156
Views
0
CrossRef citations to date
0
Altmetric
Original Articles

The effect of insular cortex lesion on hyperacusis-like behavior in rats

, , ORCID Icon, , &
Pages 1071-1081 | Received 13 Jul 2019, Accepted 07 Jan 2020, Published online: 07 Apr 2020

References

  • Salloum RH, Yurosko C, Santiago L, et al. Induction of enhanced acoustic startle response by noise exposure: dependence on exposure conditions and testing parameters and possible relevance to hyperacusis. PloS one. 2014;9(10):e111747.
  • Pienkowski M, Tyler RS, Roncancio ER, et al. A review of hyperacusis and future directions: part II. Measurement, mechanisms, and treatment. Am J Audiol. 2014;23(4):420–436.
  • Fabijanska A, et al. Epidemiology of tinnitus and hyperacusis in Poland in Proceedings of the Sixth International Tinnitus Seminar, Citeseer; 1999.
  • Andersson G, Lindvall N, Hursti T, et al. Hypersensitivity to sound (hyperacusis): a prevalence study conducted via the internet and post: Hipersensibilidad al sonido (hiperacusia): un estudio de prevalencia realizado por internet y por correo. Int J Audiol. 2002;41(8):545–554.
  • Jastreboff PJ, Jastreboff MM. Decreased sound tolerance: hyperacusis, misophonia, diplacousis, and polyacousis. Handb Clin Neurol. 2015;129:375–387.
  • Liberman MC, Kiang NY. Acoustic trauma in cats: cochlear pathology and auditory-nerve activity. Acta Oto-laryngol. 1978;358:1–68.
  • Brozoski T, Bauer C, Caspary D. Elevated fusiform cell activity in the dorsal cochlear nucleus of chinchillas with psychophysical evidence of tinnitus. J Neurosci. 2002;22(6):2383–2390.
  • Salvi RJ, Saunders SS, Gratton MA, et al. Enhanced evoked response amplitudes in the inferior colliculus of the chinchilla following acoustic trauma. Hearing Res. 1990;50(1-2):245–257.
  • Norena A, et al. Neural changes in the auditory cortex of awake guinea pigs after two tinnitus inducers: salicylate and acoustic trauma. Neuroscience. 2010;166(4):1194–1209.
  • Penfield W, Faulk M. Jr, The insula: further observations on its function. Brain. 1955;78(4):445–470.
  • Boucher O, et al. Neuropsychological deficits following damage to the insular cortex: a clinical review. In Insula: neuroanatomy, functions, and clinical disorders. Palo Alto: Nova Publishers; 2014, p. 119–160.
  • Nieuwenhuys R. The insular cortex: a review. Prog Brain Res. 2012;195:123–163.
  • Lemieux F, Lanthier S, Chevrier M-C, et al. Insular ischemic stroke: clinical presentation and outcome. Cerebrovasc Dis Extra. 2012;2(1):80–87.
  • Cereda C, Ghika J, Maeder P, et al. Strokes restricted to the insular cortex. Neurology. 2002;59(12):1950–1955.
  • Bamiou D-E, Musiek FE, Luxon LM. The insula (Island of Reil) and its role in auditory processing: literature review. Brain Res Rev. 2003;42(2):143–154.
  • van der Loo E, Congedo M, Vanneste S, et al. Insular lateralization in tinnitus distress. Auton Neurosci. 2011;165(2):191–194.
  • Irwin A, Hall DA, Peters A, et al. Listening to urban soundscapes: Physiological validity of perceptual dimensions. Psychophysiology. 2011;48(2):258–268.
  • Kliuchko M, Puoliväli T, Heinonen-Guzejev M, et al. Neuroanatomical substrate of noise sensitivity. Neuroimage. 2018;167:309–315.
  • Boucher O, Turgeon C, Champoux S, et al. Hyperacusis following unilateral damage to the insular cortex: a three-case report. Brain Res. 2015;1606:102–112.
  • Khalil S, Ogunyemi L, Osborne J. Middle cerebral artery aneurysm presenting as isolated hyperacusis. J Laryngol Otol. 2002;116(5):376–378.
  • Chen G-D, Manohar S, Salvi R. Amygdala hyperactivity and tonotopic shift after salicylate exposure. Brain Res. 2012; 1485:63–76.
  • Davis M, Walker DL, Lee Y. Roles of the amygdala and bed nucleus of the Stria terminalis in fear and anxiety measured with the acoustic startle reflex: possible relevance to PTSD A. Ann NY Acad Sci. 1997;821(1 Psychobiology):305–331.
  • Walker DL, Davis M. The role of amygdala glutamate receptors in fear learning, fear-potentiated startle, and extinction. Pharmacol Biochem Behav. 2002;71(3):379–392.
  • Ghaziri J, Tucholka A, Girard G, et al. Subcortical structural connectivity of insular subregions. Sci Rep. 2018; 8(1):8596.
