Brain Structure and Function

, Volume 223, Issue 3, pp 1165–1190 | Cite as

Early sensory experience influences the development of multisensory thalamocortical and intracortical connections of primary sensory cortices

  • Julia U. Henschke
  • Anja M. Oelschlegel
  • Frank Angenstein
  • Frank W. Ohl
  • Jürgen Goldschmidt
  • Patrick O. Kanold
  • Eike BudingerEmail author
Original Article


The nervous system integrates information from multiple senses. This multisensory integration already occurs in primary sensory cortices via direct thalamocortical and corticocortical connections across modalities. In humans, sensory loss from birth results in functional recruitment of the deprived cortical territory by the spared senses but the underlying circuit changes are not well known. Using tracer injections into primary auditory, somatosensory, and visual cortex within the first postnatal month of life in a rodent model (Mongolian gerbil) we show that multisensory thalamocortical connections emerge before corticocortical connections but mostly disappear during development. Early auditory, somatosensory, or visual deprivation increases multisensory connections via axonal reorganization processes mediated by non-lemniscal thalamic nuclei and the primary areas themselves. Functional single-photon emission computed tomography of regional cerebral blood flow reveals altered stimulus-induced activity and higher functional connectivity specifically between primary areas in deprived animals. Together, we show that intracortical multisensory connections are formed as a consequence of sensory-driven multisensory thalamocortical activity and that spared senses functionally recruit deprived cortical areas by an altered development of sensory thalamocortical and corticocortical connections. The functional–anatomical changes after early sensory deprivation have translational implications for the therapy of developmental hearing loss, blindness, and sensory paralysis and might also underlie developmental synesthesia.


Cross-modal Deprivation Development Sensory integration Rodent Synesthesia 



We like to thank K. Böttger, A. Gürke, D. Montag, J. Stallmann, and D. Vincenz-Zörner for excellent technical assistance. We also thank the three anonymous reviewers for their most helpful comments on the manuscript. This work was supported by the DFG ( SFB TRR31 (J.U.H., F.W.O., E.B.) and NIH ( RO1 DC009607 (P.O.K.).

Compliance with ethical standards

Informed consent

Informed consent was obtained from all individual participants included in the study.

Conflict of interest

All authors declare that they have no financial, personal, or professional conflict of interest.

Ethical standards

Authors declare that all animal studies have been approved by the appropriate ethics committee (see “Materials and methods”) and have, therefore, been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments.

Supplementary material

429_2017_1549_MOESM1_ESM.pdf (2.2 mb)
Supplementary material 1 (PDF 2237 kb)


