Throughout life, sensory systems adapt to the sensory environment to provide optimal responses to relevant tasks. In the case of a developing system, sensory inputs induce changes that are permanent and detectable up to adulthood. Previously, we have shown that rearing rat pups in a complex acoustic environment (spectrally and temporally modulated sound) from postnatal day 14 (P14) to P28 permanently improves the response characteristics of neurons in the inferior colliculus and auditory cortex, influencing tonotopical arrangement, response thresholds and strength, and frequency selectivity, along with stochasticity and the reproducibility of neuronal spiking patterns. In this study, we used a set of behavioral tests based on a recording of the acoustic startle response (ASR) and its prepulse inhibition (PPI), with the aim to extend the evidence of the persistent beneficial effects of the developmental acoustical enrichment. The enriched animals were generally not more sensitive to startling sounds, and also, their PPI of ASR, induced by noise or pure tone pulses, was comparable to the controls. They did, however, exhibit a more pronounced PPI when the prepulse stimulus was represented either by a change in the frequency of a background tone or by a silent gap in background noise. The differences in the PPI of ASR between the enriched and control animals were significant at lower (55 dB SPL), but not at higher (65-75 dB SPL), intensities of background sound. Thus, rearing pups in the acoustically enriched environment led to an improvement of the frequency resolution and gap detection ability under more difficult testing conditions, i.e., with a worsened stimulus clarity. We confirmed, using behavioral tests, that an acoustically enriched environment during the critical period of development influences the frequency and temporal processing in the auditory system, and these changes persist until adulthood.

Department of Auditory Neuroscience Institute of Experimental Medicine Czech Academy of Sciences Prague Czech Republic

Department of Cognitive Systems and Neurosciences Czech Institute of Informatics Robotics and Cybernetics Czech Technical University Prague Czech Republic

Department of Medical Biophysics and Medical Informatics 3rd Faculty of Medicine Charles University Prague Czech Republic

Department of Technical Studies College of Polytechnics Jihlava Czech Republic

See more in PubMed

Zhang L., Bao S., Merzenich M. Persistent and specific influences of early acoustic environments on primary auditory cortex. Nature Neuroscience. 2001;4(11):1123–1130. doi: 10.1038/nn745. PubMed DOI

de Villers-Sidani E., Chang E., Bao S., Merzenich M. Critical period window for spectral tuning defined in the primary auditory cortex (A1) in the rat. Journal of Neuroscience. 2007;27(1):180–189. doi: 10.1523/jneurosci.3227-06.2007. PubMed DOI PMC

Chang E., Bao S., Imaizumi K., Schreiner C., Merzenich M. Development of spectral and temporal response selectivity in the auditory cortex. Proceedings of the National Academy of Sciences. 2005;102(45):16460–16465. doi: 10.1073/pnas.0508239102. PubMed DOI PMC

Bures Z., Grecova J., Popelar J., Syka J. Noise exposure during early development impairs the processing of sound intensity in adult rats. European Journal of Neuroscience. 2010;32(1):155–164. doi: 10.1111/j.1460-9568.2010.07280.x. PubMed DOI

Chang E., Merzenich M. Environmental noise retards auditory cortical development. Science. 2003;300(5618):498–502. doi: 10.1126/science.1082163. PubMed DOI

Kral A., Hartmann R., Tillein J., Heid S., Klinke R. Delayed maturation and sensitive periods in the auditory cortex. Audiology and Neuro-Otology. 2001;6(6):346–362. doi: 10.1159/000046845. PubMed DOI

Grecova J., Bures Z., Popelar J., Suta D., Syka J. Brief exposure of juvenile rats to noise impairs the development of the response properties of inferior colliculus neurons. European Journal of Neuroscience. 2009;29(9):1921–1930. doi: 10.1111/j.1460-9568.2009.06739.x. PubMed DOI

Zhang L., Bao S., Merzenich M. Disruption of primary auditory cortex by synchronous auditory inputs during a critical period. Proceedings of the National Academy of Sciences. 2002;99(4):2309–2314. doi: 10.1073/pnas.261707398. PubMed DOI PMC

