Role of Afferent Activity in the Development of Cortical Specification

  • Alvin W. Lyckman
  • Mriganka Sur
Part of the Results and Problems in Cell Differentiation book series (RESULTS, volume 39)


The surgical cross-modal rewiring paradigm is an experimental method for examining the physiological and anatomical consequences of exposing developing cortical subregions to specific types of patterned sensory inputs. Data from these experiments provide strong inferences about the role of extrinsic (subcortical) cortical inputs in shaping the local cortical networks that organize and process sensory information. Behavioral results from this work also suggest that such activity (and activity in general) is a profound organizer of cerebral connectivity. We discuss one future direction of these studies: the implication that extrinsic inputs regulate developmental genes that are responsible for refining the connectivity within local circuits, and a strategy to discover and characterize such genes.


Primary Auditory Cortex Medial Geniculate Body Orientation Tuning Usher Syndrome Retinal Ganglion Cell Axon 
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.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Allison JD, Casagrande VA, Bonds AB (1995) The influence of input from the lower cortical layers on the orientation tuning of upper layer V1 cells in a primate. Vis Neurosci 12:309–320PubMedCrossRefGoogle Scholar
  2. Angelucci A, Clasca F, Bricolo E, Cramer KS, Sur M (1997) Experimentally induced retinal projections to the ferret auditory thalamus: development of clustered eye-specific patterns in a novel target. J Neurosci 17:2040–2055PubMedGoogle Scholar
  3. Angelucci A, Clasca F, 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. J Comp Neurol 400:417–439PubMedCrossRefGoogle Scholar
  4. Antonini A, Fagiolini M, Stryker MP (1999) Anatomical correlates of functional plasticity in mouse visual cortex. J Neurosci 19:4388–4406PubMedGoogle Scholar
  5. Bakin JS, Kwon MC, Masino SA, Weinberger NM, Frostig RD (1996) Suprathreshold auditory cortex activation visualized by intrinsic signal optical imaging. Cereb Cortex 6:120–130PubMedCrossRefGoogle Scholar
  6. Bishop KM, Goudreau G, O’Leary DD (2000) Regulation of area identity in the mammalian neocortex by Emx2 and Pax6. Science 288:344–349PubMedCrossRefGoogle Scholar
  7. Blasdel GG, Salama G (1986) Voltage-sensitive dyes reveal a modular organization in monkey striate cortex. Nature 321:579–585PubMedCrossRefGoogle Scholar
  8. Boyd J, Matsubara J (1991) Intrinsic connections in cat visual cortex: a combined anterograde and retrograde tracing study. Brain Res 560:207–215PubMedCrossRefGoogle Scholar
  9. Brosch M, Schreiner CE (2000) Sequence sensitivity of neurons in cat primary auditory cortex. Cereb Cortex 10:1155–1167PubMedCrossRefGoogle Scholar
  10. Catalano SM, Shatz CJ (1998) Activity-dependent cortical target selection by thalamic axons. Science 281:559–562PubMedCrossRefGoogle Scholar
  11. Chapman B, Zahs KR, Stryker MP (1991) Relation of cortical cell orientation selectivity to alignment of receptive fields of the geniculocortical afferents that arborize within a single orientation column in ferret visual cortex. J Neurosci 11:1347–1358PubMedGoogle Scholar
  12. Corriveau RA (1999) Electrical activity and gene expression in the development of vertebrate neural circuits. J Neurobiol 41:148–157PubMedCrossRefGoogle Scholar
  13. Crook JM, Eysel UT (1992) GABA-induced inactivation of functionally characterized sites in cat visual cortex (area 18): effects on orientation tuning. J Neurosci 12:1816–1825PubMedGoogle Scholar
