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

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Abstract

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.

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References

  • Afra P, Funke M, Matsuo F (2009) Acquired auditory-visual synesthesia: a window to early cross-modal sensory interactions. Psychol Res Behav Manag 2:31–37

    Article  PubMed Central  PubMed  Google Scholar 

  • Allman BL, Keniston LP, Meredith MA (2009) Adult deafness induces somatosensory conversion of ferret auditory cortex. Proc Natl Acad Sci USA 106(14):5925–5930

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ashwell KWS, Paxinos G (2008) Atlas of the rat developing nervous system. Academic Press, San Diego

    Google Scholar 

  • 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):2620–2638

    Article  PubMed Central  PubMed  Google Scholar 

  • Barnes SJ, Finnerty GT (2010) Sensory experience and cortical rewiring. Neuroscientist 16(2):186–198

    Article  PubMed  Google Scholar 

  • Barone P, Lacassagne L, Kral A (2013) Reorganization of the connectivity of cortical field DZ in congenitally deaf cat. PLoS One 8(4):e60093

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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):453–465

    Article  PubMed  Google Scholar 

  • Bavelier D, Neville HJ (2002) Cross-modal plasticity: where and how? Nat Rev Neurosci 3(6):443–452

    Article  CAS  PubMed  Google Scholar 

  • Benowitz LI, Routtenberg A (1997) GAP-43: an intrinsic determinant of neuronal development and plasticity. Trends Neurosci 20(2):84–91

    Article  CAS  PubMed  Google Scholar 

  • Berardi N, Pizzorusso T, Ratto GM, Maffei L (2003) Molecular basis of plasticity in the visual cortex. Trends Neurosci 26(7):369–378

    Article  CAS  PubMed  Google Scholar 

  • Berezovskii VK, Nassi JJ, Born RT (2011) Segregation of feedforward and feedback projections in mouse visual cortex. J Comp Neurol 519(18):3672–3683

    Article  PubMed Central  PubMed  Google Scholar 

  • 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):124–135

    Article  CAS  PubMed  Google Scholar 

  • 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

  • Bizley JK, Jones GP, Town SM (2016) Where are multisensory signals combined for perceptual decision-making? Curr Opin Neurobiol 40:31–37

    Article  CAS  PubMed  Google Scholar 

  • Blankenship AG, Feller MB (2010) Mechanisms underlying spontaneous patterned activity in developing neural circuits. Nat Rev Neurosci 11(1):18–29

    Article  CAS  PubMed  Google Scholar 

  • Bolles RC, Woods PJ (1964) The ontogeny of behaviour in the albino rat. Anim Behav 12(4):427–441

    Article  Google Scholar 

  • 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):16–27

    Article  PubMed  Google Scholar 

  • 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):1065–1083

    Article  CAS  PubMed  Google Scholar 

  • Burkhalter A (1993) Development of forward and feedback connections between areas V1 and V2 of human visual cortex. Cereb Cortex 3(5):476–487

    Article  CAS  PubMed  Google Scholar 

  • 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):291–301

    Article  CAS  PubMed  Google Scholar 

  • 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 65:213–222

    Article  CAS  PubMed  Google Scholar 

  • 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):89–108

    Article  PubMed  Google Scholar 

  • Cappe C, Barone P (2005) Heteromodal connections supporting multisensory integration at low levels of cortical processing in the monkey. Eur J Neurosci 22(11):2886–2902

    Article  PubMed  Google Scholar 

  • 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):2025–2037

    Article  PubMed Central  PubMed  Google Scholar 

  • 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):2334–2348

    Article  PubMed  Google Scholar 

  • 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):2297–2320

    Article  PubMed  Google Scholar 

  • 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):2949–2963

    Article  PubMed  Google Scholar 

  • 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):1365–1376

    Article  PubMed  Google Scholar 

  • Clowry G, Molnar Z, Rakic P (2010) Renewed focus on the developing human neocortex. J Anat 217(4):276–288

