title: Extrinsic embryonic sensory stimulation alters multimodal behavior and cellular activation.
abstract: Embryonic vision is generated and maintained by spontaneous neuronal activation patterns, yet extrinsic stimulation also sculpts sensory development. Because the sensory and motor systems are interconnected in embryogenesis, how extrinsic sensory activation guides multimodal differentiation is an important topic. Further, it is unknown whether extrinsic stimulation experienced near sensory sensitivity onset contributes to persistent brain changes, ultimately affecting postnatal behavior. To determine the effects of extrinsic stimulation on multimodal development, we delivered auditory stimulation to bobwhite quail groups during early, middle, or late embryogenesis, and then tested postnatal behavioral responsiveness to auditory or visual cues. Auditory preference tendencies were more consistently toward the conspecific stimulus for animals stimulated during late embryogenesis. Groups stimulated during middle or late embryogenesis showed altered postnatal species-typical visual responsiveness, demonstrating a persistent multimodal effect. We also examined whether auditory-related brain regions are receptive to extrinsic input during middle embryogenesis by measuring postnatal cellular activation. Stimulated birds showed a greater number of ZENK-immunopositive cells per unit volume of brain tissue in deep optic tectum, a midbrain region strongly implicated in multimodal function. We observed similar results in the medial and caudomedial nidopallia in the telencephalon. There were no ZENK differences between groups in inferior colliculus or in caudolateral nidopallium, avian analog to prefrontal cortex. To our knowledge, these are the first results linking extrinsic stimulation delivered so early in embryogenesis to changes in postnatal multimodal behavior and cellular activation. The potential role of competitive interactions between the sensory and motor systems is discussed.
authors.affiliation: Department of Psychology, University of Texas, Austin, Texas 78712, USA. rmarkham@mail.utexas.edu
authors.forename: Rebecca G
authors.initials: RG
authors.lastname: Markham
authors.forename: Toru
authors.initials: T
authors.lastname: Shimizu
authors.forename: Robert
authors.initials: R
authors.lastname: Lickliter
mesh_terms: D000161:Acoustic Stimulation / Q000379:methods; D000344:Afferent Pathways / Q000166:cytology* / Q000196:embryology*; D000367:Age Factors; D000818:Animals; D000831:Animals, Newborn; D001307:Auditory Perception / Q000502:physiology*; D001522:Behavior, Animal / Q000502:physiology* / Q000528:radiation effects; D001931:Brain Mapping; D016009:Chi-Square Distribution; D002755:Choice Behavior / Q000502:physiology; D004625:Embryo, Nonmammalian; D017874:Immediate-Early Proteins / Q000378:metabolism; D008425:Maternal Behavior / Q000502:physiology; D010775:Photic Stimulation / Q000379:methods; D011784:Quail / Q000196:embryology; D011930:Reaction Time / Q000502:physiology; D011984:Sensory Receptor Cells / Q000378:metabolism; D014796:Visual Perception / Q000502:physiology*; D014828:Vocalization, Animal / Q000502:physiology
chemical_list: D017874:Immediate-Early Proteins
references.citation: Brain Behav Evol. 1976;13(1):1-21
references.pmid: 974720
references.citation: J Neurosci. 1998 Nov 1;18(21):8839-52
references.pmid: 9786990
references.citation: Neuroreport. 1998 Aug 24;9(12):2797-801
references.pmid: 9760123
references.citation: J Neurosci Methods. 1994 Jan;51(1):83-9
references.pmid: 8189753
references.citation: PLoS Biol. 2008 Mar 18;6(3):e62