  1. Afra P, Funke M, Matsuo F (2009) Acquired auditory-visual synesthesia: a window to early cross-modal sensory interactions. Psychol Res Behav Manag 2:31–37PubMedCentralCrossRefPubMedGoogle Scholar
  2. Allman BL, Keniston LP, Meredith MA (2009) Adult deafness induces somatosensory conversion of ferret auditory cortex. Proc Natl Acad Sci USA 106(14):5925–5930PubMedCentralCrossRefPubMedGoogle Scholar
  3. Ashwell KWS, Paxinos G (2008) Atlas of the rat developing nervous system. Academic Press, San DiegoGoogle Scholar
  4. Banks MI, Uhlrich DJ, Smith PH, Krause BM, Manning KA (2011) Descending projections from extrastriate visual cortex modulate responses of cells in primary auditory cortex. Cereb Cortex 21(11):2620–2638PubMedCentralCrossRefPubMedGoogle Scholar
  5. Barnes SJ, Finnerty GT (2010) Sensory experience and cortical rewiring. Neuroscientist 16(2):186–198CrossRefPubMedGoogle Scholar
  6. Barone P, Lacassagne L, Kral A (2013) Reorganization of the connectivity of cortical field DZ in congenitally deaf cat. PLoS One 8(4):e60093PubMedCentralCrossRefPubMedGoogle Scholar
  7. Batardiere A, Barone P, Knoblauch K, Giroud P, Berland M, Dumas AM, Kennedy H (2002) Early specification of the hierarchical organization of visual cortical areas in the macaque monkey. Cereb Cortex 12(5):453–465CrossRefPubMedGoogle Scholar
  8. Bavelier D, Neville HJ (2002) Cross-modal plasticity: where and how? Nat Rev Neurosci 3(6):443–452CrossRefPubMedGoogle Scholar
  9. Benowitz LI, Routtenberg A (1997) GAP-43: an intrinsic determinant of neuronal development and plasticity. Trends Neurosci 20(2):84–91CrossRefPubMedGoogle Scholar
  10. Berardi N, Pizzorusso T, Ratto GM, Maffei L (2003) Molecular basis of plasticity in the visual cortex. Trends Neurosci 26(7):369–378CrossRefPubMedGoogle Scholar
  11. Berezovskii VK, Nassi JJ, Born RT (2011) Segregation of feedforward and feedback projections in mouse visual cortex. J Comp Neurol 519(18):3672–3683PubMedCentralCrossRefPubMedGoogle Scholar
  12. Bhattacharya S, Herrera-Molina R, Sabanov V, Ahmed T, Iscru E, Stober F, Richter K, Fischer KD, Angenstein F, Goldschmidt J, Beesley PW, Balschun D, Smalla KH, Gundelfinger ED, Montag D (2017) Genetically induced retrograde amnesia of associative memories after neuroplastin ablation. Biol Psychiatry 81(2):124–135CrossRefPubMedGoogle Scholar
  13. Bieler M, Sieben K, Schildt S, Roder B, Hanganu-Opatz IL (2017) Visual–tactile processing in primary somatosensory cortex emerges before cross-modal experience. Synapse 71(6). doi: 10.1002/syn.21958
  14. Bizley JK, Jones GP, Town SM (2016) Where are multisensory signals combined for perceptual decision-making? Curr Opin Neurobiol 40:31–37CrossRefPubMedGoogle Scholar
  15. Blankenship AG, Feller MB (2010) Mechanisms underlying spontaneous patterned activity in developing neural circuits. Nat Rev Neurosci 11(1):18–29CrossRefPubMedGoogle Scholar
  16. Bolles RC, Woods PJ (1964) The ontogeny of behaviour in the albino rat. Anim Behav 12(4):427–441CrossRefGoogle Scholar
  17. Budinger E, Scheich H (2009) Anatomical connections suitable for the direct processing of neuronal information of different modalities via the rodent primary auditory cortex. Hear Res 258(1–2):16–27CrossRefPubMedGoogle Scholar
  18. Budinger E, Heil P, Hess A, Scheich H (2006) Multisensory processing via early cortical stages: connections of the primary auditory cortical field with other sensory systems. Neuroscience 143(4):1065–1083CrossRefPubMedGoogle Scholar
  19. Burkhalter A (1993) Development of forward and feedback connections between areas V1 and V2 of human visual cortex. Cereb Cortex 3(5):476–487CrossRefPubMedGoogle Scholar
  20. Cabana T, Cassidy G, Pflieger JF, Baron G (1993) The ontogenic development of sensorimotor reflexes and spontaneous locomotion in the Mongolian gerbil (Meriones unguiculatus). Brain Res Bull 30(3–4):291–301CrossRefPubMedGoogle Scholar
  21. Cahill L, Ohl F, Scheich H (1996) Alteration of auditory cortex activity with a visual stimulus through conditioning: a 2-deoxyglucose analysis. Neurobiol Learn Mem 65:213–222CrossRefPubMedGoogle Scholar
