Abstract
Sensory stimulation has a critical role to play in the development of an individual. Environmental factors tend to modify the inputs received by the sensory pathway. The developing brain is most vulnerable to these alterations and interacts with the environment to modify its neural circuitry. In addition to other sensory stimuli, auditory stimulation can also act as external stimuli to provide enrichment during the perinatal period. There is evidence that suggests that enriched environment in the form of auditory stimulation can play a substantial role in modulating plasticity during the prenatal period. This review focuses on the emerging role of prenatal auditory stimulation in the development of higher brain functions such as learning and memory in birds and mammals. The molecular mechanisms of various changes in the hippocampus following sound stimulation to effect neurogenesis, learning and memory are described. Sound stimulation can also modify neural connectivity in the early postnatal life to enhance higher cognitive function or even repair the secondary damages in various neurological and psychiatric disorders. Thus, it becomes imperative to examine in detail the possible ameliorating effects of prenatal sound stimulation in existing animal models of various psychiatric disorders, such as autism.
Similar content being viewed by others
Abbreviations
- BDNF:
-
brain-derived neurotrophic factor
- CaBPs:
-
calcium-binding proteins
- CREB:
-
cAMP response element-binding
- E:
-
embryonic day
- MNH:
-
mediorostral nidopallium hyperpallium ventral
- NL:
-
nucleus laminaris
- NM:
-
nucleus magnocellularis
- PV:
-
parvalbumin
- SPL:
-
sound pressure level
References
Abikoff H, Courtney ME, Szeibel PJ and Koplewicz HS 1996 The effects of auditory stimulation on the arithmetic performance of children with ADHD and nondisabled children. J. Learn. Dis. 29 238–246
Aguado F, Carmona MA, Pozas E, Aguiló A, Martínez-Guijarro FJ, Alcantara S, Borrell V, Yuste R, Ibañez CF and Soriano E 2003 BDNF regulates spontaneous correlated activity at early developmental stages by increasing synaptogenesis and expression of the K+/Cl- co-transporter KCC2. Development 130 1267–1280
Alladi PA, Roy TS, Singh N and Wadhwa S 2005a Developmentally regulated expression of c-fos and c-jun in the brainstem auditory nuclei of Gallus domesticus is modified by prenatal auditory enrichment. J. Neurobiol. 62 92–105
Alladi PA, Roy TS, Singh N and Wadhwa S 2005b Prenatal auditory enrichment with species-specific calls and sitar music modulates expression of Bcl-2 and Bax to alter programmed cell death in developing chick auditory nuclei. Int. J. Dev. Neurosci. 23 363–373
Alladi PA, Roy TS, Singh N and Wadhwa S 2002, Effect of prenatal auditory enrichment on developmental expression of synaptophysin and syntaxin 1 in chick brainstem auditory nuclei. Neuroscience 114 577–590
Angelucci F, Fiore M, Ricci E, Padua L, Sabino A and Tonali PA 2007 Investigating the neurobiology of music: brain-derived neurotrophic factor modulation in the hippocampus of young adult mice. Behav. Pharmacol. 18 491–496
Aoun P, Jones T, Shaw GL and Bodner M 2000 Long-term enhancement of maze learning in mice via a generalized Mozart effect. Neurol. Res. 27 791–796
Bartoletti A, Medini P, Berardi N and Maffei L 2004 Environmental enrichment prevents effects of dark-rearing in the rat visual cortex. Nat. Neurosci. 7 215–216