Bures Z., Bartosova J., Lindovsky J., Chumak T., Popelar J., Syka J. Acoustical enrichment during early postnatal development changes response properties of inferior colliculus neurons in rats. European Journal of Neuroscience. 2014;40(11):3674–3683. doi: 10.1111/ejn.12732. PubMed DOI

Engineer N., Percaccio C., Pandya P., Moucha R., Rathbun D., Kilgard M. Environmental enrichment improves response strength, threshold, selectivity, and latency of auditory cortex neurons. Journal of Neurophysiology. 2004;92(1):73–82. doi: 10.1152/jn.00059.2004. PubMed DOI

Percaccio C., Engineer N., Pruette A., et al. Environmental enrichment increases paired-pulse depression in rat auditory cortex. Journal of Neurophysiology. 2005;94(5):3590–3600. doi: 10.1152/jn.00433.2005. PubMed DOI

Percaccio C., Pruette A., Mistry S., Chen Y., Kilgard M. Sensory experience determines enrichment-induced plasticity in rat auditory cortex. Brain Research. 2007;1174:76–91. doi: 10.1016/j.brainres.2007.07.062. PubMed DOI

Homma N. Y., Hullett P. W., Atencio C. A., Schreiner C. E. Auditory cortical plasticity dependent on environmental noise statistics. Cell Reports. 2020;30(13):4445–4458.e5. doi: 10.1016/j.celrep.2020.03.014. PubMed DOI PMC

Svobodová Burianová J., Syka J. Postnatal exposure to an acoustically enriched environment alters the morphology of neurons in the adult rat auditory system. Brain Structure & Function. 2020;225(7):1979–1995. doi: 10.1007/s00429-020-02104-8. PubMed DOI

Cai R., Guo F., Zhang J., Xu J., Cui Y., Sun X. Environmental enrichment improves behavioral performance and auditory spatial representation of primary auditory cortical neurons in rat. Neurobiology of Learning and Memory. 2009;91(4):366–376. doi: 10.1016/j.nlm.2009.01.005. PubMed DOI

Zhu X., Wang F., Hu H., et al. Environmental acoustic enrichment promotes recovery from developmentally degraded auditory cortical processing. Journal of Neuroscience. 2014;34(16):5406–5415. doi: 10.1523/jneurosci.5310-13.2014. PubMed DOI PMC

Xu J., Yu L., Cai R., Zhang J., Sun X. Early auditory enrichment with music enhances auditory discrimination learning and alters NR2B protein expression in rat auditory cortex. Behavioural Brain Research. 2009;196(1):49–54. doi: 10.1016/j.bbr.2008.07.018. PubMed DOI

Ranasinghe K. G., Carraway R. S., Borland M. S., et al. Speech discrimination after early exposure to pulsed-noise or speech. Hearing Research. 2012;289(1-2):1–12. doi: 10.1016/j.heares.2012.04.020. PubMed DOI PMC

Pysanenko K., Bures Z., Lindovsky J., Syka J. The effect of complex acoustic environment during early development on the responses of auditory cortex neurons in rats. Neuroscience. 2018;371:221–228. doi: 10.1016/j.neuroscience.2017.11.049. PubMed DOI

Bures Z., Pysanenko K., Lindovsky J., Syka J. Acoustical enrichment during early development improves response reliability in the adult auditory cortex of the rat. Neural Plasticity. 2018;2018:11. doi: 10.1155/2018/5903720.5903720 PubMed DOI PMC

Fitch R. H., Threlkeld S. W., McClure M. M., Peiffer A. M. Use of a modified prepulse inhibition paradigm to assess complex auditory discrimination in rodents. Brain Research Bulletin. 2008;76(1-2):1–7. doi: 10.1016/j.brainresbull.2007.07.013. PubMed DOI PMC

Weible A. P., Moore A. K., Liu C., et al. Perceptual gap detection is mediated by gap termination responses in auditory cortex. Current Biology. 2014;24(13):1447–1455. doi: 10.1016/j.cub.2014.05.031. PubMed DOI PMC

