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Published in: Brain Structure and Function 8/2017

01-11-2017 | Original Article

Morphological correlates of sex differences in acoustic startle response and prepulse inhibition through projections from locus coeruleus to cochlear root neurons

Authors: Sebastian Hormigo, Ricardo Gómez-Nieto, Consuelo Sancho, Javier Herrero-Turrión, Juan Carro, Dolores E. López, José de Anchieta de Castro e Horta-Júnior

Published in: Brain Structure and Function | Issue 8/2017

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Abstract

The noradrenergic locus coeruleus (LC) plays an important role in the promotion and maintenance of arousal and alertness. Our group recently described coerulean projections to cochlear root neurons (CRNs), the first relay of the primary acoustic startle reflex (ASR) circuit. However, the role of the LC in the ASR and its modulation, prepulse inhibition (PPI), is not clear. In this study, we damaged LC neurons and fibers using a highly selective neurotoxin, DSP-4, and then assessed ASR and PPI in male and female rats. Our results showed that ASR amplitude was higher in males at 14 days after DSP-4 injection when compared to pre-administration values and those in the male control group. Such modifications in ASR amplitude did not occur in DSP-4-injected females, which exhibited ASR amplitude within the range of control values. PPI differences between males and females seen in controls were not observed in DSP-4-injected rats for any interstimulus interval tested. DSP-4 injection did not affect ASR and PPI latencies in either the male or the female groups, showing values that were consistent with the sex-related variability observed in control rats. Furthermore, we studied the noradrenergic receptor system in the cochlear nerve root using gene expression analysis. When compared to controls, DSP-4-injected males showed higher levels of expression in all adrenoceptor subtypes; however, DSP-4-injected females showed varied effects depending on the receptor type, with either up-, downregulations, or maintenance of expression levels. Lastly, we determined noradrenaline levels in CRNs and other LC-targeted areas using HPLC assays, and these results correlated with behavioral and adrenoceptor expression changes post DSP-4 injection. Our study supports the participation of LC in ASR and PPI, and contributes toward a better understanding of sex-related differences observed in somatosensory gating paradigms.
Literature
go back to reference Aasen I, Kolli L, Kumari V (2005) Sex effects in prepulse inhibition and facilitation of the acoustic startle response: implications for pharmacological and treatment studies. J Psychopharmacol 19(1):39–45PubMedCrossRef Aasen I, Kolli L, Kumari V (2005) Sex effects in prepulse inhibition and facilitation of the acoustic startle response: implications for pharmacological and treatment studies. J Psychopharmacol 19(1):39–45PubMedCrossRef
go back to reference Adams LM, Geyer MA (1981) Effects of 6-hydroxydopamine lesions of locus coeruleus on startle in rats. Psychopharmacology (Berl) 73(4):394–398CrossRef Adams LM, Geyer MA (1981) Effects of 6-hydroxydopamine lesions of locus coeruleus on startle in rats. Psychopharmacology (Berl) 73(4):394–398CrossRef
go back to reference Alsene KM, Bakshi VP (2011) Pharmacological stimulation of locus coeruleus reveals a new antipsychotic-responsive pathway for deficient sensorimotor gating. Neuropsychopharmacology 36(8):1656–1667PubMedPubMedCentralCrossRef Alsene KM, Bakshi VP (2011) Pharmacological stimulation of locus coeruleus reveals a new antipsychotic-responsive pathway for deficient sensorimotor gating. Neuropsychopharmacology 36(8):1656–1667PubMedPubMedCentralCrossRef
go back to reference Asakura M, Nagashima H, Fujii S, Sasuga Y, Misonoh A, Hasegawa H, Osada K (2000) Influences of chronic stress on central nervous systems. Nihon Shinkei Seishin Yakurigaku Zasshi 20(3):97–105PubMed Asakura M, Nagashima H, Fujii S, Sasuga Y, Misonoh A, Hasegawa H, Osada K (2000) Influences of chronic stress on central nervous systems. Nihon Shinkei Seishin Yakurigaku Zasshi 20(3):97–105PubMed
go back to reference Aston-Jones G, Bloom FE (1981) Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in sleep-waking cycle. J Neurosci 1(8):876–886PubMed Aston-Jones G, Bloom FE (1981) Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in sleep-waking cycle. J Neurosci 1(8):876–886PubMed