Bernatzky G, Bernatzky P, Hesse HP, Staffen W and Ladurner G 2004 Stimulating music increases motor coordination in patients afflicted with Morbus Parkinson. Neurosci. Lett. 361 4–8
Birnholz JC and Benacerraf BR 1983 The development of human fetal hearing. Science 222 516–518
Blum T, Saling E and Bauer R 1985 First magneto-encephalographic recordings of the brain activity of a human fetus. Brit. J. Obstet. Gynecol. 92 1224–1229
Brotons M and Marti P 2003 Music therapy with Alzheimer's patients and their family caregivers: a pilot project. Music Ther. 40 138–150
Boso M, Emanuele E, Minazzi V, Abbamonte M and Politi P 2007 Effect of long-term interactive music therapy on behavior profile and musical skills in young adults with severe autism. J. Altern. Complement Med. 13 709–712
Boso M, Politi P, Barale F and Enzo E 2006 Neurophysiology and neurobiology of the musical experience. Func. Neurol. 21 187–191
Braun K, Bock J, Metzger M, Jiang S and Schnabel R 1999 The dorsocaudal neostriatum of the domestic chick: a structure serving higher associative functions. Behav. Brain Res. 98 211–218
Burns JL, Labbé E, Arke B, Capeless K, Cooksey B, Steadman A and Gonzales C 2002 The effects of different types of music on perceived and physiological measures of stress. J. Music Ther. 39 101–116
Cancedda L, Putignano E, Sale A, Viegi A, Berardi N and Maffei L 2004 Acceleration of visual system development by environmental enrichment. J. Neurosci. 24 4840–4848
Champoux M, Higley JD and Suomi SJ 1997 Behavioral and physiological characteristics of Indian and Chinese-Indian hybrid rhesus macaque infants. Dev. Psychobiol. 31 49–63
Chaudhury S, Jain S and Wadhwa S 2010 Expression of synaptic proteins in the hippocampus and spatial learning in chicks following prenatal auditory stimulation. Dev. Neurosci. 32 114–124
Chaudhury S, Nag TC and Wadhwa S 2009 Effect of prenatal auditory stimulation on numerical synaptic density and mean synaptic height in the posthatch Day 1 chick hippocampus. Synapse 63 152–159
Chaudhury S, Nag TC and Wadhwa S 2008 Calbindin D-28 K and parvalbumin expression in embryonic chick hippocampus is enhanced by prenatal auditory stimulation. Brain Res. 1191 96–106
Chaudhury S, Nag TC and Wadhwa S 2006 Prenatal acoustic stimulation influences neuronal size and the expression of calcium-binding proteins (calbindin D-28 K and parvalbumin) in chick hippocampus. J. Chem. Neuroanat. 32 117–126
Chaudhury S and Wadhwa S 2009 Prenatal auditory stimulation alters the levels of CREB mRNA, p-CREB and BDNF expression in chick hippocampus. Int. J. Dev. Neurosci. 27 583–90
Chen DG Huang YF Zhang JY and Qi GP 1994 Influence of prenatal music and touch-enrichment on the IQ, motor development, and behavior of infants. Chin. J. Psychol. 8 148–151
Cheng L, Wang SH, Chen QC and Liao XM 2011 Moderate noise induced cognition impairment of mice and its underlying mechanisms. Physiol. Behav. 104 981–988
Chikahisa S, Sei H, Morishima M, Sano A, Kitaoka K, Nakaya Y and Morita Y 2006 Exposure to music in the perinatal period enhances learning performance and alters BDNF/TrkB signaling in mice as adults. Behav. Brain Res.169 312–319
Chugani HT, Behen ME, Muzik O, Juhasz C, Nagy F and Chugani DC 2001 Local brain functional activity following early deprivation: a study of post institutionalized Romanian orphans. Neuroimage 14 1290–1301
Cirulli F, Berry A, Bonsignore LT, Capone F, D'Andrea I, Aloe L, Branchi I and Alleva E 2010 Early life influences on emotional reactivity: evidence that social enrichment has greater effects than handling on anxiety-like behaviors, neuroendocrine responses to stress and central BDNF levels. Neurosci. Biobehav. Rev. 34, 808–820