  14. Crook JM, Kisvarday ZF, Eysel UT (1996) GABA-induced inactivation of functionally characterized sites in cat visual cortex (area 18): effects on direction selectivity. J Neurophysiol 75: 2071–2088PubMedGoogle Scholar
  15. Dinse HR, Godde B, Hilger T, Reuter G, Cords SM, Lenarz T, von Seelen W (1997) Optical imaging of cat auditory cortex cochleotopic selectivity evoked by acute electrical stimulation of a multi-channel cochlear implant. Eur J Neurosci 9:113–119PubMedCrossRefGoogle Scholar
  16. Dragoi V, Sur M (2000) Dynamic properties of recurrent inhibition in primary visual cortex: contrast and orientation dependence of contextual effects. J Neurophysiol 83:1019–1030PubMedGoogle Scholar
  17. Ellsworth CA, Lyckman AW, Sur M (2001) Eye-specific patterning of retino-geniculate terminations in the medial geniculate nucleus of rewired mice. Soc Neurosci Abstr 27, No 14Google Scholar
  18. Eudy JD, Sumegi J (1999) Molecular genetics of Usher syndrome. Cell Mol Life Sci 56:258–267PubMedCrossRefGoogle Scholar
  19. Ferster D, Chung S, Wheat H (1996) Orientation selectivity of thalamic input to simple cells of cat visual cortex. Nature 380:249–252PubMedCrossRefGoogle Scholar
  20. Fitzsimonds RM, Poo M-M (1998) Retrograde signaling in the development and modification of synapses. Physiol Rev 78:143–170PubMedGoogle Scholar
  21. Frost DO (1981) Orderly anomalous retinal projections to the medial geniculate, ventrobasal, and lateral posterior nuclei of the hamster. J Comp Neurol 203:227–256PubMedCrossRefGoogle Scholar
  22. Frost DO, Boire D, Gingras G, Ptito M (2000) Surgically created neural pathways mediate visual pattern discrimination. Proc Natl Acad Sci USA 97:11068–11073PubMedCrossRefGoogle Scholar
  23. Frostig RD, Lieke EE, Ts’o DY, Grinvald A (1990) Cortical functional architecture and local coupling between neuronal activity and the microcirculation revealed by in vivo high-resolution optical imaging of intrinsic signals. Proc Natl Acad Sci USA 87:6082–6086PubMedCrossRefGoogle Scholar
  24. Gilbert CD, Wiesel TN (1989) Columnar specificity of intrinsic horizontal and corticocortical connections in cat visual cortex. J Neurosci 9:2432–2442PubMedGoogle Scholar
  25. Giraud A, Price CJ, Graham JM, Truy E, Frackowiak KS (2001) Cross-modal plasticity underpins language recovery after cochlear implantation. Neuron 30:657–663PubMedCrossRefGoogle Scholar
  26. Grinvald A, Lieke E, Frostig RD, Gilbert CD, Wiesel TN (1986) Functional architecture of cortex revealed by optical imaging of intrinsic signals. Nature 324:361–364PubMedCrossRefGoogle Scholar
  27. Hubel DH, Wiesel TN (1998) Early exploration of the visual cortex. Neuron 20:401–412PubMedCrossRefGoogle Scholar
  28. Hubener M, Shoham D, Grinvald A, Bonhoeffer T (1997) Spatial relationships among three columnar systems in cat area 17. T Neurosci 17:9270–9284Google Scholar
  29. Issa NP, Trepel C, Stryker MP (2000) Spatial frequency maps in cat visual cortex. J Neurosci 20: 8504–8514PubMedGoogle Scholar
  30. Keats BJ, Corey DP (1999) The Usher syndromes. Am J Med Genet 89:158–166PubMedCrossRefGoogle Scholar
  31. Kilgard MP, Merzenich MM (1999) Distributed representation of spectral and temporal information in rat primary auditory cortex. Hear Res 134:16–28PubMedCrossRefGoogle Scholar
  32. Kisvarday ZF, Eysel UT (1992) Cellular organization of reciprocal patchy networks in layer III of cat visual cortex (area 17). Neuroscience 46:275–286PubMedCrossRefGoogle Scholar
  33. Kohara K, Kitamura A, Morishima M, Tsumoto T (2001) Activity-dependent transfer of brain-derived neurotrophic factor to postsynaptic neurons. Science 291:2419–2423PubMedCrossRefGoogle Scholar
