The time parameters of the spike activity of single neurons in the brainstem part of the auditory system carry basic information on the properties of perceived signals. To characterize these parameters, the activity of single neurons in the midbrain center (semicircular torus) of the common frog (Rana temporaria) was studied on exposure to prolonged tones amplitude-modulated with repeating bursts of low-frequency noise. Time-shuffled autocorrelation functions were calculated, these corresponding to the sum of the correlation functions between responses to all bursts presented with the exception of responses evoked by one of the bursts. This approach excludes the effects of the refractory properties of the neuron being studied, allowing the responses of a single neuron to be used to evaluate the nature of the spike activity in the local population of cells with presumptively identical properties but which are statistically independent of each other. Significant variation in the statistical characteristics of output spike activity in different cells in the semicircular toroid was found, such that signals could be characterized in terms of different time properties. Neurons with highly specific reactions to the time characteristics of the envelope were observed.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Avissar, M., Wittig, J. H., Saunders, J. C., and Parsons, T. D., “Refractoriness enhances temporal coding by auditory nerve fibers,” J. Neurosci., 33, No. 18, 7681–7690 (2013).
Bibikov, N. G. and Ivanitskii, G. A., “Modeling of spontaneous spike activity and short-term adaptation in fibers of the auditory nerve,” Biofizika, 30, 141–144 (1985).
Bibikov, N. G. and Nizamov, S. V., “Analysis of the activity of auditory neurons in the frog medulla oblongata on exposure to tones modulated by low-frequency noise,” Biofizika, 54, No. 5, 921–934 (2009).
Bibikov, N. G., “Correlation of cochlear nucleus neuronal reactions with low-frequency amplitude modujlation of a tonal signal,” Akustich. Zh., 60, No. 5, 555–566 (2014a).
Bibikov, N. G., “Encoding of the stimulus envelope in peripheral and central regions of the auditory system of the frog,” Acustica, 31, 310–314 (1974).
Bibikov, N. G., “Envelope characteristics of sound signals extracted by neurons in the autitory center of the frog medulla oblongata,” Biofizika, 60, No. 3, 409–419 (2014b).
Bibikov, N. G., “Extraction of some of the characteristics of low-frequency tonal signal envelopes by neurons in the auditory center of the frog midbrain,” Sens. Sistemy, 30, 201–214 (2016).
Bibikov, N. G., “Mixed autocorrelation function for neuron spike activity,” in: Proc. 14th All-Russ. Conf. Neuroinformatics-2012, MIFI-Press (2012), p. 84–91.
Bibikov, N. G., “On the mutual correlation between the spike activity of neurons in the auditory pathway (an analytical review),” Sens. Sistemy, 29, No. 1, 3–12 (2015).
Bibikov, N. G., “Quantitative assessment of changes in the synchronization of frog cochlear nucleus neuron reactions with the envelope of a sound signal during long-term adaptation,” Akustich. Zh., 54, No. 4, 669–681 (2008).
Bibikov, N. G., “Relationship between the variability of the responses of neurons in the frog semicircular torus and acoustic stimulus parameters,” Neirofiziol. (Kiev), 46, No. 1, 18–27 (2014c).
Bibikov, N. G., “Separate assessment of the effects of conditioning signal and a neuronal spike on the responses of individual neurons in the auditory system,” Sens. Sistemy, 3, No. 3, 364–369 (1990).
Bibikov, N. G., Ovchinnikov, O. B., and Nizamov, S. V., “Assessment decreases in excitability after spike generation for central auditory neurons in the frog,” Biofizika, 46, No. 3, 545–554 (2001).
Brette, R., “Philosophy of the spike: rate-based vs. spike based theories of the brain,” Front. Syst. Neuroscience, https://doi.org/10.3389/fn-sys.2015.00151 (2015).
Chen, C., Read, H. L., and Escabi, M. A., “Precise feature based time scales and frequency decorrelation lead to a sparse auditory code,” J. Neurosci., 32, No. 25, 8454–8468 (2012).
Deger, M., Helias, M., Boucsein, C., and Rotter, S., “Statistical properties of superimposed stationary spike trains,” J. Comput. Neurosci., 32, 443–463 (2012).
Garcia-Lazaro, J. A., Belliveau, L. A., and Lesica, N. A., “Independent population coding of speech with sub-millisecond precision,” J. Neurosci., 33, No. 49, 19,362–19,372 (2013).
Gaumond, R. P., Kim, D. O., and Molnar, C. E., “Response of cochlear nerve fibers to brief acoustic stimuli: role of discharge-history effects,” J. Acoust. Soc. Am., 74, 1392–1398 (1983).
Goldberg, J. M. and Brown, P. B., “Responses of binaural neurons superior olivary complex dichotic tonal stimuli: some physiological mechanisms of sound localization,” J. Neurophysiol., 32, 603–536 (1969).
Heijden van der, M., Louage, D. H., and Joris, P. X., “Responses of auditory nerve and anteroventral cochlear nucleus fibers to broadband and narrowband noise: implications for the sensitivity to interaural delays,” J. Assoc. Res. Otolaryngol., 12, 485–502 (2011).