Clayton NS and Dickinson A 1998 Episodic-like memory during cache recovery by scrub jays. Nature 395 272–274
Cockerton T, Moore S, and Norman D 1997 Cognitive test performance and background music. Perceptual Motor Skills 85 1435–1438
Cohen GM and Fermin CD 1978 The development of hair cells in the embryonic chick’s basilar papilla. Acta Otolaryngol. (Stockh). 86 342–358
Dávila SG, Campo JL, Gil MG, Prieto MT and Torres O 2011 Effects of auditory and physical enrichment on 3 measurements of fear and stress (tonic immobility duration, heterophil to lymphocyte ratio, and fluctuating asymmetry) in several breeds of layer chicks. Poult. Sci. 90 2459–2466
Dmitrieva LP and Gottlieb G 1994 Influence of auditory experience on the development of brainstem auditory-evoked potentials in mallard duck embryos and hatchlings. Behav. Neurol. Biol. 61 19–28
Emery NJ and Clayton NS 2001 Effects of experience and social context on prospective caching strategies by scrub jays. Nature 414 443–446
Erichsen JT, Ciocchetti A, Fontanesi F and Bagnoli P 1994 Neuroactive substances in the developing dorsomedial telencephalon of the pigeon (Columba livia): differential distribution and time course of maturation. J. Comp. Neurol. 345 537–561
Ezzone S, Baker C, Rosselet R and Terepka E 1998 Music as an adjunct to antiemetic therapy. Oncol. Nurs. Forum 25 1551–1516
Foushée RD and Lickliter R 2002 Early visual experience affects postnatal auditory responsiveness in bobwhite quail (Colinus virginianus). J. Comp. Psychol. 116 369–380
Fukui H and Toyoshima K 2008 Music facilitates the neurogenesis, regeneration and repair of neurons. Med. Hypotheses 71 765–769
Funabiki Y, Murai T and Toichi M 2012 Cortical activation during attention to sound in autism spectrum disorders. Res. Dev. Disabil. 33 518–524
Ghim JW, Baeg EH, Kim YB and Jung MW 2011 Stimulus-induced reduction of noise correlation in rat prefrontal cortex. Neuroreport 22 824–829
Gibbs ME 2008 Memory systems in the chick: regional and temporal control by noradrenaline. Brain Res. Bull. 76 170–82
Gold C, Heldal TO, Dahle T and Wigram T 2005 Music therapy for schizophrenia or schizophrenia-like illnesses. Cochrane Database Syst. Rev. 18 CD004025
Gottlieb G 1963 "Imprinting" in nature. Science 139 497–498
Gottlieb G 1965 Prenatal auditory sensitivity in chickens and ducks. Science 147 1596–1598
Guilarte TR, Toscano CD, McGlothan JL and Weaver SA 2003 Environmental enrichment reverses cognitive and molecular deficits induced by developmental lead exposure. Ann. Neurol. 53 50–56
Hallam S, Price J and Katsarou G 2002 The effects of background music on primary school pupils’ task performance. Educational Studies 28 111–122
Harlow HF and Harlow M 1966 Learning to love. Am. Sci. 54 244–272
Harshaw C and Lickliter R 2011 Biased embryos: Prenatal experience alters the postnatal malleability of auditory preferences in bobwhite quail. Dev. Psychobiol. 53 291–302
Harshaw C and Lickliter R 2010 Biased Embryos: Prenatal Experience alters the postnatal malleability of auditory preferences in Bobwhite Quail. Dev. Psychobiol. 53 291–302
Herdener M, Esposito F, di Salle F, Boller C, Hilti CC, Habermeyer B, Scheffler K, Wetzel S, Seifritz E and Cattapan-Ludewig K 2010 Musical training induces functional plasticity in human hippocampus. J. Neurosci. 30 1377–1384
