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Corticofugal modulation of the midbrain frequency map in the bat auditory system

Abstract

The auditory system, like the visual and somatosensory systems, contains topographic maps in its central neural pathways. These maps can be modified by sensory deprivation, injury and experience in both young and adult animals. Such plasticity has been explained by changes in the divergent and convergent projections of the ascending sensory system. Another possibility, however, is that plasticity may be mediated by descending corticofugal connections. We have investigated the role of descending connections from the cortex to the inferior colliculus of the big brown bat. Electrical stimulation of the auditory cortex causes a downward shift in the preferred frequencies of collicular neurons toward that of the stimulated cortical neurons. This results in a change in the frequency map within the colliculus. Moreover, similar changes can be induced by repeated bursts of sound at moderate intensities. Thus, one role of the mammalian corticofugal system may be to modify subcortical sensory maps in response to sensory experience.

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Figure 1: Shift in the frequency map of the inferior colliculus (IC) evoked by a focal electrical stimulation (ES) of the auditory cortex (AC) paired with an acoustic stimulus (AS).
Figure 2: Shifts in the frequency map of the inferior colliculus evoked by focal electrical stimulation of the auditory cortex paired with an acoustic stimulus (a-c).
Figure 3: Changes in the frequency-response curves of three single collicular neurons evoked by focal electrical stimulation of the auditory cortex paired with an acoustic stimulus (a-c), and changes in response magnitudes (d) and BF's (e) of 42 single collicular neurons as a function of BF difference between collicular and electrically stimulated cortical neurons.

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References

  1. Kelly, J.P. & Wong, D. Laminar connections of the cat's auditory cortex. Brain Res. 212, 1– 15 (1981)

    Article  CAS  Google Scholar 

  2. Saldana, E., Feliciano, M. & Mugnaini, E. Distribution of descending projections from primary auditory neocortex to inferior colliculus mimics the topography of the intracollicular projections . J. Comp. Neurol. 371, 15– 40 (1996)

    Article  CAS  Google Scholar 

  3. Huffman, R.F. & Henson, O.W. Jr. The descending auditory pathway and acousticomotor systems: connections with the inferior colliculus . Brain Res. Rev. 15, 295– 323 (1990)

    Article  CAS  Google Scholar 

  4. Andersen, R.A., Snyder, R.L. & Merzenich, M.M. The topographic organization of corticocollicular projections from physiologically identified loci in the AI, AII, and anterior auditory cortical field of the cat. J. Comp. Neurol. 191, 479–494 (1980)

    Article  CAS  Google Scholar 

  5. Herbert, H., Aschoff, A. & Ostwald, J. Topography of projections from the auditory cortex to the inferior colliculus in the rat. J. Comp. Neurol. 304, 103– 122 (1991)

    Article  CAS  Google Scholar 

  6. Massopust, L.C. Jr. & Ordy, J.M. Auditory organization of the inferior colliculus in the cat. Exp. Neurol. 6, 465–477 (1962)

    Article  Google Scholar 

  7. Watanabe, T., Yanagisawa, K., Kamzaki, J. & Katsuki, Y. Cortical efferent flow influencing unit responses of medial geniculate body to sound stimulation . Exp. Brain Res. 2, 302– 317 (1966)

    Article  CAS  Google Scholar 

  8. Amato, G., La Grutta, V. & Enia, F. The control exerted by the auditory cortex on the activity of the medial geniculate body and inferior colliculus. Arch. Sci. Biol. 53, 291–313 (1969)

    CAS  Google Scholar 

  9. Sun, X., Chen, Q.C. & Jen, P.H. Corticofugal control of central auditory sensitivity in the big brown bat, Eptesicus fuscus. Neurosci. Lett. 212, 131 –134 (1996)

    Article  CAS  Google Scholar 

  10. Andersen, P., Junge, K. & Sveen, O. Cortico-fugal facilitation of thalamic transmission. Brain Behav. Evol. 6, 170–184 (1972)

    Article  CAS  Google Scholar 

  11. Villa, A.P.E. et al. Corticofugal modulation of the information processing in the auditory thalamus of the cat . Exp. Brain Res. 86, 506– 517 (1991)

    Article  CAS  Google Scholar 

  12. Ryugo, D.K. & Weinberger, N.M. Corticofugal modulation of the medial geniculate body. Exp. Neurol. 51, 377–391 (1976)

    Article  CAS  Google Scholar 

  13. Syka, J. & Popelar, J. Inferior colliculus in the rat: neuronal responses to stimulation of the auditory cortex. Neurosci. Lett. 51, 235–240 (1984)

    Article  CAS  Google Scholar 

  14. Sun, X., Jen, P.H.S., Sun, D. & Zhang, S. Corticofugal influences on the responses of bat inferior colliculus to sound stimulation. Brain Res. 495, 1–8 (1989)

    Article  CAS  Google Scholar 

  15. Yan, J. & Suga, N. Corticofugal modulation of time-domain processing of biosonar information in bats. Science 273, 1100–1103 (1996)

    Article  CAS  Google Scholar 

  16. Zhang, Y., Suga, N. & Yan, J. Corticofugal modulation of frequency processing in bat auditory system. Nature 387, 900–903 (1997)

    Article  CAS  Google Scholar 

  17. Casseday, J.H. & Covey, E. Frequency tuning properties of neurons in the inferior colliculus of an FM bat. J. Comp. Physiol. 319, 34–50 (1992)

    CAS  Google Scholar 

  18. Hubel, D.H., Wiesel, T.N. & Levay, S. Plasticity of ocular dominance columns in monkey striate cortex. Philos. Trans. R. Soc. Lond. Biol. 278, 377– 409 (1977)