  22. Campi KL, Bales KL, Grunewald R, Krubitzer L (2010) Connections of auditory and visual cortex in the prairie vole (Microtus ochrogaster): evidence for multisensory processing in primary sensory areas. Cereb Cortex 20(1):89–108CrossRefPubMedGoogle Scholar
  23. Cappe C, Barone P (2005) Heteromodal connections supporting multisensory integration at low levels of cortical processing in the monkey. Eur J Neurosci 22(11):2886–2902CrossRefPubMedGoogle Scholar
  24. Cappe C, Morel A, Barone P, Rouiller EM (2009) The thalamocortical projection systems in primate: an anatomical support for multisensory and sensorimotor interplay. Cereb Cortex 19(9):2025–2037PubMedCentralCrossRefPubMedGoogle Scholar
  25. Chabot N, Robert S, Tremblay R, Miceli D, Boire D, Bronchti G (2007) Audition differently activates the visual system in neonatally enucleated mice compared with anophthalmic mutants. Eur J Neurosci 26(8):2334–2348CrossRefPubMedGoogle Scholar
  26. Chabot N, Butler BE, Lomber SG (2015) Differential modification of cortical and thalamic projections to cat primary auditory cortex following early- and late-onset deafness. J Comp Neurol 523(15):2297–2320CrossRefPubMedGoogle Scholar
  27. Charbonneau V, Laramee ME, Boucher V, Bronchti G, Boire D (2012) Cortical and subcortical projections to primary visual cortex in anophthalmic, enucleated and sighted mice. Eur J Neurosci 36(7):2949–2963CrossRefPubMedGoogle Scholar
  28. Clemo HR, Lomber SG, Meredith MA (2016) Synaptic basis for cross-modal plasticity: enhanced supragranular dendritic spine density in anterior ectosylvian auditory cortex of the early deaf cat. Cereb Cortex 26(4):1365–1376CrossRefPubMedGoogle Scholar
  29. Clowry G, Molnar Z, Rakic P (2010) Renewed focus on the developing human neocortex. J Anat 217(4):276–288PubMedCentralCrossRefPubMedGoogle Scholar
  30. Driver J, Noesselt T (2008) Multisensory interplay reveals crossmodal influences on ‘sensory-specific’ brain regions, neural responses, and judgments. Neuron 57(1):11–23PubMedCentralCrossRefPubMedGoogle Scholar
  31. Ehret G (1976) Development of absolute auditory thresholds in the house mouse (Mus musculus). J Am Audiol Soc 1(5):179–184PubMedGoogle Scholar
  32. Elwood RW, Broom DM (1978) The influence of litter size and parental behaviour on the development of Mongolian gerbil pups. Anim Behav 26(Part 2(0)):438–454CrossRefGoogle Scholar
  33. Espinosa JS, Stryker MP (2012) Development and plasticity of the primary visual cortex. Neuron 75(2):230–249PubMedCentralCrossRefPubMedGoogle Scholar
  34. Feldman DE, Brecht M (2005) Map plasticity in somatosensory cortex. Science 310(5749):810–815CrossRefPubMedGoogle Scholar
  35. Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1(1):1–47CrossRefPubMedGoogle Scholar
  36. Finck A, Schneck CD, Hartman AF (1972) Development of cochlear function in the neonate Mongolian gerbil (Meriones unguiculatus). J Comp Physiol Psychol 78(3):375–380CrossRefPubMedGoogle Scholar
  37. Finney EM, Fine I, Dobkins KR (2001) Visual stimuli activate auditory cortex in the deaf. Nat Neurosci 4(12):1171–1173CrossRefPubMedGoogle Scholar
  38. Frasnelli J, Collignon O, Voss P, Lepore F (2011) Crossmodal plasticity in sensory loss. Prog Brain Res 191:233–249CrossRefPubMedGoogle Scholar
  39. Fuller JL, Wimer RE (1966) Neural, sensory, and motor functions. Biology of the laboratory mouse. McGraw-Hill, New York, pp 609–628Google Scholar
  40. Ghoshal A, Tomarken A, Ebner F (2011) Cross-sensory modulation of primary sensory cortex is developmentally regulated by early sensory experience. J Neurosci 31(7):2526–2536CrossRefPubMedGoogle Scholar
  41. Gielen SC, Schmidt RA, Van den Heuvel PJ (1983) On the nature of intersensory facilitation of reaction time. Percept Psychophys 34(2):161–168CrossRefPubMedGoogle Scholar
  42. Gleeson JG, Allen KM, Fox JW, Lamperti ED, Berkovic S, Scheffer I, Cooper EC, Dobyns WB, Minnerath SR, Ross ME, Walsh CA (1998) Doublecortin, a brain-specific gene mutated in human X-linked lissencephaly and double cortex syndrome, encodes a putative signaling protein. Cell 92(1):63–72CrossRefPubMedGoogle Scholar