references.pmid: 18351801
references.citation: Behav Neurosci. 2006 Dec;120(6):1315-25
references.pmid: 17201477
references.citation: Glia. 2003 Jan;41(1):25-37
references.pmid: 12465043
references.citation: Nature. 1974 Oct 18;251(5476):609-10
references.pmid: 4421398
references.citation: Eur J Morphol. 1998 Dec;36(4-5):227-43
references.pmid: 10099952
references.citation: J Neurosci. 1991 Feb;11(2):445-53
references.pmid: 1846908
references.citation: J Comp Neurol. 1998 Apr 20;393(4):426-38
references.pmid: 9550149
references.citation: Brain Res. 1973 Dec 7;63:59-74
references.pmid: 4764322
references.citation: J Neurosci. 2002 Feb 15;22(4):RC210
references.pmid: 11844844
references.citation: J Neurosci. 2003 Nov 26;23(34):10815-26
references.pmid: 14645474
references.citation: J Comp Neurol. 1990 Jun 1;296(1):1-22
references.pmid: 2358525
references.citation: Neurosci Lett. 2003 Jan 16;336(2):81-4
references.pmid: 12499045
references.citation: J Comp Neurol. 1998 Jul 6;396(3):399-414
references.pmid: 9624592
references.citation: J Physiol (Paris). 1974 Jun;68(2):219-41
references.pmid: 4607102
references.citation: Dev Psychobiol. 1994 Apr;27(3):169-83
references.pmid: 8200489
references.citation: Dev Psychobiol. 1989 Nov;22(7):651-67
references.pmid: 2806727
references.citation: Neurobiol Dis. 2006 Sep;23(3):731-9
references.pmid: 16887357
references.citation: J Neurophysiol. 1963 Nov;26:978-93
references.pmid: 14084170
references.citation: Neurosci Behav Physiol. 2008 Mar;38(3):289-96
references.pmid: 18264776
references.citation: J Exp Zool. 1965 Jun;159(1):1-13
references.pmid: 5215365
references.citation: Anim Behav. 1973 Nov;21(4):720-5
references.pmid: 4777201
references.citation: Nature. 1964 Sep 12;203:1192-3
references.pmid: 14213686
references.citation: Brain Res Brain Res Rev. 2000 Apr;32(2-3):343-79
references.pmid: 10760548
references.citation: J Comp Neurol. 1976 Nov 15;170(2):153-72
references.pmid: 62764
references.citation: Neurosci Lett. 1990 Jun 8;113(3):241-6
references.pmid: 2381560
references.citation: J Neurobiol. 2005 Dec;65(3):251-9
references.pmid: 16155900
references.citation: J Comp Neurol. 2005 Aug 1;488(3):342-51
references.pmid: 15952168
references.citation: Neuroscience. 2005;130(3):611-7
references.pmid: 15590145
references.citation: Curr Opin Neurobiol. 2002 Feb;12(1):104-9
references.pmid: 11861172
references.citation: Proc Natl Acad Sci U S A. 2007 Nov 27;104(48):19108-13
references.pmid: 18025474
references.citation: Prog Neurobiol. 2004 Nov;74(4):183-211
references.pmid: 15556287
references.citation: J Neurosci. 1990 Sep;10(9):3118-34
references.pmid: 2204687
references.citation: Exp Neurol. 1979 Dec;66(3):587-601
references.pmid: 488239
references.citation: Mol Biol Evol. 1998 Mar;15(3):284-92
references.pmid: 9501495
references.citation: J Comp Neurol. 2004 May 10;472(4):395-410
references.pmid: 15065115
references.citation: J Neurophysiol. 2006 Jul;96(1):128-41
references.pmid: 16598067
references.citation: J Comp Physiol Psychol. 1973 Jul;84(1):134-9
references.pmid: 4717545
references.citation: Nature. 2000 Apr 20;404(6780):871-6
references.pmid: 10786793
references.citation: J Neurosci. 2007 Jan 3;27(1):180-9
references.pmid: 17202485
references.citation: Dev Psychobiol. 1992 Jan;25(1):17-31
references.pmid: 1740227
references.citation: J Comp Neurol. 2003 Sep 29;464(4):511-24
references.pmid: 12900921
references.citation: J Exp Zool. 1967 Nov;166(2):171-203
references.pmid: 6080550
references.citation: J Neurophysiol. 1978 Jul;41(4):870-84
references.pmid: 681991