Skip to main content

Advertisement

Log in

Excitatory Crossmodal Input to a Widespread Population of Primary Sensory Cortical Neurons

  • Original Article
  • Published:
Neuroscience Bulletin Aims and scope Submit manuscript

Abstract

Crossmodal information processing in sensory cortices has been reported in sparsely distributed neurons under normal conditions and can undergo experience- or activity-induced plasticity. Given the potential role in brain function as indicated by previous reports, crossmodal connectivity in the sensory cortex needs to be further explored. Using perforated whole-cell recording in anesthetized adult rats, we found that almost all neurons recorded in the primary somatosensory, auditory, and visual cortices exhibited significant membrane-potential responses to crossmodal stimulation, as recorded when brain activity states were pharmacologically down-regulated in light anesthesia. These crossmodal cortical responses were excitatory and subthreshold, and further seemed to be relayed primarily by the sensory thalamus, but not the sensory cortex, of the stimulated modality. Our experiments indicate a sensory cortical presence of widespread excitatory crossmodal inputs, which might play roles in brain functions involving crossmodal information processing or plasticity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  1. Ghazanfar AA, Schroeder CE. Is neocortex essentially multisensory? Trends Cogn Sci 2006, 10: 278–285.

    Article  PubMed  Google Scholar 

  2. Wallace MT, Ramachandran R, Stein BE. A revised view of sensory cortical parcellation. Proc Natl Acad Sci U S A 2004, 101: 2167–2172.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Shimojo S, Shams L. Sensory modalities are not separate modalities: Plasticity and interactions. Curr Opin Neurobiol 2001, 11: 505–509.

    Article  PubMed  CAS  Google Scholar 

  4. Olcese U, Iurilli G, Medini P. Cellular and synaptic architecture of multisensory integration in the mouse neocortex. Neuron 2013, 79: 579–593.

    Article  PubMed  CAS  Google Scholar 

  5. Sathian K, Zangaladze A. Feeling with the mind’s eye: Contribution of visual cortex to tactile perception. Behav Brain Res 2002, 135: 127–132.

    Article  PubMed  CAS  Google Scholar 

  6. von Kriegstein K, Kleinschmidt A, Sterzer P, Giraud AL. Interaction of face and voice areas during speaker recognition. J Cogn Neurosci 2005, 17: 367–376.

    Article  Google Scholar 

  7. Morrell F. Visual system’s view of acoustic space. Nature 1972, 238: 44–46.

    Article  PubMed  CAS  Google Scholar 

  8. Luo H, Liu ZX, Poeppel D. Auditory cortex tracks both auditory and visual stimulus dynamics using low-frequency neuronal phase modulation. PLoS Biol 2010, 8: e1000445.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Fu KM, Johnston TA, Shah AS, Arnold L, Smiley J, Hackett TA. Auditory cortical neurons respond to somatosensory stimulation. J Neurosci 2003, 23: 7510–7515.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Giard MH, Peronnet F. Auditory-visual integration during multimodal object recognition in humans: A behavioral and electrophysiological study. J Cogn Neurosci 1999, 11: 473–490.

    Article  PubMed  CAS  Google Scholar 

  11. Schwartz JL, Berthommier F, Savariaux C. Seeing to hear better: Evidence for early audio-visual interactions in speech identification. Cognition 2004, 93: B69–B78.

    Article  PubMed  Google Scholar 

  12. Zhou YD, Fuster JM. Visuo-tactile cross-modal associations in cortical somatosensory cells. Proc Natl Acad Sci U S A 2000, 97: 9777–9782.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Zhou YD, Fuster JM. Somatosensory cell response to an auditory cue in a haptic memory task. Behav Brain Res 2004, 153: 573–578.

    Article  PubMed  Google Scholar 

  14. Falchier A, Clavagnier S, Barone P, Kennedy H. Anatomical evidence of multimodal integration in primate striate cortex. J Neurosci 2002, 22: 5749–5759.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Calvert GA, Brammer MJ, Iversen SD. Crossmodal identification. Trends Cogn Sci 1998, 2: 247–253.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  17. Rockland KS, Ojima H. Multisensory convergence in calcarine visual areas in macaque monkey. Int J Psychophysiol 2003, 50: 19–26.

    Article  PubMed  Google Scholar 

  18. Macaluso E, Frith CD, Driver J. Modulation of human visual cortex by crossmodal spatial attention. Science 2000, 289: 1206–1208.

    Article  PubMed  CAS  Google Scholar 

  19. Goldman-Rakic PS. Topography of cognition: Parallel distributed networks in primate association cortex. Annu Rev Neurosci 1988, 11: 137–156.