  43. Gleiss S, Kayser C (2012) Audio-visual detection benefits in the rat. PLoS One 7(9):e45677PubMedCentralCrossRefPubMedGoogle Scholar
  44. Gougoux F, Lepore F, Lassonde M, Voss P, Zatorre RJ, Belin P (2004) Neuropsychology: pitch discrimination in the early blind. Nature 430(6997):309CrossRefPubMedGoogle Scholar
  45. Groenewegen HJ, Witter MP (2004) Thalamus. In: Paxinos G (ed) The rat nervous system. Elsevier Academic Press, San Diego, pp 407–453CrossRefGoogle Scholar
  46. Grossenbacher PG, Lovelace CT (2001) Mechanisms of synesthesia: cognitive and physiological constraints. Trends Cogn Sci 5(1):36–41CrossRefPubMedGoogle Scholar
  47. Guerreiro MJ, Putzar L, Roder B (2016) The effect of early visual deprivation on the neural bases of auditory processing. J Neurosci 36(5):1620–1630CrossRefPubMedGoogle Scholar
  48. Hammond-Kenny A, Bajo VM, King AJ, Nodal FR (2017) Behavioural benefits of multisensory processing in ferrets. Eur J Neurosci 45(2):278–289CrossRefPubMedGoogle Scholar
  49. Hanganu-Opatz IL, Rowland BA, Bieler M, Sieben K (2015) Unraveling cross-modal development in animals: neural substrate, functional coding and behavioral readout. Multisens Res 28(1–2):33–69CrossRefPubMedGoogle Scholar
  50. Hensch TK (2004) Critical period regulation. Annu Rev Neurosci 27:549–579CrossRefPubMedGoogle Scholar
  51. Hensch TK (2005) Critical period plasticity in local cortical circuits. Nat Rev Neurosci 6(11):877–888CrossRefPubMedGoogle Scholar
  52. Henschke JU, Noesselt T, Scheich H, Budinger E (2015) Possible anatomical pathways for short-latency multisensory integration processes in primary sensory cortices. Brain Struct Funct 220(2):955–977CrossRefPubMedGoogle Scholar
  53. Heydt JL, Cunningham LL, Rubel EW, Coltrera MD (2004) Round window gentamicin application: an inner ear hair cell damage protocol for the mouse. Hear Res 192(1–2):65–74CrossRefPubMedGoogle Scholar
  54. Horwitz B, Tagamets MA, McIntosh AR (1999) Neural modeling, functional brain imaging, and cognition. Trends Cogn Sci 3(3):91–98CrossRefPubMedGoogle Scholar
  55. Hubbard EM, Brang D, Ramachandran VS (2011) The cross-activation theory at 10. J Neuropsychol 5(2):152–177CrossRefPubMedGoogle Scholar
  56. Hubener M, Bonhoeffer T (2014) Neuronal plasticity: beyond the critical period. Cell 159(4):727–737CrossRefPubMedGoogle Scholar
  57. Ibrahim LA, Mesik L, Ji XY, Fang Q, Li HF, Li YT, Zingg B, Zhang LI, Tao HW (2016) Cross-modality sharpening of visual cortical processing through layer-1-mediated inhibition and disinhibition. Neuron 89(5):1031–1045PubMedCentralCrossRefPubMedGoogle Scholar
  58. Innocenti GM, Price DJ (2005) Exuberance in the development of cortical networks. Nat Rev Neurosci 6(12):955–965CrossRefPubMedGoogle Scholar
  59. Iurilli G, Ghezzi D, Olcese U, Lassi G, Nazzaro C, Tonini R, Tucci V, Benfenati F, Medini P (2012) Sound-driven synaptic inhibition in primary visual cortex. Neuron 73(4):814–828PubMedCentralCrossRefPubMedGoogle Scholar
  60. Izraeli R, Koay G, Lamish M, Heicklen-Klein AJ, Heffner HE, Heffner RS, Wollberg Z (2002) Cross-modal neuroplasticity in neonatally enucleated hamsters: structure, electrophysiology and behaviour. Eur J Neurosci 15(4):693–712CrossRefPubMedGoogle Scholar
  61. Jacobs GH, Deegan JF 2nd (1994) Sensitivity to ultraviolet light in the gerbil (Meriones unguiculatus): characteristics and mechanisms. Vis Res 34(11):1433–1441CrossRefPubMedGoogle Scholar
  62. Jones E (2007) Principles of thalamic organization. In: Jones E (ed) The thalamus. Cambridge University Press, Cambridge, pp 87–170Google Scholar
  63. Kaas JH, Collins CE (2003) Anatomic and functional reorganization of somatosensory cortex in mature primates after peripheral nerve and spinal cord injury. Adv Neurol 93:87–95PubMedGoogle Scholar
  64. Kanold PO, Luhmann HJ (2010) The subplate and early cortical circuits. Annu Rev Neurosci 33:23–48CrossRefPubMedGoogle Scholar
  65. Karlen SJ, Kahn DM, Krubitzer L (2006) Early blindness results in abnormal corticocortical and thalamocortical connections. Neuroscience 142(3):843–858CrossRefPubMedGoogle Scholar