  34. Kozloski J, Hamzei-Sichani F, Yuste R (2001) Stereotyped position of local synaptic targets in neocortex. Science 293:868–872PubMedCrossRefGoogle Scholar
  35. Kuffler SW, Martin AR, Nicholls JG (1984) From neuron to brain: a cellular approach to the function of the nervous system. Sinauer Associates, Sunderland, MAGoogle Scholar
  36. Levanen S, Hamdorf D (2001) Feeling vibrations: enhanced tactile sensitivity in congenitally deaf humans. Neurosci Lett 301:75–77PubMedCrossRefGoogle Scholar
  37. LeVay S, Voigt T (1990) Retrograde transneuronal transport of wheat-germ agglutinin to the retina from visual cortex in the cat. Exp Brain Res 82:77–81PubMedCrossRefGoogle Scholar
  38. Luethke LE, Krubitzer LA, Kaas JH (1989) Connections of primary auditory cortex in the New World monkey, Saguinus. J Comp Neurol 285:487–513PubMedCrossRefGoogle Scholar
  39. Lyckman AW, Jhaveri S, Feldheim DA, Vanderhaeghen P, Flanagan JG, Sur M (2001) Enhanced plasticity of retinothalamic projections in an ephrin-A2/A5 double mutant. J Neurosci 21: 7684–7690PubMedGoogle Scholar
  40. Mallamaci A, Muzio L, Chan CH, Parnavelas J, Boncinelli E (2000) Area identity shifts in the early cerebral cortex of Emx2-/- mutant mice. Nat Neurosci 3:679–686PubMedCrossRefGoogle Scholar
  41. Matsubara JA, Phillips DP (1988) Intracortical connections and their physiological correlates in the primary auditory cortex (AI) of the cat. J Comp Neurol 268:38–48PubMedCrossRefGoogle Scholar
  42. Mendelson JR, Grasse KL (1992) A comparison of monaural and binaural responses to frequency modulated (FM) sweeps in cat primary auditory cortex. Exp Brain Res 91:435–454PubMedCrossRefGoogle Scholar
  43. Middlebrooks JC, Dykes RW, Merzenich MM (1980) Binaural response-specific bands in primary auditory cortex (AI) of the cat: topographical organization orthogonal to isofrequency contours. Brain Res 181:31–48PubMedCrossRefGoogle Scholar
  44. Mountcastle VB (1998) Perceptual neuroscience: the cerebral cortex. Harvard University Press, Cambridge, MAGoogle Scholar
  45. Nedivi E (1999) Molecular analysis of developmental plasticity in neocortex. J Neurobiol 41: 135–147PubMedCrossRefGoogle Scholar
  46. Ojima H, Honda CN, Jones EG (1991) Patterns of axon collateralization of identified supragranular pyramidal neurons in the cat auditory cortex. Cereb Cortex 1:80–94PubMedCrossRefGoogle Scholar
  47. Pallas SL, Sur M (1994) Morphology of retinal axon arbors induced to arborize in a novel target, the medial geniculate nucleus. II. Comparison with axons from the inferior colliculus. J Comp Neurol 349:363–376PubMedCrossRefGoogle Scholar
  48. Pallas SL, Hahm J, Sur M (1994) Morphology of retinal axons induced to arborize in a novel target, the medial geniculate nucleus. I. Comparison with arbors in normal targets. J Comp Neurol 349:343–362PubMedCrossRefGoogle Scholar
  49. Pinaudeau C, Gaillard A, Roger M (2000) Stage of specification of the spinal cord and tectal projections from cortical grafts. Eur J Neurosci 12:2486–2496PubMedCrossRefGoogle Scholar
  50. Pugh MC, Ringach DL, Shapley R, Shelley MJ (2000) Computational modeling of orientation tuning dynamics in monkey primary visual cortex. I Comput Neurosci 8:143–159CrossRefGoogle Scholar
  51. Rao SC, Toth LJ, Sur M (1997) Optically imaged maps of orientation preference in primary visual cortex of cats and ferrets. I Comp Neurol 387:358–370CrossRefGoogle Scholar
  52. Read HL, Winer JA, Schreiner CE (2001) Modular organization of intrinsic connections associated with spectral tuning in cat auditory cortex. Proc Natl Acad Sci USA 98:8042–8047PubMedCrossRefGoogle Scholar
  53. Reid RC, Alonso JM (1995) Specificity of monosynaptic connections from thalamus to visual cortex. Nature 378:281–284PubMedCrossRefGoogle Scholar
