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To the problem of neuronal firing correlation between neurons located in the auditory pathway (Analitic review)

© 2015 N. G. Bibikov

OAS NN Andreyev Acoustical Institute 117036, Moscow, Shvernik st. 4

Received 21 Aug 2014

The state-of-the-art review of the literature concerning the interaction of the neurons located in close proximity to each other along neuronal auditory pathway is presented. The current data support the independence of the moments of the spike appearance in the auditory nerve fibers, even which are connected with single inner hair cell. Mechanisms to ensure this independence are discussed. There is every reason to believe that the independence of firing is maintained in the ventral cochlear nucleus. The interdependence of temporal patterns of impulses in closely spaced neurons located in inferior colliculus yet explores insufficiently. However, there are some reasons to believe that in the central nucleus of the inferior colliculus that independence is still present. In the structures surrounding the central nucleus, those usually doesn’t included in the direct auditory pathway, the interdependence of neighboring neurons impulsation becomes quite pronounced. In the medial geniculate body the weakest functional interneuronal connection corresponds to the ventral part of the nucleus which is the part of direct auditory pathway. Finally, for the primary sensory cortical projection zones differences in the degree of interdependence of impulses of neurons in layers of the cortex have been observed. The most independent firing takes place in cells which receiving the signals directly from the thalamic sensory nuclei. These data suggest that in the direct auditory pathway all temporal information is effectively used with the minimum of redundancy. This allows the most detailed analysis of the time course of the sound signals in a wide range of frequencies and intensities. In brain regions associated with the synthesis and classification of complex auditory signals, the correlation between neurons becomes more pronounced.

Key words: correlation, spontaneous activity, single neurons, the auditory pathway, independence, analysis of auditory images

Cite: Bibikov N. G. K voprosu o vzaimnoi korrelyatsii impulsnoi aktivnosti neironov slukhovogo puti (analiticheskii obzor) [To the problem of neuronal firing correlation between neurons located in the auditory pathway (analitic review)]. Sensornye sistemy [Sensory systems]. 2015. V. 29(1). P. 3-14 (in Russian).

References:

  • Бибиков Н.Г., Дымов А.Б. Факторы Фано и Аллана процесса спонтанной импульсной активности слуховых нейронов продолговатого мозга // Сенсорные системы. 2009. Т. 23. No 3. С. 246–259.
  • Бибиков Н.Г., Иваницкий Г.А. Моделирование спонтанной импульсации и кратковременной адаптации в волокнах слухового нерва // Биофизика. 1985. Т. 30. No 1. С. 141–144.
  • Богданов А.В., Галашина А.Г. Анализ сопряженной импульсации пар нейронов в микроструктурах коры мозга // Российск. физиол. журн. 2000. Т. 86. С. 497–506.
  • Гасанов У.Г., Галашина А.Г. Анализ межнейронных связей в слуховой коре бодрствующих кошек// Журн. высш. нерв. деятельности. 1975. Т. 25. No 5. С. 1053–1060.
  • Дубровский Н.А. Эхолокационный анализатор дельфина афалины // Акустический журнал. 2004. Т. 50. No 3. С. 369–378.
  • Серков Ф.Н., Яновский Е.Ш., Тальнов А.Н. О моносинаптических тормозящих постсинаптических потенциалах нейронов коры больших полушарий // Нейрофизиология. 1975. Т. 7. No 5. С. 458–467.
  • Силкис И.Г. О функциональной организации моносинаптических межнейронных связей в коре больших полушарий // Журн. высш. нерв. деятельности. 1978. Т. 28. No 3. С. 643–649.
  • Яновский Е.Ш., Киенко В.М. Межнейронные взаимодействия в слуховой коре бодрствующих кошек// Нейрофизиология. 1984. Т.16. No 2. С. 161–167.
  • Abbott L.F., Dayan P. The effect of correlated variability on the accuracy of a population code // Neural computation. 1999. V. 11. No 1. P. 91–101.
  • Akemann W., Mutoh H., Perron A., Rossier J., Knöpfel T. Imaging brain electric signals with genetically targeted voltage sensitive fluorescent proteins //Nature methods. 2010. V. 7. No. 8. P. 643–649.
  • Ahn J.,Kreeger L.J.,Lubejko S.T.,Butts D.A.,MacLeod K.M. Heterogeneity of intrinsic biophysical properties among cochlear nucleus neurons improves the population coding of temporal information // J. Neurophysiol. 2014. V. 111. No 11. P. 2320–2331.
  • Atencio C.A., Schreiner C.E. Auditory cortical local subnetworks are characterized by sharply synchronous activity // J. Neuroscience. 2013. V. 33. No 47. P. 18503– 18514.
  • Averbeck B.B., Latham P.E., Pouget A. Neural correlations, population coding and computation // Nat. Rev. Neurosci. 2006. V. 7. No 5. P. 358–366.
  • Averbeck B.B., Lee D. Effects of noise correlations on information encoding and decoding // J. Neurophysiol. 2006. V. 95. No 6. P. 3633–3644.
  • Bibikov N.G., Dubrovsky N.A., Ivanitsky G.A., RimskayaKorsakova L.K., Telepnev V.N. A model for filtering and analog to pulse conversion on the periphery of auditory pathway // Proc. XI th Intern. Cong. Phonetic Sciences. Tallinn. 1987. V. 3. Р. 67–70.
  • Brosch M., Schreiner C.E. Correlations between neural discharges are related to receptive field properties in cat primary auditory cortex // Europ. J. Neurosci. 1999. V. 11. No 10. P. 3517–3530.
  • Cohen M.R., Kohn A. Measuring and interpreting neuronal correlations // Nature Neuroscience. 2011. V. 14. No 7. P. 811–819.
  • Davis K.A., Voigt H.F. Evidence of stimulus dependent correlated activity in the dorsal cochlear nucleus of decerebrate gerbils // J. Neurophysiol. 1997. V. 78. No 1. P. 229–247.
  • Dean I., Robinson B.L., Harper N.S., McAlpine D. Rapid neural adaptation to sound level statistics // J. Neuroscience. 2008. V. 28. No 25. P. 6430–6438.
  • Ecker A.S., Berens P., Keliris G.A., Bethge M., Logothetis N.K., Tolias A.S. Decorrelated neuronal firing in cortical microcircuits // Science. 2010. V. 327. No 5965. P. 584–587.
  • Eggermont J.J. Neuronal pair and triplet interactions in the auditory midbrain of the leopard frog // J. Neurophysiol. 1991. V. 66. P. 1549–1563.
  • Eggermont J.J. Neural interaction in cat primary auditory cortex. II. Effects of sound stimulation // J. Neurophysiol. 1994. V. 71. P. 246–270.
  • Eggermont J.J. Properties of correlated neural activity clusters in cat auditory cortex resemble those of neural assemblies // J. Neurophysiol. 2006. V. 96. No 2. P. 746–764.
  • Eggermont J.J., Smith G.M. Neural connectivity only accounts for a small part of neural correlation in auditory cortex // Exp. Brain Res. 1996. V. 110. No 3. P. 379– 391.
  • Erchova I.A., Lebedev M.A., Diamond M.E. Somatosensory cortical neuronal population activity across states of anaesthesia // Europ. J. Neurosci. 2002. V. 15. No 4. P. 744–752.
  • Espinosa I.E., Gerstein G.L. Cortical auditory neuron interactions during presentation of 3 tone sequences: effective connectivity // Brain Res. 1988. V. 450. No 1. P. 39–50.
  • Garcia-Lazaro J.A., Belliveau L.A.C., Lesica N.A. Independent population coding of speech with sub millisecond precision // J. Neuroscience. 2013. V. 33. No 49. P. 19362–19372.