Keller C. H., Kaylegian K., Wehr M. Gap encoding by parvalbumin-expressing interneurons in auditory cortex. Journal of Neurophysiology. 2018;120(1):105–114. doi: 10.1152/jn.00911.2017. PubMed DOI PMC

Ison J. R. Temporal acuity in auditory function in the rat: reflex inhibition by brief gaps in noise. Journal of Comparative and Physiological Psychology. 1982;96(6):945–954. doi: 10.1037/0735-7036.96.6.945. PubMed DOI

Šuta D., Rybalko N., Shen D., Popelář J., Poon P., Syka J. Frequency discrimination in rats exposed to noise as juveniles. Physiology & Behavior. 2015;144:60–65. doi: 10.1016/j.physbeh.2015.03.005. PubMed DOI

Clause A., Nguyen T., Kandler K. An acoustic startle-based method of assessing frequency discrimination in mice. Journal of Neuroscience Methods. 2011;200(1):63–67. doi: 10.1016/j.jneumeth.2011.05.027. PubMed DOI PMC

Basavaraj S., Yan J. Prepulse inhibition of acoustic startle reflex as a function of the frequency difference between prepulse and background sounds in mice. PLoS ONE. 2012;7(9, article e45123) doi: 10.1371/journal.pone.0045123. PubMed DOI PMC

Rybalko N., Chumak T., Bures Z., Popelar J., Suta D., Syka J. Development of the acoustic startle response in rats and its change after early acoustic trauma. Behavioural Brain Research. 2015;286:212–221. doi: 10.1016/j.bbr.2015.02.046. PubMed DOI

Rybalko N., Bures Z., Burianova J., Popelar J., Grecova J., Syka J. Noise exposure during early development influences the acoustic startle reflex in adult rats. Physiology & Behavior. 2011;102(5):453–458. doi: 10.1016/j.physbeh.2010.12.010. PubMed DOI

Rybalko N., Mitrovic D., Šuta D., Bureš Z., Popelář J., Syka J. Behavioral evaluation of auditory function abnormalities in adult rats with normal hearing thresholds that were exposed to noise during early development. Physiology & Behavior. 2019;210, article 112620 doi: 10.1016/j.physbeh.2019.112620. PubMed DOI

Zhou X., Merzenich M. M. Enduring effects of early structured noise exposure on temporal modulation in the primary auditory cortex. Proceedings of the National Academy of Sciences. 2008;105(11):4423–4428. doi: 10.1073/pnas.0800009105. PubMed DOI PMC

Zhou X., Merzenich M. M. Developmentally degraded cortical temporal processing restored by training. Nature Neuroscience. 2009;12(1):26–28. doi: 10.1038/nn.2239. PubMed DOI PMC

Han Y. K., Kover H., Insanally M. N., Semerdjian J. H., Bao S. Early experience impairs perceptual discrimination. Nature Neuroscience. 2007;10(9):1191–1197. doi: 10.1038/nn1941. PubMed DOI

Oliver D. L., Izquierdo M. A., Malmierca M. S. Persistent effects of early augmented acoustic environment on the auditory brainstem. Neuroscience. 2011;184:75–87. doi: 10.1016/j.neuroscience.2011.04.001. PubMed DOI PMC

Poon P. W., Chen X. Postnatal exposure to tones alters the tuning characteristics of inferior collicular neurons in the rat. Brain Research. 1992;585(1-2):391–394. doi: 10.1016/0006-8993(92)91243-8. PubMed DOI

Insanally M. N., Kover H., Kim H., Bao S. Feature-dependent sensitive periods in the development of complex sound representation. Journal of Neuroscience. 2009;29(17):5456–5462. doi: 10.1523/jneurosci.5311-08.2009. PubMed DOI PMC

Poon P. W., Chen X. Y., Hwang J. C. Altered sensitivities of auditory neurons in the rat midbrain following early postnatal exposure to patterned sounds. Brain Research. 1990;524(2):327–330. doi: 10.1016/0006-8993(90)90710-s. PubMed DOI

Zhou X., Merzenich M. Environmental noise exposure degrades normal listening processes. Nature Communications. 2012;3(1) doi: 10.1038/ncomms1849. PubMed DOI