    Article  PubMed Central  PubMed  Google Scholar 

  • Driver J, Noesselt T (2008) Multisensory interplay reveals crossmodal influences on ‘sensory-specific’ brain regions, neural responses, and judgments. Neuron 57(1):11–23

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ehret G (1976) Development of absolute auditory thresholds in the house mouse (Mus musculus). J Am Audiol Soc 1(5):179–184

    CAS  PubMed  Google Scholar 

  • 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)):438–454

    Article  Google Scholar 

  • Espinosa JS, Stryker MP (2012) Development and plasticity of the primary visual cortex. Neuron 75(2):230–249

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Feldman DE, Brecht M (2005) Map plasticity in somatosensory cortex. Science 310(5749):810–815

    Article  CAS  PubMed  Google Scholar 

  • Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1(1):1–47

    Article  CAS  PubMed  Google Scholar 

  • Finck A, Schneck CD, Hartman AF (1972) Development of cochlear function in the neonate Mongolian gerbil (Meriones unguiculatus). J Comp Physiol Psychol 78(3):375–380

    Article  CAS  PubMed  Google Scholar 

  • Finney EM, Fine I, Dobkins KR (2001) Visual stimuli activate auditory cortex in the deaf. Nat Neurosci 4(12):1171–1173

    Article  CAS  PubMed  Google Scholar 

  • Frasnelli J, Collignon O, Voss P, Lepore F (2011) Crossmodal plasticity in sensory loss. Prog Brain Res 191:233–249

    Article  PubMed  Google Scholar 

  • Fuller JL, Wimer RE (1966) Neural, sensory, and motor functions. Biology of the laboratory mouse. McGraw-Hill, New York, pp 609–628

    Google Scholar 

  • 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):2526–2536

    Article  CAS  PubMed  Google Scholar 

  • Gielen SC, Schmidt RA, Van den Heuvel PJ (1983) On the nature of intersensory facilitation of reaction time. Percept Psychophys 34(2):161–168

    Article  CAS  PubMed  Google Scholar 

  • 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):63–72

    Article  CAS  PubMed  Google Scholar 

  • Gleiss S, Kayser C (2012) Audio-visual detection benefits in the rat. PLoS One 7(9):e45677

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gougoux F, Lepore F, Lassonde M, Voss P, Zatorre RJ, Belin P (2004) Neuropsychology: pitch discrimination in the early blind. Nature 430(6997):309

    Article  CAS  PubMed  Google Scholar 

  • Groenewegen HJ, Witter MP (2004) Thalamus. In: Paxinos G (ed) The rat nervous system. Elsevier Academic Press, San Diego, pp 407–453

    Chapter  Google Scholar 

  • Grossenbacher PG, Lovelace CT (2001) Mechanisms of synesthesia: cognitive and physiological constraints. Trends Cogn Sci 5(1):36–41

    Article  PubMed  Google Scholar 

  • Guerreiro MJ, Putzar L, Roder B (2016) The effect of early visual deprivation on the neural bases of auditory processing. J Neurosci 36(5):1620–1630

    Article  CAS  PubMed  Google Scholar 

  • Hammond-Kenny A, Bajo VM, King AJ, Nodal FR (2017) Behavioural benefits of multisensory processing in ferrets. Eur J Neurosci 45(2):278–289

    Article  PubMed  Google Scholar 

  • 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):33–69

    Article  PubMed  Google Scholar 

  • Hensch TK (2004) Critical period regulation. Annu Rev Neurosci 27:549–579

    Article  CAS  PubMed  Google Scholar 

  • Hensch TK (2005) Critical period plasticity in local cortical circuits. Nat Rev Neurosci 6(11):877–888

    Article  CAS  PubMed  Google Scholar 

  • 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):955–977

    Article  PubMed  Google Scholar 

  • 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):65–74

    Article  CAS  PubMed  Google Scholar 

  • Horwitz B, Tagamets MA, McIntosh AR (1999) Neural modeling, functional brain imaging, and cognition. Trends Cogn Sci 3(3):91–98