Honeycutt H and Lickliter R 2002 Prenatal experience and postnatal perceptual preferences: evidence for attentional-bias in bobwhite quail embryos (Colinus virginianus). J. Comp. Psychol. 116 270–276
Honeycutt H and Lickliter R 2003 The influence of prenatal tactile and vestibular stimulation on auditory and visual responsiveness in bobwhite quail: A matter of timing. Dev. Psychobiol. 43 71–81
Hirano Y, Fujita M, Watanabe K, Niwa M, Takahashi T, Kanematsu M, Ido Y, Tomida M and Onozuka M 2006 Effect of unpleasant loud noise on hippocampal activities during picture encoding: an fMRI study. Brain Cogn. 61 280–285
Hykin J, Moore R, Duncan K, Clare S, Baker P, Johnson I, Bowtell R, Mansfield P and Gowland P 1999 Fetal brain activity demonstrated by functional magnetic resonance imaging. Lancet 354 645–646
Iuvone L, Geloso MC and Dell’Anna E 1996 Changes in open field behavior, spatial memory, and hippocampus parvalbumin immunoreactivity following enrichment in rats exposed to neonatal anoxia. Exp. Neurol. 139 25–33
Ivanov VK and Geake JG 2003 The Mozart effect and primary school children. Psychol. Music 31 405–413
Jackson H and Rubel EW 1978 Ontogeny of behavioral responsiveness to sound in the chick embryo as indicated by electrical recordings of motility. J. Comp. Physiol. Psychol. 92 682–696
Jackson H, Hackett JT and Rubel EW 1982 Organization and development of brainstem auditory nuclei in the chick: ontogeny of postsynaptic responses. J. Comp. Neurol. 210 80–86
Jain S, Sharma R and Wadhwa S 2004 Effect of prenatal species-specific and music stimulation on the postnatal auditory preference of domestic chick. Indian J. Physiol. Pharmacol. 48 174–183
Jarvis ED, Güntürkün O, Bruce L, Csillag A, Karten H, Kuenzel W, Medina L, Paxinos G, et al. 2005 Avian Brain Nomenclature Consortium; Avian brains and a new understanding of vertebrate brain evolution. Nat. Rev. Neurosci. 6 151–159
Jáuregui-Huerta F, Garcia-Estrada J, Ruvalcaba-Delgadillo Y, Trujillo X, Huerta M, Feria-Velasco A, Gonzalez-Perez O and Luquin S 2011 Chronic exposure of juvenile rats to environmental noise impairs hippocampal cell proliferation in adulthood. Noise Health 13 286–291
Johnston TD and Gottlieb G 1981 Visual preferences of imprinted ducklings are altered by the maternal call. J. Comp. Physiol. Psychol. 95 663–675
Johnson JK, Shaw GL, Vuong M, Vuong S and Cotman CW 2002 Short-term improvement on a visual-spatial task after music listening in Alzheimer’s disease: A group study. Activities Adaptation and Aging 26 37–50
Kallen B 1962 II. Embryogenesis of brain nuclei in the chick telencephalon. Ergeb. Anat. Entwicklungsgesch. 36 62–82
Kauser H, Roy S, Pal A, Sreenivas V, Mathur R, Wadhwa S and Jain S 2011 Prenatal complex rhythmic music sound stimulation facilitates postnatal spatial learning but transiently impairs memory in the domestic chick. Dev. Neurosci. 33 48–56
Kim H, Lee MH, Chang HK, Lee TH, Lee HH, Shin MC, Won R, Shin HS and Kim CJ 2006 Influence of prenatal noise and music on the spatial memory and neurogenesis in the hippocampus of developing rats. Brain Dev. 28 109–114
Knight WE and Rickard NS 2001 Relaxing music prevents stress-induced increases in subjective anxiety, systolic blood pressure, and heart rate in healthy males and females. J. Music Ther. 38 254–272
Knowlton VY 1967 Effects of extraembryonic membrane deficiency on differentiation of the embryonic avian brain and sense organs. Acta. Anat. (Basel). 66 420–445
Knudsen EI 2002 Instructed learning in the auditory localization pathway of the barn owl. Nature 417 322–328