Zheng W. Auditory map reorganization and pitch discrimination in adult rats chronically exposed to low-level ambient noise. Frontiers in Systems Neuroscience. 2012;6(65) doi: 10.3389/fnsys.2012.00065. PubMed DOI PMC

Yeomans J. S., Frankland P. W. The acoustic startle reflex: neurons and connections. Brain Research Reviews. 1995;21(3):301–314. doi: 10.1016/0165-0173(96)00004-5. PubMed DOI

Gómez-Nieto R., Horta-Júnior J. A. C., Castellano O., Sinex D. G., López D. E. The Neurophysiological Bases of Auditory Perception. New York, NY: Springer New York; 2010. Auditory prepulse inhibition of neuronal activity in the rat cochlear root nucleus; pp. 79–90.

Davis M. The mammalian startle response. In: Eaton R. C., editor. Neural Mechanisms of Startle Behavior. Boston, MA: Springer US; 1984. pp. 287–351.

Lee Y., Lopez D. E., Meloni E. G., Davis M. A primary acoustic startle pathway: obligatory role of cochlear root neurons and the nucleus reticularis pontis caudalis. Journal of Neuroscience. 1996;16(11):3775–3789. doi: 10.1523/JNEUROSCI.16-11-03775.1996. PubMed DOI PMC

Koch M. The neurobiology of startle. Progress in Neurobiology. 1999;59(2):107–128. doi: 10.1016/s0301-0082(98)00098-7. PubMed DOI

Swerdlow N. R., Geyer M. A., Braff D. L. Neural circuit regulation of prepulse inhibition of startle in the rat: current knowledge and future challenges. Psychopharmacology. 2001;156(2-3):194–215. doi: 10.1007/s002130100799. PubMed DOI

Fendt M., Li L., Yeomans J. S. Brain stem circuits mediating prepulse inhibition of the startle reflex. Psychopharmacology. 2001;156(2-3):216–224. doi: 10.1007/s002130100794. PubMed DOI

Yeomans J. S., Lee J., Yeomans M. H., Steidl S., Li L. Midbrain pathways for prepulse inhibition and startle activation in rat. Neuroscience. 2006;142(4):921–929. doi: 10.1016/j.neuroscience.2006.06.025. PubMed DOI

Moreno-Paublete R., Canlon B., Cederroth C. R. Differential neural responses underlying the inhibition of the startle response by pre-pulses or gaps in mice. Frontiers in Cellular Neuroscience. 2017;11:p. 19. doi: 10.3389/fncel.2017.00019. PubMed DOI PMC

Friedman J. T., Peiffer A. M., Clark M. G., Benasich A. A., Fitch R. H. Age and experience-related improvements in gap detection in the rat. Developmental Brain Research. 2004;152(2):83–91. doi: 10.1016/j.devbrainres.2004.06.007. PubMed DOI

Swetter B. J., Fitch R. H., Markus E. J. Age-related decline in auditory plasticity: experience dependent changes in gap detection as measured by prepulse inhibition in young and aged rats. Behavioral Neuroscience. 2010;124(3):370–380. doi: 10.1037/a0019519. PubMed DOI

Turner J. G., Brozoski T. J., Bauer C. A., et al. Gap detection deficits in rats with tinnitus: a potential novel screening tool. Behavioral Neuroscience. 2006;120(1):188–195. doi: 10.1037/0735-7044.120.1.188. PubMed DOI

Shinn J. B., Chermak G. D., Musiek F. E. GIN (gaps-in-noise) performance in the pediatric population. Journal of the American Academy of Audiology. 2009;20(4):229–238. doi: 10.3766/jaaa.20.4.3. PubMed DOI

John A. B., Hall J. W., 3rd, Kreisman B. M. Effects of advancing age and hearing loss on gaps-in-noise test performance. American Journal of Audiology. 2012;21(2):242–250. doi: 10.1044/1059-0889(2012/11-0023). PubMed DOI

Fitzgibbons P. J., Gordon-Salant S. Auditory temporal processing in elderly listeners. Journal-American Academy of Audiology. 1996;7(3):183–189. PubMed