  66. Katz LC, Shatz CJ (1996) Synaptic activity and the construction of cortical circuits. Science 274(5290):1133–1138CrossRefPubMedGoogle Scholar
  67. Kayser C, Logothetis NK (2007) Do early sensory cortices integrate cross-modal information? Brain Struct Funct 212(2):121–132CrossRefPubMedGoogle Scholar
  68. Kilb W, Kirischuk S, Luhmann HJ (2011) Electrical activity patterns and the functional maturation of the neocortex. Eur J Neurosci 34(10):1677–1686CrossRefPubMedGoogle Scholar
  69. Klemen J, Chambers CD (2012) Current perspectives and methods in studying neural mechanisms of multisensory interactions. Neurosci Biobehav Rev 36(1):111–133CrossRefPubMedGoogle Scholar
  70. Klinge C, Eippert F, Roder B, Buchel C (2010) Corticocortical connections mediate primary visual cortex responses to auditory stimulation in the blind. J Neurosci 30(38):12798–12805CrossRefPubMedGoogle Scholar
  71. Ko H, Cossell L, Baragli C, Antolik J, Clopath C, Hofer SB, Mrsic-Flogel TD (2013) The emergence of functional microcircuits in visual cortex. Nature 496(7443):96–100PubMedCentralCrossRefPubMedGoogle Scholar
  72. Kobayasi KI, Suwa Y, Riquimaroux H (2013) Audiovisual integration in the primary auditory cortex of an awake rodent. Neurosci Lett 534:24–29CrossRefPubMedGoogle Scholar
  73. Kolarik AJ, Cirstea S, Pardhan S, Moore BC (2014) A summary of research investigating echolocation abilities of blind and sighted humans. Hear Res 310:60–68CrossRefPubMedGoogle Scholar
  74. Kolodziej A, Lippert M, Angenstein F, Neubert J, Pethe A, Grosser OS, Amthauer H, Schroeder UH, Reymann KG, Scheich H, Ohl FW, Goldschmidt J (2014) SPECT-imaging of activity-dependent changes in regional cerebral blood flow induced by electrical and optogenetic self-stimulation in mice. Neuroimage 103:171–180CrossRefPubMedGoogle Scholar
  75. Kotak VC, Pendola LM, Rodriguez-Contreras A (2012) Spontaneous activity in the developing gerbil auditory cortex in vivo involves GABAergic transmission. Neuroscience 226:130–144PubMedCentralCrossRefPubMedGoogle Scholar
  76. Kral A, Sharma A (2012) Developmental neuroplasticity after cochlear implantation. Trends Neurosci 35(2):111–122CrossRefPubMedGoogle Scholar
  77. Kupers R, Ptito M (2014) Compensatory plasticity and cross-modal reorganization following early visual deprivation. Neurosci Biobehav Rev 41:36–52CrossRefPubMedGoogle Scholar
  78. Laramee ME, Boire D (2014) Visual cortical areas of the mouse: comparison of parcellation and network structure with primates. Front Neural Circuits 8:149PubMedGoogle Scholar
  79. Lee HK, Whitt JL (2015) Cross-modal synaptic plasticity in adult primary sensory cortices. Curr Opin Neurobiol 35:119–126PubMedCentralCrossRefPubMedGoogle Scholar
  80. Lessard N, Pare M, Lepore F, Lassonde M (1998) Early-blind human subjects localize sound sources better than sighted subjects. Nature 395(6699):278–280CrossRefPubMedGoogle Scholar
  81. Lomber SG, Meredith MA, Kral A (2010) Cross-modal plasticity in specific auditory cortices underlies visual compensations in the deaf. Nat Neurosci 13(11):1421–1427CrossRefPubMedGoogle Scholar
  82. Lopez-Bendito G, Molnar Z (2003) Thalamocortical development: how are we going to get there? Nat Rev Neurosci 4(4):276–289CrossRefPubMedGoogle Scholar
  83. Loskota WJ, Lomax P, Verity MA (1974) A stereotaxic atlas of the Mongolian gerbil (Meriones unguiculatus). Ann Arbor Science, MichiganGoogle Scholar
  84. Maidenbaum S, Abboud S, Amedi A (2014) Sensory substitution: closing the gap between basic research and widespread practical visual rehabilitation. Neurosci Biobehav Rev 41:3–15CrossRefPubMedGoogle Scholar
  85. Markov NT, Kennedy H (2013) The importance of being hierarchical. Curr Opin Neurobiol 23(2):187–194CrossRefPubMedGoogle Scholar
  86. Masse IO, Ross S, Bronchti G, Boire D (2017) Asymmetric direct reciprocal connections between primary visual and somatosensory cortices of the mouse. Cereb Cortex 27(9):4361–4378PubMedGoogle Scholar
  87. McGovern DP, Astle AT, Clavin SL, Newell FN (2016) Task-specific transfer of perceptual learning across sensory modalities. Curr Biol 26(1):R20–R21CrossRefPubMedGoogle Scholar
