  90. Zhang LI, Tan AYY, Schreiner CE, and Merzenich MM (2003) Topography and synaptic shaping of direction selectivity in primary auditory cortex. Nature 424:201–205.CrossRefPubMedGoogle Scholar
  91. Zhang ZW and Deschênes M (1997) Intracortical axonal projections of lamina VI cells of the primary somatosensory cortex in the rat: a single-cell labeling study. Journal of Neuroscience 17:6365–6379.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  1. 1.Medical Research Council Institute of Hearing Research, University ParkNottinghamUK
  2. 2.Department of Rehabilitation SciencesThe Hong Kong Polytechnic UniversityKowloonHong Kong

Personalised recommendations