Koelsch S, Fritz T, V Cramon DY, Müller K and Friederici AD 2006 Investigating emotion with music: an fMRI study. Hum. Brain Mapp. 27 239–250
Lazic M, Schneider SM and Lickliter R 2007 Enriched rearing facilitates spatial exploration in northern bobwhite (Colinus virginianus) neonates. Dev. Psychobiol. 49 548–551
Leal-Galicia P, Castañeda-Bueno M, Quiroz-Baez R and Arias C 2008 Long-term exposure to environmental enrichment since youth prevents recognition memory decline and increases synaptic plasticity markers in aging. Neurobiol. Learn. Mem. 90 511–518
Leng X and Shaw GL 1991 Toward a neural theory of higher brain function using music as a window. Concepts Neurosci. 2 229–258
Lickliter R, Bahrick LE and Honeycutt H 2002 Intersensory redundancy facilitates prenatal perceptual learning in bobwhite quail (Colinus virginianus) embryos. Dev. Psychol. 38 15–23
Lickliter R and Stoumbos J 1991 Enhanced prenatal auditory experience facilitates species-specific visual responsiveness in bobwhite quail chicks (Colinus virginianus). J. Comp. Psychol. 105 89–94
Lickliter R and Stoumbos J 1992 Modification of prenatal auditory experience alters postnatal auditory preferences of bobwhite quails chicks. Q. J. Exp. Psychol. Biol. 44 199–214
Li WJ, Yu H, Yang JM, Gao J, Jiang H, Feng M, Zhao YX and Chen ZY 2010 Anxiolytic effect of music exposure on BDNFMet/Met transgenic mice. Brain Res. 1347 71–79
Lind J 1980 Music and the small human being. Acta Paediatr. Scand. 69 131–136
Lippe WR 1994 Rhythmic spontaneous activity in the developing avian auditory system. J. Neurosci. 14 1486–1495
Ma L, Chen YH and Wei LX 2011 Effects of early enriched environment on long-term behavior development and serum corticosterone level in rats. Zhongguo Dang Dai Er Ke Za Zhi 13 586–589
Maegele M, Lippert-Gruener M, Ester-Bode T, Sauerland S, Schäfer U, Molcanyi M, Lefering R, Bouillon B, Neiss WF, Angelov DN, Klug N, McIntosh TK and Neugebauer EA 2005 Reversal of neuromotor and cognitive dysfunction in an enriched environment combined with multimodal early onset stimulation after traumatic brain injury in rats. J. Neurotraum. 22 772–782
Manikandan S, Padma MK, Srikumar R, Jeya Parthasarathy N, Muthuvel A and Sheela Devi R 2006 Effects of chronic noise stress on spatial memory of rats in relation to neuronal dendritic alteration and free radical-imbalance in hippocampus and medial prefrontal cortex. Neurosci. Lett. 399 17–22
Metzger M, Jiang S and Braun K 1998 Organization of the dorsocaudal neostriatal complex: a retrograde and anterograde tracing study in the domestic chick with special emphasis on pathways relevant to imprinting. J. Comp. Neurol. 395 380–404
Mitchell DE and Sengpiel F 2009 Neural mechanisms of recovery following early visual deprivation. Philos. Trans. R. Soc. London B. Biol. Sci. 364 383–398
Molla R, Rodriguez J, Calvet S and Garcia-Verdugo JM 1986 Neuronal types of the cerebral cortex of the adult chicken (Gallus gallus). AGolgi study. J. Hirnforsch. 27 381–390
Morrongiello BA and Rocca PT 1987 Infants' localization of sounds in the horizontal plane: effects of auditory and visual cues. Child Dev. 58 918–927
Moxon KA, Gerhardt GA, Bickford PC, Austin K, Rose GM, Woodward DJ and Adler LE 1999 Multiple single units and population responses during inhibitory gating of hippocampal auditory response in freely-moving rats. Brain Res. 825 75–85
Muir D and Field J 1979 Newborn infants orient to sounds. Child Dev. 50 431–436
