Skip to main content
SpringerLink
Log in

Neural Mechanism of Corticofugal Modulation of Tuning Property in Frequency Domain of Bat’s Auditory System

  • Published:
Neural Processing Letters Aims and scope Submit manuscript

Abstract

It is quite important for sensory processing to understand how feedback modulates the information processing in early brain areas in order to extract behaviorally-relevant features of stimulus. The auditory system of bats provides an ideal system for clarifying the mechanism of the adaptive processing by feedback. To investigate this mechanism, we developed a neural network model of bat’s auditory system for detecting Doppler-shifted frequency of sound echoes. Using the model, we demonstrate the receptive field modulation of cortical neurons and the modulation of the feedback to IC neurons, evoked by an electric stimulation and a GABA antagonist. Our model reproduces qualitatively the experimental results of best frequency (BF) shifts by Xiao and Suga (Proc Natl Acad Sci USA 99(24):15743–15748, 2002). We also show how the modulations cause the BF shifts of cortical and subcortical neurons. Furthermore we investigate the neuronal characteristics required for enhancing BF shifts.

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

Access this article

Log in via an institution

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

Similar content being viewed by others

References

  1. Anderson JS, Carandini M, Ferster DSJ, Car M, Orientation DF (2000) Orientation tuning of input conductance, excitation, and inhibition in cat primary visual cortex. J Neurophysiol 84:909–926

    Google Scholar 

  2. Ashida G, Carr CE (2011) Sound localization: Jeffress and beyond. Curr Opin Neurobiol 21(5):745–751

    Article  Google Scholar 

  3. Bishop AL, Henson OW (1987) The efferent cochlear projections of the superior olivary complex in the mustached bat. Hear Res 31:175–182

    Article  Google Scholar 

  4. Buonomano DV, Merzenich MM (1998) Cortical plasticity: from synapses to maps. Annu Rev Neurosci 21:149–186

    Article  Google Scholar 

  5. Calford M (2002) Dynamic representational plasticity in sensory cortex. Neuroscience 111:709–738

    Article  Google Scholar 

  6. Dayan P, Abbott LF (2005) Theoretical neuroscience: computational and mathematical modeling of neural systems. MIT Press, Cambridge

    MATH  Google Scholar 

  7. Feliciano M, Saldaña E, Mugnaini E (1995) Direct projections from the rat primary auditory neocortex to nucleus sagulum, paralemniscal regions, superior olivary complex and cochlear nuclei. Auditory Neurosci 1:287–308

    Google Scholar 

  8. Gaioni S, Riquimaroux HNS (1990) Biosonar behavior of mustached bats swung on a pendulum prior to cortical ablation. J Neurophysiol 64:1801–1817

    Google Scholar 

  9. Gao E, Suga N (1998) Experience-dependent corticofugal adjustment of midbrain frequency map in bat auditory system. Proc Natl Acad Sci U S A 95(21):12663–12670

    Article  Google Scholar 

  10. Gao E, Suga N (2000) Experience-dependent plasticity in the auditory cortex and the inferior colliculus of bats: role of the corticofugal system. Proc Natl Acad Sci U S A 97:8081–8086

    Article  Google Scholar 

  11. Goldman LJ, Henson OW Jr (1977) Prey recognition and selection by the constant frequency bat, pteronotus p. parnellii. Behav Ecol Sociobiol 2:411–419

    Article  Google Scholar 

  12. Guillery R, Sherman S (2002) Thalamic relay functions and their role in corticocortical communication: generalizations from the visual system. Neuron 17:163–175

    Article  Google Scholar 

  13. Guillery RW (1969) The organization of synaptic interconnections in the laminae of the dorsal lateral geniculate nucleus of the cat. Z Zellforsch Mikrosk Anat 96:1–38

    Article  Google Scholar 

  14. Henson OW Jr, Henson MM, Kobler JB, Pollak GD (1980) The constant frequency component of the biosonar signals of the bat pteronotus parnellii parnellii. In: Busnel RG, Fish J (eds) Animal sonar systems. Plenum, New York, pp 913–916

    Chapter  Google Scholar 

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

    Article  Google Scholar 

  16. Izhikevich EM (2003) Simple model of spiking neurons. IEEE Trans Neural Netw 14:1569–1572

    Article  Google Scholar 

  17. Kaas J (1991) Plasticity of sensory and motor maps in adult mammals. Annu Rev Neurosci 14:137–167

    Article  Google Scholar 

  18. Kashimori Y, Inoue S, Kambara T (2001) A neural mechanism of hyperaccurate detection of phase advance and delay in the jamming avoidance response of weakly electric fish. Biol Cybern 85:117–131

    Article  Google Scholar 

  19. Kelly JP, Wong D (1981) Laminar connections of the cat’s auditory cortex. Brain Res 212:1–15

    Article  Google Scholar 

  20. Kisvárday ZF, Beaulieu C, Eysel U (1993) Network of GABAergic large basket cells in cat visual cortex (area 18): implication for lateral disinhibition. J Comp Neurol 327:398–415