  88. Meng X, Kao JP, Lee HK, Kanold PO (2015) Visual deprivation causes refinement of intracortical circuits in the auditory cortex. Cell Rep 12(6):955–964PubMedCentralCrossRefPubMedGoogle Scholar
  89. Merabet LB, Pascual-Leone A (2010) Neural reorganization following sensory loss: the opportunity of change. Nat Rev Neurosci 11(1):44–52CrossRefPubMedGoogle Scholar
  90. Meredith MA, Allman BL (2012) Early hearing-impairment results in crossmodal reorganization of ferret core auditory cortex. Neural Plast 2012:601591PubMedCentralCrossRefPubMedGoogle Scholar
  91. Meredith MA, Lomber SG (2011) Somatosensory and visual crossmodal plasticity in the anterior auditory field of early-deaf cats. Hear Res 280(1–2):38–47PubMedCentralCrossRefPubMedGoogle Scholar
  92. Meredith MA, Lomber SG (2017) Species-dependent role of crossmodal connectivity among the primary sensory cortices. Hear Res 343:83–91CrossRefPubMedGoogle Scholar
  93. Mezzera C, Lopez-Bendito G (2016) Cross-modal plasticity in sensory deprived animal models: from the thalamocortical development point of view. J Chem Neuroanat 75(Pt A):32–40CrossRefPubMedGoogle Scholar
  94. Molholm S, Ritter W, Murray MM, Javitt DC, Schroeder CE, Foxe JJ (2002) Multisensory auditory-visual interactions during early sensory processing in humans: a high-density electrical mapping study. Brain Res Cogn Brain Res 14(1):115–128CrossRefPubMedGoogle Scholar
  95. Mowery TM, Kotak VC, Sanes DH (2016) The onset of visual experience gates auditory cortex critical periods. Nat Commun 7:10416PubMedCentralCrossRefPubMedGoogle Scholar
  96. Murray MM, Lewkowicz DJ, Amedi A, Wallace MT (2016) Multisensory processes: a balancing act across the lifespan. Trends Neurosci 39(8):567–579PubMedCentralCrossRefPubMedGoogle Scholar
  97. Navarro X, Vivo M, Valero-Cabre A (2007) Neural plasticity after peripheral nerve injury and regeneration. Prog Neurobiol 82(4):163–201CrossRefPubMedGoogle Scholar
  98. Noesselt T, Tyll S, Boehler CN, Budinger E, Heinze HJ, Driver J (2010) Sound-induced enhancement of low-intensity vision: multisensory influences on human sensory-specific cortices and thalamic bodies relate to perceptual enhancement of visual detection sensitivity. J Neurosci 30(41):13609–13623PubMedCentralCrossRefPubMedGoogle Scholar
  99. Nys J, Scheyltjens I, Arckens L (2015) Visual system plasticity in mammals: the story of monocular enucleation-induced vision loss. Front Syst Neurosci 9:60PubMedCentralCrossRefPubMedGoogle Scholar
  100. Pallas SL (2001) Intrinsic and extrinsic factors that shape neocortical specification. Trends Neurosci 24(7):417–423CrossRefPubMedGoogle Scholar
  101. Paperna T, Malach R (1991) Patterns of sensory intermodality relationships in the cerebral cortex of the rat. J Comp Neurol 308(3):432–456CrossRefPubMedGoogle Scholar
  102. Paxinos G, Halliday G, Watson C, Koutcherov Y, Wang H (2006) Atlas of the developing mouse brain at E17.5, P0, and P6. Academic Press, San DiegoGoogle Scholar
  103. Petrus E, Isaiah A, Jones AP, Li D, Wang H, Lee HK, Kanold PO (2014) Crossmodal induction of thalamocortical potentiation leads to enhanced information processing in the auditory cortex. Neuron 81(3):664–673PubMedCentralCrossRefPubMedGoogle Scholar
  104. Petrus E, Rodriguez G, Patterson R, Connor B, Kanold PO, Lee HK (2015) Vision loss shifts the balance of feedforward and intracortical circuits in opposite directions in mouse primary auditory and visual cortices. J Neurosci 35(23):8790–8801PubMedCentralCrossRefPubMedGoogle Scholar
  105. Piche M, Chabot N, Bronchti G, Miceli D, Lepore F, Guillemot JP (2007) Auditory responses in the visual cortex of neonatally enucleated rats. Neuroscience 145(3):1144–1156CrossRefPubMedGoogle Scholar
  106. Pouchelon G, Gambino F, Bellone C, Telley L, Vitali I, Luscher C, Holtmaat A, Jabaudon D (2014) Modality-specific thalamocortical inputs instruct the identity of postsynaptic L4 neurons. Nature 511(7510):471–474CrossRefPubMedGoogle Scholar
  107. Price DJ, Kennedy H, Dehay C, Zhou L, Mercier M, Jossin Y, Goffinet AM, Tissir F, Blakey D, Molnar Z (2006) The development of cortical connections. Eur J Neurosci 23(4):910–920CrossRefPubMedGoogle Scholar