  • Chen Y-C, Li X, Liu L, et al. Tinnitus and hyperacusis involve hyperactivity and enhanced connectivity in auditory-limbic-arousal-cerebellar network. Elife. 2015;4:e06576.
  • Kemble ED, Ison JR. Limbic lesions and the inhibition of startle reactions in the rat by conditions of preliminary stimulation. Physiol Behav. 1971;7(6):925–928.
  • Mollet GA. Fundamentals of human neuropsychology. J Undergrad Neurosci Educ. 2008;6(2):R3.
  • Wiebking C, Bauer A, de Greck M, et al. Abnormal body perception and neural activity in the insula in depression: an fMRI study of the depressed “material me. World J Biol Psychiat. 2010;11(3):538–549.
  • Uddin LQ, Menon V. The anterior insula in autism: under-connected and under-examined. Neurosci Biobehav Rev. 2009;33(8):1198–1203.
  • Shulman A, Strashun AM, Avitable MJ, et al. Ultra-high frequency acoustic stimulation and tinnitus control: a positron emission tomography study. Int Tinnitus J. 2004; 10(2) :113–125.
  • Sanchez-Juan P, Combarros O. Gustatory nervous pathway syndromes. Neurologia (Barcelona, Spain). 2001;16(6):262–271.
  • Liu Z, Xu C, Xu Y, et al. Decreased regional homogeneity in insula and cerebellum: a resting-state fMRI study in patients with major depression and subjects at high risk for major depression. Psychiat ResNeuroimag. 2010;182(3):211–215.
  • Jabbi M, Kippenhan JS, Kohn P, et al. The Williams syndrome chromosome 7q11. 23 hemideletion confers hypersocial, anxious personality coupled with altered insula structure and function. Proc Natl Acad Sci. 2012;109(14):E860–E866.
  • Borsook D, Veggeberg R, Erpelding N, et al. The insula: a “hub of activity” in migraine. Neuroscientist. 2016;22(6):632–652.
  • King CT, Hashimoto K, Blonde GD, et al. Unconditioned oromotor taste reactivity elicited by sucrose and quinine is unaffected by extensive bilateral damage to the gustatory zone of the insular cortex in rats. Brain Res. 2015;1599:9–19.
  • Paxinos G, Watson CR, Emson PC. AChE-stained horizontal sections of the rat brain in stereotaxic coordinates. J Neurosci Methods. 1980;3(2):129–149.
  • Schier LA, Blonde GD, Spector AC. Bilateral lesions in a specific subregion of posterior insular cortex impair conditioned taste aversion expression in rats. J Comp Neurol. 2016; 524(1) :54–73.
  • Cosme CV, Gutman AL, LaLumiere RT. The dorsal agranular insular cortex regulates the cued reinstatement of cocaine-seeking, but not food-seeking, behavior in rats. Neuropsychopharmacology. 2015; 40(10) :2425–2433.
  • Kirby ED, Jensen K, Goosens KA, et al. Stereotaxic surgery for excitotoxic lesion of specific brain areas in the adult rat. J Vis Exp. 2012;(65):e4079.
  • Ison JR, Allen PD, O’Neill WE. Age-related hearing loss in C57BL/6J mice has both frequency-specific and non-frequency-specific components that produce a hyperacusis-like exaggeration of the acoustic startle reflex. JARO. 2007;8(4):539–550.
  • Turner JG, Parrish J. Gap detection methods for assessing salicylate-induced tinnitus and hyperacusis in rats. Am J Audiol. 2008;17(2):S185–S192.
  • Sun W, Deng A, Jayaram A, et al. Noise exposure enhances auditory cortex responses related to hyperacusis behavior. Brain Res. 2012;1485:108–116.
  • Sun W, Lu J, Stolzberg D, et al. Salicylate increases the gain of the central auditory system. Neuroscience. 2009;159(1):325–334.
  • Chen G, Lee C, Sandridge SA, et al. Behavioral evidence for possible simultaneous induction of hyperacusis and tinnitus following intense sound exposure. JARO. 2013;14(3):413–424.
  • Hickox AE, Liberman MC. Is noise-induced cochlear neuropathy key to the generation of hyperacusis or tinnitus? J Neurophysiol. 2014;111(3):552–564.
  • Pace E, Zhang J. Noise-induced tinnitus using individualized gap detection analysis and its relationship with hyperacusis, anxiety, and spatial cognition. PloS one. 2013;8(9):e75011.
  • Baguley DM. Hyperacusis. J R Soc Med. 2003;96(12):582–585.
  • Dauman R, Bouscau-Faure F. Assessment and amelioration of hyperacusis in tinnitus patients. Acta Oto-laryngol. 2005;125(5):503–509.
  • Coelho CB, Sanchez TG, Tyler RS. Hyperacusis, sound annoyance, and loudness hypersensitivity in children. Prog Brain Res. 2007;166:169–178.
  • Rosen JB, Hitchcock JM, Miserendino MJ, et al. Lesions of the perirhinal cortex but not of the frontal, medial prefrontal, visual, or insular cortex block fear-potentiated startle using a visual conditioned stimulus. J Neurosci. 1992;12(12):4624–4633.