    Article  CAS  PubMed  Google Scholar 

  • Hubbard EM, Brang D, Ramachandran VS (2011) The cross-activation theory at 10. J Neuropsychol 5(2):152–177

    Article  PubMed  Google Scholar 

  • Hubener M, Bonhoeffer T (2014) Neuronal plasticity: beyond the critical period. Cell 159(4):727–737

    Article  CAS  PubMed  Google Scholar 

  • 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):1031–1045

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Innocenti GM, Price DJ (2005) Exuberance in the development of cortical networks. Nat Rev Neurosci 6(12):955–965

    Article  CAS  PubMed  Google Scholar 

  • 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):814–828

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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):693–712

    Article  PubMed  Google Scholar 

  • Jacobs GH, Deegan JF 2nd (1994) Sensitivity to ultraviolet light in the gerbil (Meriones unguiculatus): characteristics and mechanisms. Vis Res 34(11):1433–1441

    Article  CAS  PubMed  Google Scholar 

  • Jones E (2007) Principles of thalamic organization. In: Jones E (ed) The thalamus. Cambridge University Press, Cambridge, pp 87–170

    Google Scholar 

  • Kaas JH, Collins CE (2003) Anatomic and functional reorganization of somatosensory cortex in mature primates after peripheral nerve and spinal cord injury. Adv Neurol 93:87–95

    PubMed  Google Scholar 

  • Kanold PO, Luhmann HJ (2010) The subplate and early cortical circuits. Annu Rev Neurosci 33:23–48

    Article  CAS  PubMed  Google Scholar 

  • Karlen SJ, Kahn DM, Krubitzer L (2006) Early blindness results in abnormal corticocortical and thalamocortical connections. Neuroscience 142(3):843–858

    Article  CAS  PubMed  Google Scholar 

  • Katz LC, Shatz CJ (1996) Synaptic activity and the construction of cortical circuits. Science 274(5290):1133–1138

    Article  CAS  PubMed  Google Scholar 

  • Kayser C, Logothetis NK (2007) Do early sensory cortices integrate cross-modal information? Brain Struct Funct 212(2):121–132

    Article  PubMed  Google Scholar 

  • Kilb W, Kirischuk S, Luhmann HJ (2011) Electrical activity patterns and the functional maturation of the neocortex. Eur J Neurosci 34(10):1677–1686

    Article  PubMed  Google Scholar 

  • Klemen J, Chambers CD (2012) Current perspectives and methods in studying neural mechanisms of multisensory interactions. Neurosci Biobehav Rev 36(1):111–133

    Article  PubMed  Google Scholar 

  • 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):12798–12805

    Article  CAS  PubMed  Google Scholar 

  • 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):96–100

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kobayasi KI, Suwa Y, Riquimaroux H (2013) Audiovisual integration in the primary auditory cortex of an awake rodent. Neurosci Lett 534:24–29

    Article  CAS  PubMed  Google Scholar 

  • Kolarik AJ, Cirstea S, Pardhan S, Moore BC (2014) A summary of research investigating echolocation abilities of blind and sighted humans. Hear Res 310:60–68

    Article  PubMed  Google Scholar 

  • 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 103:171–180

    Article  PubMed  Google Scholar 

  • Kotak VC, Pendola LM, Rodriguez-Contreras A (2012) Spontaneous activity in the developing gerbil auditory cortex in vivo involves GABAergic transmission. Neuroscience 226:130–144

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kral A, Sharma A (2012) Developmental neuroplasticity after cochlear implantation. Trends Neurosci 35(2):111–122

    Article  CAS  PubMed  Google Scholar 

  • Kupers R, Ptito M (2014) Compensatory plasticity and cross-modal reorganization following early visual deprivation. Neurosci Biobehav Rev 41:36–52