Heinz, M. G. and Swaminathan, J., “Quantifying envelope and fine-structure coding in auditory nerve responses to chimaeric speech,” J. Assoc. Res. Otolaryngol., 10, 407–423 (2009).
Joris, P. X., Louage, D. H., Cardoen L, and Heijden M., “, Correlation index: a new metric to quantify temporal coding,” Hear. Res., 216–217, 19–30 (2006).
Joris, P. X., van de Sande, B., and van der Heijden, M., “Temporal damping in response to broadband noise. I. Inferior colliculus,” J. Neurophysiol., 93, 1857–1870 (2005).
Kale, S., Micheyl, L., and Heinz, M. G., “Implications of within-fiber temporal coding for perceptual studies of f0 discrimination and discrimination of harmonic and inharmonic tone complexes,” J. Assoc. Res. Otolaryngol., 15, 465–482 (2014).
Kaplan, H. M., “Anesthesia in amphibian and reptiles,” Proc. Fed. Am. Soc. Exp. Biol., 28, 1541–1546 (1969).
Kim, D. O., Sirianni, J. G., and Chang, S. O., “Responses of DCN-PVCN neurons and auditory nerve fibers in unanesthetized cats to AM and pure tones: analysis with autocorrelation/power-spectrum,” Hear. Res., 45, 95–113 (1990).
Louage, D. H., van der Heijden, M., and Joris, P. X., “Enhanced temporal response properties of anteroventral cochlear nucleus neurons to broadband noise,” J. Neurosci., 25, 1560–1570 (2005).
Louage, D. H., van der Heijden, M., and Joris, P. X., “Temporal properties of responses to broadband noise in the auditory nerve,” J. Neurophysiol., 91, 2051–2065 (2004).
Shackleton, T. M., Lui, L. F., and Palmer, A. R., “Responses to diotic, dichotic, and alternating phase harmonic stimuli in the inferior colliculus of guinea pigs,” J. Assoc. Res. Otolaryngol., 10, 76–90 (2008).
Shivdasani, M. N., Mauger, S. J., Rathbone, G. D., and Paolini, A. G., “Neu ral synchrony in ventral cochlear nucleus neuron populations is not mediated by intrinsic processes but is stimulus induced: implications for auditory brainstem implants,” J. Neural Eng., 065003 (2009), doi https://doi.org/10.1088/1741-2560/6/6/065003 (2009).
Spirou, G. A., Brownell, W. E., and Zidanic, M., “Recordings from cat trapezoid body and HRP labeling of globular bushy cell axons,” J. Neurophysiol., 63, 1169–1190 (1990).
Steinberg, L. J. and Pena, J. L., “Difference in response reliability predicted by spectrotemporal tuning in the cochlear nuclei of barn owls,” J. Neurosci., 31, No. 9, 3234–3242 (2011).
Street, S. E. and Manis, P. B., “Action potential timing precision in dorsal cochlear nucleus pyramidal cells,” J. Neurophysiol., 97, No. 6, 4162–4172 (2007).
Suckow, M. A., Terril, L. A., Grigdesby, C. F., and March, P. A., “Evaluation of hypothermia-induced analgesia and influence of opioid antagonists in leopard frogs (Rana pipiens),” Pharmacol. Biochem. Behav., 63, 39–43 (1999).
Truccolo, W., Hochberg, L. R., and Donoghue, J. P., “Collective dynamics in human and monkey sensorimotor cortex: predicting single neuron spikes nature,” Nat. Neurosci., 13, No. 1, 105–111 (2012).
Wu, J. S., Young, E. D., and Glowatzki, E., “Maturation of spontaneous firing properties after hearing onset in rat auditory nerve fibers: spontaneous rates, refractoriness, and interfiber correlations,” J. Neurosci., 36, No. 41, 10,584–10,597 (2016).
Yang, S., Lin, W., and Feng, A. S., “Wide-ranging frequency preferences of auditory midbrain neurons: Roles of membrane time constant and synaptic properties,” Eur. J. Neurosci., 30, No. 1, 76–90 (2009).
Yang, S., Yang, S., Cox, C. L., et al., “Cell’s intrinsic biophysical properties play a role in the systematic decrease in time-locking ability of central auditory neurons,” Neuroscience, 208, No. 1, 49–57 (2012).
Yuste, R., “From the neuron doctrine to neural networks,” Nature Rev. Neurosci., 16, No. 8, 487–497 (2015).
Zimmermann, M., “Ethical principles for maintenance and use of animals in neuroscience research,” Neurosci. Lett., 73, 1 (1987).
Author information
Authors and Affiliations
Corresponding author
Additional information
Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 67, No. 2, pp. 217–230, March–April, 2017.
Rights and permissions
About this article
Cite this article
Bibikov, N.G., Nizamov, S.V. Statistical Characteristics of the Spike Activity of Neurons in the Midbrain Auditory Center in Frogs on Exposure to Tones Modulated by Low-Frequency Noise. Neurosci Behav Physi 48, 764–773 (2018). https://doi.org/10.1007/s11055-018-0628-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11055-018-0628-y