Schneider B. A., Pichora-Fuller M. K., Kowalchuk D., Lamb M. Gap detection and the precedence effect in young and old adults. The Journal of the Acoustical Society of America. 1994;95(2):980–991. doi: 10.1121/1.408403. PubMed DOI

Snell K. B., Frisina D. R. Relationships among age-related differences in gap detection and word recognition. The Journal of the Acoustical Society of America. 2000;107(3):1615–1626. doi: 10.1121/1.428446. PubMed DOI

Syka J., Rybalko N., Mazelova J., Druga R. Gap detection threshold in the rat before and after auditory cortex ablation. Hearing Research. 2002;172(1-2):151–159. doi: 10.1016/S0378-5955(02)00578-6. PubMed DOI

Penner M. J. Detection of temporal gaps in noise as a measure of the decay of auditory sensation. The Journal of the Acoustical Society of America. 1977;61(2):552–557. doi: 10.1121/1.381297. PubMed DOI

Giraudi D., Salvi R., Henderson D., Hamernik R. Gap detection by the chinchilla. The Journal of the Acoustical Society of America. 1980;68(3):802–806. doi: 10.1121/1.384818. PubMed DOI

Kelly J. B., Masterton B. Auditory sensitivity of the albino rat. Journal of Comparative and Physiological Psychology. 1977;91(4):930–936. doi: 10.1037/h0077356. PubMed DOI

Dean K. F., Sheets L. P., Crofton K. M., Reiter L. W. The effect of age and experience on inhibition of the acoustic startle response by gaps in background noise. Psychobiology. 1990;18(1):89–95. doi: 10.3758/BF03327220. DOI

Leitner D. S., Hammond G. R., Springer C. P., et al. Parameters affecting gap detection in the rat. Perception & Psychophysics. 1993;54(3):395–405. doi: 10.3758/BF03205275. PubMed DOI

Steube N., Nowotny M., Pilz P. K., Gaese B. H. Dependence of the startle response on temporal and spectral characteristics of acoustic modulatory influences in rats and gerbils. Frontiers in Behavioral Neuroscience. 2016;10 doi: 10.3389/fnbeh.2016.00133. PubMed DOI PMC

Halliday L. F., Bishop D. V. Frequency discrimination and literacy skills in children with mild to moderate sensorineural hearing loss. Journal of Speech Language and Hearing Research. 2005;48(5):1187–1203. doi: 10.1044/1092-4388(2005/083). PubMed DOI

Ahissar M., Protopapas A., Reid M., Merzenich M. M. Auditory processing parallels reading abilities in adults. Proceedings of the National Academy of Sciences of the United States of America. 2000;97(12):6832–6837. doi: 10.1073/pnas.97.12.6832. PubMed DOI PMC

Au T. K., Knightly L. M., Jun S. A., Oh J. S. Overhearing a language during childhood. Psychological Science. 2002;13(3):238–243. doi: 10.1111/1467-9280.00444. PubMed DOI

Hepper P. G., Shahidullah S. Habituation in normal and Down’s syndrome fetuses. The Quarterly Journal of Experimental Psychology Section B. 1992;44(3-4):305–317. doi: 10.1080/02724999208250617. PubMed DOI

Birnholz J. C., Benacerraf B. R. The development of human fetal hearing. Science. 1983;222(4623):516–518. doi: 10.1126/science.6623091. PubMed DOI

Shahidullah S., Hepper P. G. Frequency discrimination by the fetus. Early Human Development. 1994;36(1):13–26. doi: 10.1016/0378-3782(94)90029-9. PubMed DOI

Newport E. L. Language development, critical periods in. In: Nadel L., editor. Encyclopedia of Cognitive Science. Nature Publishing Group; 2006. DOI

Kuhl P. Brain mechanisms in early language acquisition. Neuron. 2010;67(5):713–727. doi: 10.1016/j.neuron.2010.08.038. PubMed DOI PMC

Friederici A. The cortical language circuit: from auditory perception to sentence comprehension. Trends in Cognitive Sciences. 2012;16(5):262–268. doi: 10.1016/j.tics.2012.04.001. PubMed DOI