    Article  PubMed  Google Scholar 

  • Laramee ME, Boire D (2014) Visual cortical areas of the mouse: comparison of parcellation and network structure with primates. Front Neural Circuits 8:149

    PubMed  Google Scholar 

  • Lee HK, Whitt JL (2015) Cross-modal synaptic plasticity in adult primary sensory cortices. Curr Opin Neurobiol 35:119–126

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lessard N, Pare M, Lepore F, Lassonde M (1998) Early-blind human subjects localize sound sources better than sighted subjects. Nature 395(6699):278–280

    Article  CAS  PubMed  Google Scholar 

  • Lomber SG, Meredith MA, Kral A (2010) Cross-modal plasticity in specific auditory cortices underlies visual compensations in the deaf. Nat Neurosci 13(11):1421–1427

    Article  CAS  PubMed  Google Scholar 

  • Lopez-Bendito G, Molnar Z (2003) Thalamocortical development: how are we going to get there? Nat Rev Neurosci 4(4):276–289

    Article  CAS  PubMed  Google Scholar 

  • Loskota WJ, Lomax P, Verity MA (1974) A stereotaxic atlas of the Mongolian gerbil (Meriones unguiculatus). Ann Arbor Science, Michigan

    Google Scholar 

  • Maidenbaum S, Abboud S, Amedi A (2014) Sensory substitution: closing the gap between basic research and widespread practical visual rehabilitation. Neurosci Biobehav Rev 41:3–15

    Article  PubMed  Google Scholar 

  • Markov NT, Kennedy H (2013) The importance of being hierarchical. Curr Opin Neurobiol 23(2):187–194

    Article  CAS  PubMed  Google Scholar 

  • 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):4361–4378

    PubMed  Google Scholar 

  • McGovern DP, Astle AT, Clavin SL, Newell FN (2016) Task-specific transfer of perceptual learning across sensory modalities. Curr Biol 26(1):R20–R21

    Article  CAS  PubMed  Google Scholar 

  • Meng X, Kao JP, Lee HK, Kanold PO (2015) Visual deprivation causes refinement of intracortical circuits in the auditory cortex. Cell Rep 12(6):955–964

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Merabet LB, Pascual-Leone A (2010) Neural reorganization following sensory loss: the opportunity of change. Nat Rev Neurosci 11(1):44–52

    Article  CAS  PubMed  Google Scholar 

  • Meredith MA, Allman BL (2012) Early hearing-impairment results in crossmodal reorganization of ferret core auditory cortex. Neural Plast 2012:601591

    Article  PubMed Central  PubMed  Google Scholar 

  • Meredith MA, Lomber SG (2011) Somatosensory and visual crossmodal plasticity in the anterior auditory field of early-deaf cats. Hear Res 280(1–2):38–47

    Article  PubMed Central  PubMed  Google Scholar 

  • Meredith MA, Lomber SG (2017) Species-dependent role of crossmodal connectivity among the primary sensory cortices. Hear Res 343:83–91

    Article  PubMed  Google Scholar 

  • 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):32–40

    Article  PubMed  Google Scholar 

  • 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):115–128

    Article  PubMed  Google Scholar 

  • Mowery TM, Kotak VC, Sanes DH (2016) The onset of visual experience gates auditory cortex critical periods. Nat Commun 7:10416

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Murray MM, Lewkowicz DJ, Amedi A, Wallace MT (2016) Multisensory processes: a balancing act across the lifespan. Trends Neurosci 39(8):567–579

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Navarro X, Vivo M, Valero-Cabre A (2007) Neural plasticity after peripheral nerve injury and regeneration. Prog Neurobiol 82(4):163–201

    Article  CAS  PubMed  Google Scholar 

  • 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):13609–13623

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nys J, Scheyltjens I, Arckens L (2015) Visual system plasticity in mammals: the story of monocular enucleation-induced vision loss. Front Syst Neurosci 9:60

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pallas SL (2001) Intrinsic and extrinsic factors that shape neocortical specification. Trends Neurosci 24(7):417–423