Noda R, Maeda Y and Yoshino A 2004 Therapeutic time window for musicokinetic therapy in a persistent vegetative state after severe brain damage. Brain Inj. 18 509–515
Panicker H, Wadhwa S and Roy TS 2002 Effect of prenatal sound stimulation on medio-rostral neostriatum/hyperstriatum ventrale region of chick forebrain: a morphometric and immunohistochemical study. J. Chem. Neuroanat. 24 127–135
Pettigrew AG, Ansselin AD and Bramley JR 1988 Development of functional innervation in the second and third order auditory nuclei of the chick. Development 104 575–588
Puelles L, Kuwana E, Puelles E, Bulfone A, Shimamura K, Keleher J, Smiga S and Rubenstein J 2000 Pallial and subpallial derivatives in the embryonic chick and mouse telencephalon, traced by the expression of the genes Dlx-2, Emx-1, Nkx-2.1, Pax-6, and Tbr-1. J. Comp. Neurol. 424 409–438
Rauscher FH, Robinson KD and Jens JJ 1998 Improved maze learning through early music exposure in rats. Neurol. Res. 20 427–432
Rauscher FH, Shaw GL and Ky KN 1993 Music and spatial task performance. Nature 365 611
Rauscher FH, Shaw GL and Ky KN 1995 Listening to Mozart enhances spatial-temporal reasoning: towards a neurophysiological basis. Neurosci Lett. 185 44–47
Rauscher FH, Shaw GL, Levine LC, Wright EL, Dennis WR and Newcomb RL 1997 Music training causes long-term enhancement of preschool children’s spatial-temporal reasoning. Neurol. Res. 19 2–8
Reynolds S, Lane SJ and Richards L 2010 Using animal models of enriched environments to inform research on sensory integration intervention for the rehabilitation of neurodevelopmental disorders. J. Neurodev. Disord. 2 120–132
Ricciardi E, Vanello N, Sani L, Gentili C, Scilingo EP, Landini L, Guazzelli M, Bicchi A, Haxby JV and Pietrini P 2007 The effect of visual experience on the development of functional architecture in hMT+. Cereb. Cortex. 17 2933–2939
Rose SP and Stewart MG 1978 Transient increase in muscarinic acetylcholine receptor and acetylcholinesterase in visual cortex on first exposure of dark-reared rats to light. Nature 271 169–170
Rossi C, Angelucci A, Costantin L, Braschi C, Mazzantini M, Babbini F, Fabbri ME Tessarollo L, Maffei L, Berardi N and Caleo M 2006 Brain-derived neurotrophic factor (BDNF) is required for the enhancement of hippocampal neurogenesis following environmental enrichment. Eur. J. Neurosci. 24 1850–1856
Sanes, DH and Walsh EJ 1998 The development of central auditory processing; in Development of the auditory system (ed) EW Rubel, AN Popper and RR Fay (New York: Springer-Verlag) pp 271–314
Siegel JJ, Nitz D and Bingman VP 2002 Electrophysiological profile of avian hippocampal unit activity: a basis for regional subdivisions. J. Comp. Neurol. 445 256–268
Siedliecki SL and Good M 2006 Effect of music on power, pain, depression and disability. J. Adv. Nurs. 54 553–562
Smith PF, Horii A, Russell N, Bilkey DK, Zheng Y, Liu P, Kerr DS and Darlington CL 2005 The effects of vestibular lesions on hippocampal function in rats. Prog. Neurobiol. 75 391–405
Sun H, Zhang J, Zhang L, Liu H, Zhu H and Yang Y 2010 Environmental enrichment influences BDNF and NR1 levels in the hippocampus and restores cognitive impairment in chronic cerebral hypoperfused rats. Curr. Neurovasc. Res. 7 268–280
Sale A, Putignano E, Cancedda L, Landi S, Cirulli F, Berardi N and Maffei L 2004 Enriched environment and acceleration of visual system development. Neuropharmacology 47 649–660