go back to reference Aston-Jones G, George P (2004) Chap. 11: Locus Coeruleus, A5 and A7 Noradrenergic Cell Groups. In: The rat nervous system Third(Edn), Academic Press, Burlington, pp 259–294CrossRef Aston-Jones G, George P (2004) Chap. 11: Locus Coeruleus, A5 and A7 Noradrenergic Cell Groups. In: The rat nervous system Third(Edn), Academic Press, Burlington, pp 259–294CrossRef
go back to reference Aston-Jones G, Akaoka H, Charléty P, Chouvet G (1991) Serotonin selectively attenuates glutamate-evoked activation of noradrenergic locus coeruleus neurons. J Neurosci 11(3):760–769PubMed Aston-Jones G, Akaoka H, Charléty P, Chouvet G (1991) Serotonin selectively attenuates glutamate-evoked activation of noradrenergic locus coeruleus neurons. J Neurosci 11(3):760–769PubMed
go back to reference Aston-Jones G, Rajkowski J, Cohen J (1999) Role of locus coeruleus in attention and behavioral flexibility. Biol Psychiatry 46(9):1309–1320 (Review)PubMedCrossRef Aston-Jones G, Rajkowski J, Cohen J (1999) Role of locus coeruleus in attention and behavioral flexibility. Biol Psychiatry 46(9):1309–1320 (Review)PubMedCrossRef
go back to reference Bakker MJ, van Dijk JG, van den Maagdenberg AM, Tijssen MA (2006) Startle syndromes. Lancet Neurol 5(6):513–524 (Review)PubMedCrossRef Bakker MJ, van Dijk JG, van den Maagdenberg AM, Tijssen MA (2006) Startle syndromes. Lancet Neurol 5(6):513–524 (Review)PubMedCrossRef
go back to reference Bangasser DA, Zhang X, Garachh V, Hanhauser E, Valentino RJ (2011) Sexual dimorphism in locus coeruleus dendritic morphology: a structural basis for sex differences in emotional arousal. Physiol Behav 103(3–4):342–351PubMedPubMedCentralCrossRef Bangasser DA, Zhang X, Garachh V, Hanhauser E, Valentino RJ (2011) Sexual dimorphism in locus coeruleus dendritic morphology: a structural basis for sex differences in emotional arousal. Physiol Behav 103(3–4):342–351PubMedPubMedCentralCrossRef
go back to reference Baudrie V, Tulen JH, Blanc J, Elghozi JL (1997) Autonomic components of the cardiovascular responses to an acoustic startle stimulus in rats. J Auton Pharmacol 17(5):303–309PubMedCrossRef Baudrie V, Tulen JH, Blanc J, Elghozi JL (1997) Autonomic components of the cardiovascular responses to an acoustic startle stimulus in rats. J Auton Pharmacol 17(5):303–309PubMedCrossRef
go back to reference Bell RL, Rodd ZA, Hsu CC, Lumeng L, Murphy JM, McBride WJ (2003) Amphetamine-modified acoustic startle responding and prepulse inhibition in adult and adolescent alcohol-preferring and -nonpreferring rats. Pharmacol Biochem Behav 75(1):163–171PubMedCrossRef Bell RL, Rodd ZA, Hsu CC, Lumeng L, Murphy JM, McBride WJ (2003) Amphetamine-modified acoustic startle responding and prepulse inhibition in adult and adolescent alcohol-preferring and -nonpreferring rats. Pharmacol Biochem Behav 75(1):163–171PubMedCrossRef
go back to reference Berridge CW, Abercrombie ED (1999) Relationship between locus coeruleus discharge rates and rates of norepinephrine release within neocortex as assessed by in vivo microdialysis. Neuroscience 93(4):1263–1270PubMedCrossRef Berridge CW, Abercrombie ED (1999) Relationship between locus coeruleus discharge rates and rates of norepinephrine release within neocortex as assessed by in vivo microdialysis. Neuroscience 93(4):1263–1270PubMedCrossRef
go back to reference Booze RM, Hall JA, Cress NM, Miller GD, Davis JN (1988) DSP-4 treatment produces abnormal tyrosine hydroxylase immunoreactive fibers in rat hippocampus. Exp Neurol 101(1):75–86PubMedCrossRef Booze RM, Hall JA, Cress NM, Miller GD, Davis JN (1988) DSP-4 treatment produces abnormal tyrosine hydroxylase immunoreactive fibers in rat hippocampus. Exp Neurol 101(1):75–86PubMedCrossRef
go back to reference Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254PubMedCrossRef Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254PubMedCrossRef
go back to reference Braff DL, Geyer MA (1990) Sensorimotor gating and schizophrenia. Human and animal model studies. Arch Gen Psychiatry 47(2):181–188PubMedCrossRef Braff DL, Geyer MA (1990) Sensorimotor gating and schizophrenia. Human and animal model studies. Arch Gen Psychiatry 47(2):181–188PubMedCrossRef