    Article  CAS  PubMed  Google Scholar 

  • Paperna T, Malach R (1991) Patterns of sensory intermodality relationships in the cerebral cortex of the rat. J Comp Neurol 308(3):432–456

    Article  CAS  PubMed  Google Scholar 

  • 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 Diego

    Google Scholar 

  • 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):664–673

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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):8790–8801

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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):1144–1156

    Article  CAS  PubMed  Google Scholar 

  • 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):471–474

    Article  CAS  PubMed  Google Scholar 

  • 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):910–920

    Article  PubMed  Google Scholar 

  • Proulx MJ, Brown DJ, Pasqualotto A, Meijer P (2014) Multisensory perceptual learning and sensory substitution. Neurosci Biobehav Rev 41:16–25

    Article  PubMed  Google Scholar 

  • 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):1–272

    Article  PubMed Central  PubMed  Google Scholar 

  • Rauschecker JP (1995) Compensatory plasticity and sensory substitution in the cerebral cortex. Trends Neurosci 18(1):36–43

    Article  CAS  PubMed  Google Scholar 

  • 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):5063–5067

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Renier L, De Volder AG, Rauschecker JP (2014) Cortical plasticity and preserved function in early blindness. Neurosci Biobehav Rev 41:53–63

    Article  PubMed  Google Scholar 

  • Roder B, Teder-Salejarvi W, Sterr A, Rosler F, Hillyard SA, Neville HJ (1999) Improved auditory spatial tuning in blind humans. Nature 400(6740):162–166

    Article  CAS  PubMed  Google Scholar 

  • 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):466–471

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 86:483–503

    Article  CAS  PubMed  Google Scholar 

  • Ryan A (1976) Hearing sensitivity of the mongolian gerbil, Meriones unguiculatis. J Acoust Soc Am 59(5):1222–1226

    Article  CAS  PubMed  Google Scholar 

  • Ryugo DK, Ryugo R, Globus A, Killackey HP (1975) Increased spine density in auditory cortex following visual or somatic deafferentation. Brain Res 90(1):143–146

    Article  CAS  PubMed  Google Scholar 

  • Sachs L (2004) Angewandte Statistik (Applied statistics). Springer, Heidelberg

    Book  Google Scholar 

  • 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):526–528

    Article  CAS  PubMed  Google Scholar 

  • Sakata S, Yamamori T, Sakurai Y (2004) Behavioral studies of auditory-visual spatial recognition and integration in rats. Exp Brain Res 159(4):409–417

    Article  PubMed  Google Scholar 

  • 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 155:287–311

    Article  CAS  PubMed  Google Scholar 

  • Schroeder CE, Foxe J (2005) Multisensory contributions to low-level, ‘unisensory’ processing. Curr Opin Neurobiol 15(4):454–458

    Article  CAS  PubMed  Google Scholar 

  • Schwentker V (1963) The gerbil. A new laboratory animal. Ill Vet 6:5–9

    Google Scholar 

  • 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):e1002304

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Smilek D, Dixon MJ, Cudahy C, Merikle PM (2001) Synaesthetic photisms influence visual perception. J Cogn Neurosci 13(7):930–936

    Article  CAS  PubMed  Google Scholar 

  • 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):635–651

    Article  CAS  PubMed  Google Scholar 

  • Spector F, Maurer D (2009) Synesthesia: a new approach to understanding the development of perception. Dev Psychol 45(1):175–189

    Article  PubMed  Google Scholar 

  • 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 8:93

    Article  PubMed Central  PubMed  Google Scholar 

  • Stein BE, Stanford TR (2008) Multisensory integration: current issues from the perspective of the single neuron. Nat Rev Neurosci 9(4):255–266

    Article  CAS  PubMed  Google Scholar 

  • 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):1713–1720

    Article  PubMed Central  PubMed  Google Scholar 

  • Stein BE, Stanford TR, Rowland BA (2014) Development of multisensory integration from the perspective of the individual neuron. Nat Rev Neurosci 15(8):520–535