  54. Roe AW, Hahm J, Sur M (1991) Experimentally induced establishment of visual topography in auditory thalamus. Soc Neurosci Abstr 17:898Google Scholar
  55. Roe AW, Pallas SL, Kwon YH, Sur M (1992) Visual projections routed to the auditory pathway in ferrets: receptive fields of visual neurons in primary auditory cortex. J Neurosci 12:3651–3664PubMedGoogle Scholar
  56. Rubenstein JL, Anderson S, Shi L, Miyashita-Lin E, Bulfone A, Hevner R (1999) Genetic control of cortical regionalization and connectivity. Cereb Cortex 9:524–532PubMedCrossRefGoogle Scholar
  57. Ruthazer ES, Baker GE, Stryker MP (1999) Development and organization of ocular dominance bands in primary visual cortex of the sable ferret. J Comp Neurol 407:151–165PubMedCrossRefGoogle Scholar
  58. Schneider GE (1973) Early lesions of superior colliculus: factors affecting the formation of abnormal retinal projections. Brain Behav Evol 8:73–109PubMedCrossRefGoogle Scholar
  59. Schreiner CE, Read HL, Sutter ML (2000) Modular organization of frequency integration in primary auditory cortex. Annu Rev Neurosci 23:501–529PubMedCrossRefGoogle Scholar
  60. Sharma J, Angelucci A, Sur M (2000) Induction of visual orientation modules in auditory cortex. Nature 404:841–847PubMedCrossRefGoogle Scholar
  61. Shatz CJ, Stryker MP (1988) Prenatal tetrodotoxin infusion blocks segregation of retinogeniculate afferents. Science 242:87–89PubMedCrossRefGoogle Scholar
  62. Somers DC, Nelson SB, Sur M (1995) An emergent model of orientation selectivity in cat visual cortical simple cells. J Neurosci 15:5448–5465PubMedGoogle Scholar
  63. Sretavan DW, Shatz CJ, Stryker MP (1988) Modification of retinal ganglion cell axon morphology by prenatal infusion of tetrodotoxin. Nature 336:468–471PubMedCrossRefGoogle Scholar
  64. Sur M, Leamey CA (2001) Development and plasticity of cortical areas and networks. Nat Rev Neurosci 2:251–262PubMedCrossRefGoogle Scholar
  65. Sur M, Garraghty PE, Roe AW (1988) Experimentally induced visual projections into auditory thalamus and cortex. Science 242:1437–1441PubMedCrossRefGoogle Scholar
  66. Sur M, Angelucci A, Sharma J (1999) Rewiring cortex: the role of patterned activity in development and plasticity of neocortical circuits. J Neurobiol 41:33–43PubMedCrossRefGoogle Scholar
  67. Swindale NV, Shoham D, Grinvald A, Bonhoeffer T, Hubener M (2000) Visual cortex maps are optimized for uniform coverage. Nat Neurosci 3:822–826PubMedCrossRefGoogle Scholar
  68. Tao H, Zhang LI, Bi G, Poo M-M (2000) Selective presynaptic propagation of long-term potentiation in defined neural networks. J Neurosci 20:3233–3243PubMedGoogle Scholar
  69. Ts’o DY, Frostig RD, Lieke EE, Grinvald A (1990) Functional organization of primate visual cortex revealed by high resolution optical imaging. Science 249:417–420PubMedCrossRefGoogle Scholar
  70. von Melchner L, Pallas SL, Sur M (2000) Visual behaviour mediated by retinal projections directed to the auditory pathway. Nature 404:871–876CrossRefGoogle Scholar
  71. White LE, Bosking WH, Fitzpatrick D (2001) Consistent mapping of orientation preference across irregular functional domains in ferret visual cortex. Vis Neurosci 18:65–76PubMedCrossRefGoogle Scholar
  72. Willott JF (ed) (1983) The auditory psychobiology of the mouse. Thomas, Springfield, ILGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2002

Authors and Affiliations

  • Alvin W. Lyckman
    • 1
  • Mriganka Sur
    • 1
    • 2
  1. 1.The Center for Learning and MemoryCambridgeUSA
  2. 2.Department of Brain and Cognitive SciencesMassachusetts Institute of Technology, E25-235CambridgeUSA

Personalised recommendations