Saunders JC, Coles RB and Gates GR 1973 The development of auditory evoked responses in the cochlea and cochlear nuclei of the chick. Brain Res. 7 59–74
Schreiber EH 1988 Influence of music on college students’ achievements. Perceptual and Motor Skills 66 338
Sleigh MJ and Lickliter R 1995 Augmented prenatal visual stimulation alters postnatal auditory and visual responsiveness in bobwhite quail chicks. Dev. Psychobiol. 28 353–366
Skeels HM 1966 Adult status of children with contrasting early life experiences. Monogr. Soc. Child Dev. 31 1–56
Stainback SB, Stainback WC and Hallahan DP 1973 Effect of background music on learning. Exceptional Children 40 109–110
Sung HC and Chang AM 2005 Use of preferred music to decrease agitated behaviours in older people with dementia: a review of the literature. J. Clin. Nurs. 14 1133–1140
Talwar N, Crawford MJ, Maratos A, Nur U, McDermott O and Procter S 2006 Music therapy for in-patients with schizophrenia: exploratory randomised controlled trial. Br. J. Psychiatry. 189 405–409
Thompson BM, Moulin CJ A, Hayre S and Jones RW 2005 Music enhances category fluency in health older adults and Alzheimer’s disease patients. Experimental Ageing Research 31 91–99
Trottier C, Reperant J and Miceli D 1995 Anatomical evidence of a retino-thalamo-hippocampal pathway in the pigeon (Columba livia). J. Hirnforsch. 36 489–500
Wadhwa S, Anand P and Bhowmick D 1999 Quantitative study of plasticity in the auditory nuclei of chick under conditions of prenatal sound attenuation and overstimulation with species-specific and music sound stimuli. Int. J. Dev. Neurosci. 17 239–253
Wallentin M, Nielsen AH, Vuust P, Dohn A, Roepstorff A and Lund TE 2011 Amygdala and heart rate variability responses from listening to emotionally intense parts of a story. Neuroimage 58 963–973
Wang H, Brozoski TJ, Ling L, Hughes LF and Caspary DM 2011 Impact of sound exposure and aging on brain-derived neurotrophic factor and tyrosine kinase B receptors levels in dorsal cochlear nucleus 80 days following sound exposure. Neuroscience 172 453–459
Whitehead MC and Morest DK 1985a The development of innervation patterns in the avian cochlea. Neuroscience 14 255–276
Whitehead MC and Morest DK 1985b The growth of cochlear fibers and the formation of their synaptic endings in the avian ear: a study with the electron microscope. Neuroscience 14 277–300
Wild JM, Karten HJ and Frost BJ 1993 Connections of the auditory forebrain in the pigeon (Columba livia). J. Comp. Neurol. 337 32–62
Ziabreva I, Poeggal G, Schnabel R and Braun K 2003 Separation-induced receptor changes in the hippocampus and amygdala of Octodon degus: influence of maternal vocalizations. J. Neurosci. 23 5329–533
Acknowledgements
The work was financially supported by Department of Biotechnology, New Delhi (Grant number: BT/PR3148/BRB/10/276/2002 and BT/ PR6771/BRB/10/448/2005 to SW and Council of Scientific and Industrial Research (no. 37/1242/06 EMRII to SJ).
Author information
Authors and Affiliations
Corresponding author
Additional information
Corresponding editor: Vidita A Vaidya
[Chaudhury S, Nag TC, Jain S and Wadhwa S 2013 Role of sound stimulation in reprogramming brain connectivity. J. Biosci. 38 1–10] DOI 10.1007/s12038-013-9341-8
Rights and permissions
About this article
Cite this article
Chaudhury, S., Nag, T.C., Jain, S. et al. Role of sound stimulation in reprogramming brain connectivity. J Biosci 38, 605–614 (2013). https://doi.org/10.1007/s12038-013-9341-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12038-013-9341-8