  108. Proulx MJ, Brown DJ, Pasqualotto A, Meijer P (2014) Multisensory perceptual learning and sensory substitution. Neurosci Biobehav Rev 41:16–25CrossRefPubMedGoogle Scholar
  109. Radtke-Schuller S, Schuller G, Angenstein F, Grosser OS, Goldschmidt J, Budinger E (2016) Brain atlas of the Mongolian gerbil (Meriones unguiculatus) in CT/MRI-aided stereotaxic coordinates. Brain Struct Funct 221(Suppl 1):1–272PubMedCentralCrossRefPubMedGoogle Scholar
  110. Rauschecker JP (1995) Compensatory plasticity and sensory substitution in the cerebral cortex. Trends Neurosci 18(1):36–43CrossRefPubMedGoogle Scholar
  111. Rauschecker JP, Tian B, Korte M, Egert U (1992) Crossmodal changes in the somatosensory vibrissa/barrel system of visually deprived animals. Proc Natl Acad Sci USA 89(11):5063–5067PubMedCentralCrossRefPubMedGoogle Scholar
  112. Renier L, De Volder AG, Rauschecker JP (2014) Cortical plasticity and preserved function in early blindness. Neurosci Biobehav Rev 41:53–63CrossRefPubMedGoogle Scholar
  113. Roder B, Teder-Salejarvi W, Sterr A, Rosler F, Hillyard SA, Neville HJ (1999) Improved auditory spatial tuning in blind humans. Nature 400(6740):162–166CrossRefPubMedGoogle Scholar
  114. Roth KA, Kuan C, Haydar TF, D’Sa-Eipper C, Shindler KS, Zheng TS, Kuida K, Flavell RA, Rakic P (2000) Epistatic and independent functions of caspase-3 and Bcl-X(L) in developmental programmed cell death. Proc Natl Acad Sci USA 97(1):466–471PubMedCentralCrossRefPubMedGoogle Scholar
  115. Rouiller EM, Simm GM, Villa AEP, Ribaupierre Yd, Ribaupierre Fd (1991) Auditory corticocortical interconnections in the cat: evidence for parallel and hierarchical arrangement of the auditory cortical areas. Exp Brain Res 86:483–503CrossRefPubMedGoogle Scholar
  116. Ryan A (1976) Hearing sensitivity of the mongolian gerbil, Meriones unguiculatis. J Acoust Soc Am 59(5):1222–1226CrossRefPubMedGoogle Scholar
  117. Ryugo DK, Ryugo R, Globus A, Killackey HP (1975) Increased spine density in auditory cortex following visual or somatic deafferentation. Brain Res 90(1):143–146CrossRefPubMedGoogle Scholar
  118. Sachs L (2004) Angewandte Statistik (Applied statistics). Springer, HeidelbergCrossRefGoogle Scholar
  119. Sadato N, Pascual-Leone A, Grafman J, Ibanez V, Deiber MP, Dold G, Hallett M (1996) Activation of the primary visual cortex by Braille reading in blind subjects. Nature 380(6574):526–528CrossRefPubMedGoogle Scholar
  120. Sakata S, Yamamori T, Sakurai Y (2004) Behavioral studies of auditory-visual spatial recognition and integration in rats. Exp Brain Res 159(4):409–417CrossRefPubMedGoogle Scholar
  121. Sanchez-Vives MV, Nowak LG, Descalzo VF, Garcia-Velasco JV, Gallego R, Berbel P (2006) Crossmodal audio–visual interactions in the primary visual cortex of the visually deprived cat: a physiological and anatomical study. Prog Brain Res 155:287–311CrossRefPubMedGoogle Scholar
  122. Schroeder CE, Foxe J (2005) Multisensory contributions to low-level, ‘unisensory’ processing. Curr Opin Neurobiol 15(4):454–458CrossRefPubMedGoogle Scholar
  123. Schwentker V (1963) The gerbil. A new laboratory animal. Ill Vet 6:5–9Google Scholar
  124. Sieben K, Bieler M, Roder B, Hanganu-Opatz IL (2015) Neonatal restriction of tactile inputs leads to long-lasting impairments of cross-modal processing. PLoS Biol 13(11):e1002304PubMedCentralCrossRefPubMedGoogle Scholar
  125. Smilek D, Dixon MJ, Cudahy C, Merikle PM (2001) Synaesthetic photisms influence visual perception. J Cogn Neurosci 13(7):930–936CrossRefPubMedGoogle Scholar
  126. Souter M, Nevill G, Forge A (1997) Postnatal maturation of the organ of Corti in gerbils: morphology and physiological responses. J Comp Neurol 386(4):635–651CrossRefPubMedGoogle Scholar
  127. Spector F, Maurer D (2009) Synesthesia: a new approach to understanding the development of perception. Dev Psychol 45(1):175–189CrossRefPubMedGoogle Scholar
  128. Stehberg J, Dang PT, Frostig RD (2014) Unimodal primary sensory cortices are directly connected by long-range horizontal projections in the rat sensory cortex. Front Neuroanat 8:93PubMedCentralCrossRefPubMedGoogle Scholar