    Article  PubMed  CAS  Google Scholar 

  20. Bavelier D, Neville HJ. Cross-modal plasticity: Where and how? Nat Rev Neurosci 2002, 3: 443–452.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  22. Merabet LB, Pascual-Leone A. Neural reorganization following sensory loss: The opportunity of change. Nat Rev Neurosci 2010, 11: 44–52.

    Article  PubMed  CAS  Google Scholar 

  23. Singh AK, Phillips F, Merabet LB, Sinha P. Why does the cortex reorganize after sensory loss? Trends Cogn Sci 2018, 22: 569–582.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Joassin F, Pesenti M, Maurage P, Verreckt E, Bruyer R, Campanella S. Cross-modal interactions between human faces and voices involved in person recognition. Cortex 2011, 47: 367–376.

    Article  PubMed  Google Scholar 

  25. Goda N, Yokoi I, Tachibana A, Minamimoto T, Komatsu H. Crossmodal association of visual and haptic material properties of objects in the monkey ventral visual cortex. Curr Biol 2016, 26: 928–934.

    Article  PubMed  CAS  Google Scholar 

  26. Bizley JK, Maddox RK, Lee AKC. Defining auditory-visual objects: Behavioral tests and physiological mechanisms. Trends Neurosci 2016, 39: 74–85.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. von Kriegstein K, Giraud AL. Implicit multisensory associations influence voice recognition. PLoS Biol 2006, 4: e326.

    Article  CAS  Google Scholar 

  28. Atilgan H, Town SM, Wood KC, Jones GP, Maddox RK, Lee AKC, et al. Integration of visual information in auditory cortex promotes auditory scene analysis through multisensory binding. Neuron 2018, 97: 640-655.e4.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Vincis R, Fontanini A. Associative learning changes cross-modal representations in the gustatory cortex. Elife 2016, 5: e16420.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Gottfried JA, Dolan RJ. The nose smells what the eye sees: Crossmodal visual facilitation of human olfactory perception. Neuron 2003, 39: 375–386.

    Article  PubMed  CAS  Google Scholar 

  31. Desgent S, Ptito M. Cortical GABAergic interneurons in cross-modal plasticity following early blindness. Neural Plast 2012, 2012: 590725.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Ibrahim LA, Mesik L, Ji XY, Fang Q, Li HF, Li YT, et al. Cross-modality sharpening of visual cortical processing through layer-1-mediated inhibition and disinhibition. Neuron 2016, 89: 1031–1045.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Leitão J, Thielscher A, Werner S, Pohmann R, Noppeney U. Effects of parietal TMS on visual and auditory processing at the primary cortical level—a concurrent TMS-fMRI study. Cereb Cortex 2013, 23: 873–884.

    Article  PubMed  Google Scholar 

  34. Convento S, Rahman MS, Yau JM. Selective attention gates the interactive crossmodal coupling between perceptual systems. Curr Biol 2018, 28: 746-752.e5.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Iurilli G, Ghezzi D, Olcese U, Lassi G, Nazzaro C, Tonini R, et al. Sound-driven synaptic inhibition in primary visual cortex. Neuron 2012, 73: 814–828.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Liu YZ, Wang Y, Tang W, Zhu JY, Wang ZR. NMDA receptor-gated visual responses in hippocampal CA1 neurons. J Physiol 2018, 596: 1965–1979.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Shang CF, Dan Y, Poo MM, Wang ZR. Periodic stimulation induces long-range modulation of cortical responses and visual perception. J Physiol 2011, 589: 3125–3133.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Sally SL, Kelly JB. Organization of auditory cortex in the albino rat: Sound frequency. J Neurophysiol 1988, 59: 1627–1638.

    Article  PubMed  CAS  Google Scholar 

  40. Doron NN, Ledoux JE, Semple MN. Redefining the tonotopic core of rat auditory cortex: Physiological evidence for a posterior field. J Comp Neurol 2002, 453: 345–360.

    Article  PubMed  Google Scholar 

  41. Ma LQ, Ning L, Wang ZR, Wang YW. Visual and noxious electrical stimulus-evoked membrane-potential responses in anterior cingulate cortical neurons. Mol Brain 2016, 9: 82.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Amzica F, Steriade M. Cellular substrates and laminar profile of sleep K-complex. Neuroscience 1998, 82: 671–686.

    Article  PubMed  CAS  Google Scholar 

  43. Wang Y, Liu YZ, Wang LD, Tang W, Wang ZR. Silent synapse unsilencing in hippocampal CA1 neurons for associative fear memory storage. Cereb Cortex 2019, 29: 4067–4076.