    Article  Google Scholar 

  21. Kleinfeld D, Berg RW, O’Connor SM (1999) Anatomical loops and their electrical dynamics in relation to whisking by rat. Somatosens Mot Res 16:69–88

    Article  Google Scholar 

  22. Knudsen E, du Lac S, Esterly S (1987) Computational maps in the brain. Annu Rev Neurosci 10:41–65

    Article  Google Scholar 

  23. Liu BH, Wu GK, Arbuckle R, Tao HW, Zhang LI (2007) Defining cortical frequency tuning with recurrent excitatory circuitry. Nat Neurosci 10:1594–1600

    Article  Google Scholar 

  24. Liu XB, Honda CN, Jones EG (1995) Distribution of four types of synapse on physiologically identified relay neurons in the ventral posterior thalamic nucleus of the cat. J Comp Neurol 352:69–91

    Article  Google Scholar 

  25. Markram H, Toled-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C (2004) Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5:793–807

    Article  Google Scholar 

  26. Nicolelis MAL, Fanselow EE (2002a) Dynamic shifting in thalamocortical processing during different behavioural states. Philos Trans R Soc Lond B Biol Sci 357:1753–1758

    Article  Google Scholar 

  27. Nicolelis MAL, Fanselow EE (2002b) Thalamocortical [correction of thalamcortical] optimization of tactile processing according to behavioral state. Nat Neurosci 5:517–523

    Article  Google Scholar 

  28. Rumelhart D, McClelland J (1986) Parallel distributed processing. MIT Press, Cambridge

    Google Scholar 

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

    Article  Google Scholar 

  30. Schnitzler H (1970) Echoortung bei der fledermacus chilonycteris rubiginosa. Z Verg Physiol 68:25–38

    Article  Google Scholar 

  31. Sherman S, Guillery R (1996) Functional organization of thalamocortical relays. J Neurophysiol 37:1367–1395

    Google Scholar 

  32. Sherman SM, Guillery RW (2002) The role of the thalamus in the flow of information to the cortex. Philos Trans R Soc B 357:1695–1708

    Article  Google Scholar 

  33. Sillito AM, Cudeiro J, Jones HE (2006) Always returning: feedback and sensory processing in visual cortex and thalamus. Trends Neurosci 29:307–316

    Article  Google Scholar 

  34. Steriade M, Timofeev I (2003) Neuronal plasticity in thalamocortical networks during sleep and waking oscillations. Neuron 37:563–576

    Article  Google Scholar 

  35. Suga N (1984) The extent to which biosonar information is represented in the bat auditory cortex. In: Edelman GM, Gall WE, Cowan WM (eds) Dynamic aspects of neocortical function. Wiley, New York, pp 315–373

    Google Scholar 

  36. Suga N (1990) Biosonar and neural computation in bats. Sci Am 262:60–68

    Article  Google Scholar 

  37. Suga N, Ma X (2003) Multiparametric corticofugal modulation and plasticity in the auditory system. Nat Rev Neurosci 4:783–794

    Article  Google Scholar 

  38. Trussell LO (1997) Cellular mechanisms for preservation of timing in central auditory pathways. Curr Opin Neurobiol 7:487–492

    Article  Google Scholar 

  39. Vogels TP, Abbott LF (2009) Gating multiple signals through detailed balance of excitation and inhibition in spiking networks. Nat Neurosci 12:483–491

    Article  Google Scholar 

  40. Xiao Z, Suga N (2002) Reorganization of the cochleotopic map in the bat’s auditory system by inhibition. Proc Natl Acad Sci USA 99(24):15743–15748

    Article  Google Scholar 

  41. Yan J, Suga N (1996) Corticofugal modulation of time-domain processing of biosonar information in bats. Science 273(5278):1100–1103

    Article  Google Scholar 

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

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Tsuyama National College of Technology, 654-1 Numa, Tsuyama, Okayama, 708-8506, Japan

    Kazuhisa Fujita

  2. Department of Engineering Science, University of Electro-Communications, Chofu, Tokyo, 182-8585, Japan

    Kazuhisa Fujita & Yoshiki Kashimori

  3. Graduate School of Information Systems, University of Electro-Communications, Chofu, Tokyo, 182-8585, Japan

    Yoshiki Kashimori

Authors
  1. Kazuhisa Fujita
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yoshiki Kashimori
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kazuhisa Fujita.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fujita, K., Kashimori, Y. Neural Mechanism of Corticofugal Modulation of Tuning Property in Frequency Domain of Bat’s Auditory System. Neural Process Lett 43, 537–551 (2016). https://doi.org/10.1007/s11063-015-9425-6

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11063-015-9425-6

Keywords

Search

Navigation