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Stiles NR, Shimojo S (2015) Auditory sensory substitution is intuitive and automatic with texture stimuli. Sci Rep 5:15628

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sur M, Rubenstein JL (2005) Patterning and plasticity of the cerebral cortex. Science 310(5749):805–810

    Article  CAS  PubMed  Google Scholar 

  • 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):106–114

    Article  CAS  PubMed  Google Scholar 

  • 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 159:459–472

    Article  PubMed  Google Scholar 

  • Thiessen DD, Yahr P (1977) The gerbil in behavioral investigations. Mechanisms of territoriality and olfactory communication. University of Texas Press, Austin

    Google Scholar 

  • 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):341–355

    Article  PubMed  Google Scholar 

  • 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):35–46

    Article  CAS  PubMed  Google Scholar 

  • 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):11–28

    Article  CAS  PubMed  Google Scholar 

  • 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):1129–1147

    CAS  PubMed  Google Scholar 

  • Ward J (2013) Synesthesia. Annu Rev Psychol 64:49–75

    Article  PubMed  Google Scholar 

  • Wickersham IR, Finke S, Conzelmann KK, Callaway EM (2007) Retrograde neuronal tracing with a deletion-mutant rabies virus. Nat Methods 4(1):47–49

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson F (1986) Eye and brain growth in the Mongolian gerbil (Meriones unguiculatus). Behav Brain Res 19(1):59–69

    Article  CAS  PubMed  Google Scholar 

  • 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):731–742

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgements

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 (http://www.dfg.de) SFB TRR31 (J.U.H., F.W.O., E.B.) and NIH (http://www.nih.gov) RO1 DC009607 (P.O.K.).

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Authors and Affiliations

  1. Department Systems Physiology of Learning, Leibniz Institute for Neurobiology, Brenneckestr. 6, 39118, Magdeburg, Germany

    Julia U. Henschke, Frank W. Ohl, Jürgen Goldschmidt & Eike Budinger

  2. German Center for Neurodegenerative Diseases Within the Helmholtz Association, Leipziger Str. 44, 39120, Magdeburg, Germany

    Julia U. Henschke

  3. Institute of Cognitive Neurology and Dementia Research (IKND), Otto-von-Guericke-University Magdeburg, Leipziger Str. 44, 39120, Magdeburg, Germany

    Julia U. Henschke

  4. Research Group Neuropharmacology, Leibniz Institute for Neurobiology, Brenneckestr. 6, 39118, Magdeburg, Germany

    Anja M. Oelschlegel

  5. Institute of Anatomy, Otto-von-Guericke-University Magdeburg, Leipziger Str. 44, 39120, Magdeburg, Germany

    Anja M. Oelschlegel

  6. Functional Neuroimaging Group, German Center for Neurodegenerative Diseases Within the Helmholtz Association, Leipziger Str. 44, 39120, Magdeburg, Germany

    Frank Angenstein

  7. Institute of Biology, Otto-von-Guericke-University Magdeburg, Leipziger Str. 44, 39120, Magdeburg, Germany

    Frank W. Ohl

  8. Department of Biology, University of Maryland, College Park, MD, 20742, USA

    Patrick O. Kanold

  9. Center for Behavioral Brain Sciences, Universitätsplatz 2, 39120, Magdeburg, Germany

    Julia U. Henschke, Frank Angenstein, Frank W. Ohl, Jürgen Goldschmidt & Eike Budinger

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  1. Julia U. Henschke
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  2. Anja M. Oelschlegel
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  3. Frank Angenstein
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Correspondence to Eike Budinger.

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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.

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Henschke, J.U., Oelschlegel, A.M., Angenstein, F. et al. Early sensory experience influences the development of multisensory thalamocortical and intracortical connections of primary sensory cortices. Brain Struct Funct 223, 1165–1190 (2018). https://doi.org/10.1007/s00429-017-1549-1

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