    Article  PubMed  Google Scholar 

  44. Iskit AB, Guc MO. Comparison of sodium pentobarbitone and urethane anesthesia in a rat model of coronary artery occlusion and reperfusion arrhythmias: Interaction with L-NAME. Pharmacol Res 1996, 33: 13–18.

    Article  PubMed  CAS  Google Scholar 

  45. Cahusac PM. Cortical layer-specific effects of the metabotropic glutamate receptor agonist 1S, 3R-ACPD in rat primary somatosensory cortex in vivo. Eur J Neurosci 1994, 6: 1505–1511.

    Article  PubMed  CAS  Google Scholar 

  46. Simons DJ, Woolsey TA. Morphology of Golgi-Cox-impregnated barrel neurons in rat SmI cortex. J Comp Neurol 1984, 230: 119–132.

    Article  PubMed  CAS  Google Scholar 

  47. Senkowski D, Schneider TR, Foxe JJ, Engel AK. Crossmodal binding through neural coherence: Implications for multisensory processing. Trends Neurosci 2008, 31: 401–409.

    Article  PubMed  CAS  Google Scholar 

  48. Sur M, Garraghty PE, Roe AW. Experimentally induced visual projections into auditory thalamus and cortex. Science 1988, 242: 1437–1441.

    Article  PubMed  CAS  Google Scholar 

  49. Sur M, Angelucci A, Sharma J. Rewiring cortex: The role of patterned activity in development and plasticity of neocortical circuits. J Neurobiol 1999, 41: 33–43.

    Article  PubMed  CAS  Google Scholar 

  50. Budinger E, Scheich H. Anatomical connections suitable for the direct processing of neuronal information of different modalities via the rodent primary auditory cortex. Hear Res 2009, 258: 16–27.

    Article  PubMed  Google Scholar 

  51. Aronoff R, Matyas F, Mateo C, Ciron C, Schneider B, Petersen CCH. Long-range connectivity of mouse primary somatosensory barrel cortex. Eur J Neurosci 2010, 31: 2221–2233.

    Article  PubMed  Google Scholar 

  52. Froudarakis E, Fahey PG, Reimer J, Smirnakis SM, Tehovnik EJ, Tolias AS. The visual cortex in context. Annu Rev Vis Sci 2019, 5: 317–339.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Wang JJ, Sun P, Lv XH, Jin S, Li AN, Kuang JX, et al. Divergent projection patterns revealed by reconstruction of individual neurons in orbitofrontal cortex. Neurosci Bull 2021, 37: 461–477.

    Article  PubMed  Google Scholar 

  54. McIntyre DC, Kelly ME, Staines WA. Efferent projections of the anterior perirhinal cortex in the rat. J Comp Neurol 1996, 369: 302–318.

    Article  PubMed  CAS  Google Scholar 

  55. Miller MW, Vogt BA. Direct connections of rat visual cortex with sensory, motor, and association cortices. J Comp Neurol 1984, 226: 184–202.

    Article  PubMed  CAS  Google Scholar 

  56. Felleman DJ, van Essen DC. Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1991, 1: 1–47.

    Article  PubMed  CAS  Google Scholar 

  57. Nikbakht N, Tafreshiha A, Zoccolan D, Diamond ME. Supralinear and supramodal integration of visual and tactile signals in rats: Psychophysics and neuronal mechanisms. Neuron 2018, 97: 626-639.e8.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  58. Lu CB, Yang T, Zhao H, Zhang M, Meng FC, Fu H, et al. Insular cortex is critical for the perception, modulation, and chronification of pain. Neurosci Bull 2016, 32: 191–201.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Konsman JP. The mouse brain in stereotaxic coordinates. Psychoneuroendocrinology 2003, 28: 827–828.

    Article  Google Scholar 

Download references

Acknowledgements

We thank Drs. J. Tsien, L. Zhang, Y. Zhou, and J. Du for suggestions and comments on this work, and Dr. X. Yuan for the help with the tracing experiments. This work was supported by grants from the National Natural Science Foundation of China (31970957 and 31471078), the Shanghai Science and Technology Commission (19ZR1416600), and funding from 2021-JCJQ-JJ-1089.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Zheng Zhao or Zhiru Wang.

Ethics declarations

Conflict of interest

The authors declare no competing interests concerning the subject of this study.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file 1 (PDF 569 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xiao, YJ., Wang, L., Liu, YZ. et al. Excitatory Crossmodal Input to a Widespread Population of Primary Sensory Cortical Neurons. Neurosci. Bull. 38, 1139–1152 (2022). https://doi.org/10.1007/s12264-022-00855-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12264-022-00855-4

Keywords

Navigation