  129. Stein BE, Stanford TR (2008) Multisensory integration: current issues from the perspective of the single neuron. Nat Rev Neurosci 9(4):255–266CrossRefPubMedGoogle Scholar
  130. Stein BE, Burr D, Constantinidis C, Laurienti PJ, Alex Meredith M, Perrault TJ Jr, Ramachandran R, Roder B, Rowland BA, Sathian K, Schroeder CE, Shams L, Stanford TR, Wallace MT, Yu L, Lewkowicz DJ (2010) Semantic confusion regarding the development of multisensory integration: a practical solution. Eur J Neurosci 31(10):1713–1720PubMedCentralCrossRefPubMedGoogle Scholar
  131. Stein BE, Stanford TR, Rowland BA (2014) Development of multisensory integration from the perspective of the individual neuron. Nat Rev Neurosci 15(8):520–535PubMedCentralCrossRefPubMedGoogle Scholar
  132. Stiles NR, Shimojo S (2015) Auditory sensory substitution is intuitive and automatic with texture stimuli. Sci Rep 5:15628PubMedCentralCrossRefPubMedGoogle Scholar
  133. Sur M, Rubenstein JL (2005) Patterning and plasticity of the cerebral cortex. Science 310(5749):805–810CrossRefPubMedGoogle Scholar
  134. Teder-Salejarvi WA, McDonald JJ, Di Russo F, Hillyard SA (2002) An analysis of audio-visual crossmodal integration by means of event-related potential (ERP) recordings. Brain Res Cogn Brain Res 14(1):106–114CrossRefPubMedGoogle Scholar
  135. Teichert M, Bolz J (2017) Simultaneous intrinsic signal imaging of auditory and visual cortex reveals profound effects of acute hearing loss on visual processing. Neuroimage 159:459–472CrossRefPubMedGoogle Scholar
  136. Thiessen DD, Yahr P (1977) The gerbil in behavioral investigations. Mechanisms of territoriality and olfactory communication. University of Texas Press, AustinGoogle Scholar
  137. Tropea D, Van Wart A, Sur M (2009) Molecular mechanisms of experience-dependent plasticity in visual cortex. Philos Trans R Soc Lond B Biol Sci 364(1515):341–355CrossRefPubMedGoogle Scholar
  138. Vallejo LA, Garrosa M, Al-Majdalawi A, Mayo A, Gayoso MJ (2000) Effects of unilateral deprivation in postnatal development of the olfactory bulb in an altricial rodent, the gerbil (Meriones unguiculatus). Brain Res Dev Brain Res 122(1):35–46CrossRefPubMedGoogle Scholar
  139. Vercelli A, Repici M, Garbossa D, Grimaldi A (2000) Recent techniques for tracing pathways in the central nervous system of developing and adult mammals. Brain Res Bull 51(1):11–28CrossRefPubMedGoogle Scholar
  140. Wall JT, Cusick CG (1986) The representation of peripheral nerve inputs in the S–I hindpaw cortex of rats raised with incompletely innervated hindpaws. J Neurosci 6(4):1129–1147PubMedGoogle Scholar
  141. Ward J (2013) Synesthesia. Annu Rev Psychol 64:49–75CrossRefPubMedGoogle Scholar
  142. Wickersham IR, Finke S, Conzelmann KK, Callaway EM (2007) Retrograde neuronal tracing with a deletion-mutant rabies virus. Nat Methods 4(1):47–49CrossRefPubMedGoogle Scholar
  143. Wilkinson F (1986) Eye and brain growth in the Mongolian gerbil (Meriones unguiculatus). Behav Brain Res 19(1):59–69CrossRefPubMedGoogle Scholar
  144. Yu X, Chung S, Chen DY, Wang S, Dodd SJ, Walters JR, Isaac JT, Koretsky AP (2012) Thalamocortical inputs show post-critical-period plasticity. Neuron 74(4):731–742PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Department Systems Physiology of LearningLeibniz Institute for NeurobiologyMagdeburgGermany
  2. 2.German Center for Neurodegenerative Diseases Within the Helmholtz AssociationMagdeburgGermany
  3. 3.Institute of Cognitive Neurology and Dementia Research (IKND)Otto-von-Guericke-University MagdeburgMagdeburgGermany
  4. 4.Research Group NeuropharmacologyLeibniz Institute for NeurobiologyMagdeburgGermany
  5. 5.Institute of AnatomyOtto-von-Guericke-University MagdeburgMagdeburgGermany
  6. 6.Functional Neuroimaging GroupGerman Center for Neurodegenerative Diseases Within the Helmholtz AssociationMagdeburgGermany
  7. 7.Institute of BiologyOtto-von-Guericke-University MagdeburgMagdeburgGermany
  8. 8.Department of BiologyUniversity of MarylandCollege ParkUSA
  9. 9.Center for Behavioral Brain SciencesMagdeburgGermany

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