  • Geis H.R.A.P., van der Heijden M., Borst J.G.G. Subcortical input heterogeneity in the mouse inferior colliculus // J. Physiology (L). 2011. V. 589. No 16. P. 3955– 3967.
  • Glowatzki E., Fuchs P.A. Transmitter release at the hair cell ribbon synapse //Nature Neuroscience. 2002. V. 5. No 2. P. 147–154.
  • Graupner M., Reyes A.D. Synaptic input correlations leading to membrane potential decorrelation of spontaneous activity in cortex //J. Neuroscience. 2013. V. 33. No 38. P. 15075–15085.
  • Hansen B.J., Chelaru M.I., Dragoi V. Correlated variability in laminar cortical circuits // Neuron. 2012. V. 76. No 3. P. 590–602.
  • Heierli P., De Ribaupierre F., De Ribaupierre Y. Functional properties and interactions of neuron pairs simultaneously recorded in the medial geniculate body of the cat // Hear. Res. 1987. V. 25. No 2. P. 209–225.
  • Johnson D.H., Kiang N.Y. Analysis of discharges recorded simultaneously from pairs of auditory nerve fibers // Biophysical Journal. 1976. V. 16. No 7. P. 719–734.
  • Joris P.X., Carney L.H., Smith P. H., Yin T.C. Enhancement of neural synchronization in the anteroventral cochlear nucleus I. Responses to tones at the characteristic frequency // J. Neurophysiol. 1994. V. 71. P. 1022–1032.
  • Kiang N.Y. Curious oddments of auditory nerve studies // Hear. Res. 1990. V. 49. No 1. P. 1–16.
  • Kvašňák E., Suta D., Popelár J., Syka J. Neuronal connections in the medial geniculate body of the guinea pig // Exp. Brain Res. 2000. V. 132. No 1. P. 87–102.
  • Lowen S.B., Ozaki T., Kaplan E., Saleh B. E., Teich M. C.
  • Fractal features of dark, maintained, and driven neural discharges in the cat visual system // Methods. 2001. V. 24. No 4. P. 377–394.
  • Martin K.A.C., Schröder S. Functional heterogeneity in neighboring neurons of cat primary visual cortex in response to both artificial and natural stimuli // J. Neuroscience. 2013. V. 33. No 17. P. 7325–7344.
  • Merchan-Perez A., Liberman M.C. Ultrastructural differences among afferent synapses on cochlear hair cells: correlations with spontaneous discharge rate // J. Comp. Neurology. 1996. V. 371. No 2. P. 208–221.
  • Nirenberg S., Latham P.E. Decoding neuronal spike trains: How important are correlations? // Proc.Nat. Acad. Sci. 2003. V. 100. No 12. P. 7348–7353.
  • Okun M., Lampl I. Instantaneous correlation of excitation and inhibition during ongoing and sensory evoked activities // Nature Neuroscience. 2008. V. 11. No 5. P. 535–537.
  • Ostojic S., Brunel N., Hakim V. How connectivity, background activity, and synaptic properties shape the cross correlation between spike trains //J. Neuroscience. 2009. V. 29. No 33. P. 10234–10253.
  • Palmer A.R., Russell I.J. Phase locking in the cochlear nerve of the guinea pig and its relation to the receptor potential of inner hair cells // Hear. Res. 1986. V. 24. No 1. P. 1–15.
  • Shivdasani M.N., Mauger S.J., Rathbone G.D., Paolini A.G. Neural synchrony in ventral cochlear nucleus neuron populations is not mediated by intrinsic processes but is stimulus induced: implications for auditory brainstem implants // J. Neural Engineering. 2009. V. 6. No 6. P. 65–68.
  • Siegel J.H. Spontaneous synaptic potentials from afferent terminals in the guinea pig cochlea // Hear. Res. 1992. V. 59. No 1. P. 85–92.
  • Smith M.A., Kohn A. Spatial and temporal scales of neuronal correlation in primary visual cortex //J. Neuroscience. 2008. V. 28. No 48. P. 12591–12603.
  • Syka J., Radionova E.A., Popelář J. Discharge characteristics of neuronal pairs in the rabbit inferior colliculus // Exp. Brain Res. 1981. V. 44. No 1. P. 11–18.
  • Tomita M., Eggermont J.J. Cross correlation and joint spectro-temporal receptive field properties in auditory cortex // J. Neurophysiol. 2005. V. 93. No 1. P. 378– 392.
  • Voigt H.F., Young E.D. Stimulus dependent neural correlation: an example from the cochlear nucleus //Exp. Brain Res. 1985. V. 60. No 3. P. 594–598.
  • Voigt H.F., Young E.D. Neural correlations in the dorsal cochlear nucleus: pairs of units with similar response properties // J. Neurophysiol. 1988. V. 59. P. 1014– 1032.
  • Voigt H.F., Young E.D. Cross correlation analysis of inhibitory interactions in dorsal cochlear nucleus // J. Neurophysiol. 1990. V. 64. P. 1590–1610.
  • Wen B., Wang G.I., Dean I., Delgutte B. Dynamic range adaptation to sound level statistics in the auditory nerve // J. Neuroscience. 2009. V. 29. No 44. P. 13797– 13808.
  • Wever E.G., Bray C.W. Present possibilities for auditory theory // Psychological Review. 1930. V. 37. No 5. P. 365–380.