  • Moraga-Amaro R, Stehberg J. The insular cortex and the amygdala: shared functions and interactions. In: Ferry B, editor. The amygdala: a discrete multitasking manager. Rijeka: In Tech; 2012. p. 12–19.
  • Shi C, Davis M. Pain pathways involved in fear conditioning measured with fear-potentiated startle: lesion studies. J Neurosci. 1999;19(1):420–430.
  • Davis M. Neural systems involved in fear and anxiety measured with fear-potentiated startle. Am Psychol. 2006;61(8):741–756.
  • Dashti S, Aboutaleb N, Shahbazi A. The effect of leptin on prepulse inhibition in a developmental model of schizophrenia. Neurosci Lett. 2013;555:57–61.
  • Noori-Daloii M, et al. Knocking down the DRD2 by shRNA expressing plasmids in the nucleus accumbens prevented the disrupting effect of apomorphine on prepulse inhibition in rat. J Sci I R Iran. 2015; 26(3):205–212.
  • Davis M, Strachan D, Kass E. Excitatory and inhibitory effects of serotonin on sensorimotor reactivity measured with acoustic startle. Science. 1980;209(4455):521–523.
  • Quednow BB, Westheide J, Kühn K-U, et al. Normal prepulse inhibition and habituation of acoustic startle response in suicidal depressive patients without psychotic symptoms. J Affect Disord. 2006;92(2-3):299–303.
  • Fournier P, Hébert S. Gap detection deficits in humans with tinnitus as assessed with the acoustic startle paradigm: does tinnitus fill in the gap? Hear Res. 2013;295:16–23.
  • Marriage J, Barnes N. Is central hyperacusis a symptom of 5-hydroxytryptamine (5-HT) dysfunction? J Laryngol Otol. 1995;109(10):915–921.
  • Holt AG, Bissig D, Mirza N, et al. Evidence of key tinnitus-related brain regions documented by a unique combination of manganese-enhanced MRI and acoustic startle reflex testing. PloS One. 2010;5(12):e14260.
  • Farahani S, Nasirinezhad F, Danyali S, et al. Does 5, 7-Dihydroxytryptamine injection into nucleus accumbens cause hyperacusis? Neurosci Lett. 2019;705:246–250.
  • Hood J, Poole J. Tolerable limit of loudness: its clinical and physiological significance. J Acoust Soc Am. 1966;40(1):47–53.
  • Perrot X, Ryvlin P, Isnard J, et al. Evidence for corticofugal modulation of peripheral auditory activity in humans. Cereb Cortex. 2006;16(7):941–948.
  • Dewson III, JH, KW, Nobel KH. Pribram Corticofugal influence at cochlear nucleus of the cat: some effects of ablation of insular-temporal cortex. Brain Res. 1966;2(2):151–159.
  • Seeley WW, Menon V, Schatzberg AF, et al. Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci. 2007;27(9):2349–2356.
  • Auerbach BD. Physiological mechanisms of hyperacusis: an update. ENT Audiol News. 2019;27(6).
  • Augustine JR. Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res Rev. 1996;22(3):229–244.
  • Zhang Y, Zhou W, Wang S, et al. The roles of subdivisions of human insula in emotion perception and auditory processing. Cereb Cortex. 2019;29(2):517–528.
  • Shipley MT, Geinisman Y. Anatomical evidence for convergence of olfactory, gustatory, and visceral afferent pathways in mouse cerebral cortex. Brain Res Bull. 1984;12(3):221–226.
  • Mak YE, Simmons KB, Gitelman DR, et al. Taste and olfactory intensity perception changes following left insular stroke. Behav Neurosci. 2005;119(6):1693–1700.
  • Lasiter PS, Deems DA, Garcia J. Involvement of the anterior insular gustatory neocortex in taste-potentiated odor aversion learning. Physiol Behav. 1985;34(1):71–77.
  • Starr CJ, Sawaki L, Wittenberg GF, et al. Roles of the insular cortex in the modulation of pain: insights from brain lesions. J Neurosci. 2009;29(9):2684–2694.
  • Ackermann H, Riecker A. The contribution of the insula to motor aspects of speech production: a review and a hypothesis. Brain Lang. 2004;89(2):320–328.
  • Showers MJC, Lauer EW. Somatovisceral motor patterns in the insula. J Comp Neurol. 1961;117(1):107–115.
  • Dambacher F, Sack AT, Lobbestael J, et al. Out of control: evidence for anterior insula involvement in motor impulsivity and reactive aggression. Soc Cogn Affect Neurosci. 2015;10(4):508–516.
  • Cechetto DF, Chen S. Subcortical sites mediating sympathetic responses from insular cortex in rats. Am J Physiol Regul Integr Comp Physiol. 1990;258(1):R245–R255.
  • Jezzini A, Caruana F, Stoianov I, et al. Functional organization of the insula and inner perisylvian regions. Proc Natl Acad Sci. 2012;109(25):10077–10082.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.