    Article  CAS  Google Scholar 

  19. Irvine, D.R.F. & Rajan, R. Injury- and use-related plasticity in the primary sensory cortex of adult mammals: possible relationship to perceptual learning. Clin. and Exp. Pharmacol. and Physiol. 23 , 939–947 (1996)

    Article  CAS  Google Scholar 

  20. Recanzone, G.H., Schreiner, C.E. & Merzenich, M.M. Plasticity in the frequency representation of primary auditory cortex following discrimination training in adult owl monkeys. J. Neurosci. 13, 87–103 (1993)

    Article  CAS  Google Scholar 

  21. Kaas, J.H. et al. Reorganization of retinotopic cortical maps in adult mammals after lesions of the retina . Science 248, 229–231 (1990)

    Article  CAS  Google Scholar 

  22. Pettet, M.W. & Gilbert, C.D. Dynamic changes in receptive-field size in cat primary visual cortex. Proc. Natl. Acad. Sci. USA 89, 8366–8370 (1992)

    Article  CAS  Google Scholar 

  23. Merzenich, M.M. et al. Somatosensory cortical map changes following digit amputation in adult monkeys. J. Comp. Neurol. 224, 591–605 (1984)

    Article  CAS  Google Scholar 

  24. Clark, S.A., Allard, T., Jenkins, W.M. & Merzenich, M.M. Receptive fields in the body-surface map in adult cortex defined by temporally correlated inputs. Nature 332, 444– 445 (1988)

    Article  CAS  Google Scholar 

  25. Jenkins, W.M., Merzenich, M.M. & Recanzone, G. Neocortical representational dynamics in adult primates: implications for neuropsychology. Neuropsychologia 28, 573–584 (1990)

    Article  CAS  Google Scholar 

  26. Weinberger, N.M., Javid, R. & Lepan, B. Long-term retention of learning-induced receptive field plasticity in the auditory cortex. Proc. Natl. Acad. Sci. USA 90, 2394–2398 (1993)

    Article  CAS  Google Scholar 

  27. Snyder, R.L., Rebscher, S.J., Cao, K.L., Leake, P.A. & Kelly, K. Chronic intracochlear electrical stimulation in the neonatally deafened cat.I: Expansion of central representation. Hear. Res. 50, 7–33 (1990)

    Article  CAS  Google Scholar 

  28. Snyder, R.L., Rebscher, S.J., Leake, P.A., Kelly, K. & Cao, K. Chronic intracochlear electrical stimulation in the neonatally deafened cat.II: Temporal properties of neurons in the inferior colliculus. Hear. Res. 56, 246–264 (1991)

    Article  CAS  Google Scholar 

  29. He, J.F. Modulatory effects of regional cortical activation on the onset responses of the cat medial geniculate neurons. J. Neurophysiol. 77, 896– 908 (1997)

    Article  CAS  Google Scholar 

  30. Suga, N. Single unit activity in cochlear nucleus and inferior colliculus of echo-locating bats. J. Physiol. 172, 449–474 (1964)

    Article  CAS  Google Scholar 

  31. Evans, E.F. The sharpening of cochlear frequency selectivity in the normal and abnormal cochlea. Audiology 14, 419–442 (1975)

    Article  CAS  Google Scholar 

  32. Liberman, M.C. Auditory-nerve response from cats raised in a low-noise chamber. J. Acoust. Soc. Am. 63, 442–455 (1978)

    Article  CAS  Google Scholar 

  33. Katsuki, Y., Suga, N. & Kanno, Y. Neural mechanisms of the peripheral and central auditory system in monkeys . J. Acoust. Soc. Am. 34, 1396– 1410 (1962)

    Article  Google Scholar 

  34. Suga, N. & Jen, P.H.S. Further studies on the peripheral auditory system of 'CF-FM' bats specialized for fine frequency analysis of Doppler-shifted echoes. J. Exp. Biol. 69, 207– 232 (1977)

    CAS  Google Scholar 

  35. Nudo, R.J., Wise, B.M., SiFuentes, F. & Milliken, G.W. Neural substrates for the effects of rehabilitative training on motor recovery after ischemic infarct. Science. 272, 1791– 1794 (1996)

    Article  CAS  Google Scholar 

  36. Recanzone, G.H., Merzenich, M.M. & Dinse, H.R. Expansion of the cortical representation of a specific skin field in primary somatosensory cortex by intracortical microstimulation . Cerebral Cortex 2, 181– 196 (1992)

    Article  CAS  Google Scholar 

  37. Spengler, F & Dinse, H.R. Reversible relocation of representational boundaries of adult rats by intracortical microstimulation. Neuroreport 5, 949–953 (1994)

    Article  CAS  Google Scholar 

  38. Jen, P.H., Sun, X.D. & Lin, P.J. Frequency and space representation in the primary auditory cortex of the frequency modulating bat Eptesicus fuscus. J. Comp. Physiol. A 165, 1–14 (1989)

    Article  CAS  Google Scholar 

  39. Dear, S.P., Simmons, J.A. & Fritz, J. A possible neuronal basis for representation of acoustic scenes in auditory cortex of the big brown bat. Nature 364, 620–623 (1993)

    Article  CAS  Google Scholar 

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Acknowledgements

The big brown bats used for this work were supplied by Dr. S. Dear. We thank Drs. S. Dear, D. Fitzpatrick, S. Kuwada, J.F. Olsen, W. E. O'Neill, Mr. A. Kadir and Mr. N. Laleman for their comments on the manuscript. This work has been supported by a research grant from National Institute on Deafness and Other Communicative Disorders (DC 00175).

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Correspondence to Nobuo Suga.

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Yan, W., Suga, N. Corticofugal modulation of the midbrain frequency map in the bat auditory system. Nat Neurosci 1, 54–58 (1998). https://doi.org/10.1038/255

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