go back to reference Braff D, Stone C, Callaway E, Geyer M, Glick I, Bali L (1978) Prestimulus effects on human startle reflex in normals and schizophrenics. Psychophysiology 15(4):339–343PubMedCrossRef Braff D, Stone C, Callaway E, Geyer M, Glick I, Bali L (1978) Prestimulus effects on human startle reflex in normals and schizophrenics. Psychophysiology 15(4):339–343PubMedCrossRef
go back to reference Braff DL, Geyer MA, Swerdlow NR (2001) Human studies of prepulse inhibition of startle: normal subjects, patient groups, and pharmacological studies. Psychopharmacology (Berl) 156(2–3):234–258CrossRef Braff DL, Geyer MA, Swerdlow NR (2001) Human studies of prepulse inhibition of startle: normal subjects, patient groups, and pharmacological studies. Psychopharmacology (Berl) 156(2–3):234–258CrossRef
go back to reference Burns MJ, Nixon GJ, Foy CA, Harris N (2005) Standardisation of data from real-time quantitative PCR methods—evaluation of outliers and comparison of calibration curves. BMC Biotechnol 7(5):31. doi:10.1186/1472-6750-5-31 CrossRef Burns MJ, Nixon GJ, Foy CA, Harris N (2005) Standardisation of data from real-time quantitative PCR methods—evaluation of outliers and comparison of calibration curves. BMC Biotechnol 7(5):31. doi:10.​1186/​1472-6750-5-31 CrossRef
go back to reference Bylund DB (1992) Subtypes of alpha 1- and alpha 2-adrenergic receptors. FASEB J 6(3):832–839 (Review)PubMed Bylund DB (1992) Subtypes of alpha 1- and alpha 2-adrenergic receptors. FASEB J 6(3):832–839 (Review)PubMed
go back to reference Carasso BS, Bakshi VP, Geyer MA (1998) Disruption in prepulse inhibition after alpha-1 adrenoceptor stimulation in rats. Neuropharmacology 37(3):401–404PubMedCrossRef Carasso BS, Bakshi VP, Geyer MA (1998) Disruption in prepulse inhibition after alpha-1 adrenoceptor stimulation in rats. Neuropharmacology 37(3):401–404PubMedCrossRef
go back to reference Cooper JR, Bloom FE, Roth RH (2003) The biochemical basis of neuropharmacology, 6th edn. Oxford U., Oxford Cooper JR, Bloom FE, Roth RH (2003) The biochemical basis of neuropharmacology, 6th edn. Oxford U., Oxford
go back to reference Couto LlB, Moroni CRr, Ferreira ClMdR, Elias-Filho DH, Parada CAl, Pelao IR, Coimbra NC (2006) Descriptive and functional neuroanatomy of locus coeruleus-noradrenaline-containing neurons involvement in bradykinin-induced antinociception on principal sensory trigeminal nucleus. J Chem Neuroanat 32(1):28–45CrossRef Couto LlB, Moroni CRr, Ferreira ClMdR, Elias-Filho DH, Parada CAl, Pelao IR, Coimbra NC (2006) Descriptive and functional neuroanatomy of locus coeruleus-noradrenaline-containing neurons involvement in bradykinin-induced antinociception on principal sensory trigeminal nucleus. J Chem Neuroanat 32(1):28–45CrossRef
go back to reference Davis M, Commissaris RL, Yang S, Wagner KR, Kehne JH, Cassella JV, Boulis NM (1989) Spinal vs. supraspinal sites of action of the alpha-2-adrenergic agonists clonidine and ST-91 on the acoustic startle reflex. Pharmacol Biochem Behav 33(1):233–240PubMedCrossRef Davis M, Commissaris RL, Yang S, Wagner KR, Kehne JH, Cassella JV, Boulis NM (1989) Spinal vs. supraspinal sites of action of the alpha-2-adrenergic agonists clonidine and ST-91 on the acoustic startle reflex. Pharmacol Biochem Behav 33(1):233–240PubMedCrossRef
go back to reference Dong L-W, Yang J, Tong L-J, Tang C, Liu M-S (1999) Transcriptional regulation of alpha-1-adrenoceptor gene in the rat liver during different phases of sepsis. Biochim Biophys Acta Mol Basis Dis 1453(2):207–215.CrossRef Dong L-W, Yang J, Tong L-J, Tang C, Liu M-S (1999) Transcriptional regulation of alpha-1-adrenoceptor gene in the rat liver during different phases of sepsis. Biochim Biophys Acta Mol Basis Dis 1453(2):207–215.CrossRef
go back to reference Fendt M, Li L, Yeomans JS (2001) Brain stem circuits mediating prepulse inhibition of the startle reflex. Psychopharmacology (Berl) 156(2–3):216–224CrossRef Fendt M, Li L, Yeomans JS (2001) Brain stem circuits mediating prepulse inhibition of the startle reflex. Psychopharmacology (Berl) 156(2–3):216–224CrossRef
go back to reference Foote SL, Aston-Jones G, Bloom FE (1980) Impulse activity of locus coeruleus neurons in awake rats and monkeys is a function of sensory stimulation and arousal. Proc Natl Acad Sci USA 77(5):3033–3037PubMedPubMedCentralCrossRef Foote SL, Aston-Jones G, Bloom FE (1980) Impulse activity of locus coeruleus neurons in awake rats and monkeys is a function of sensory stimulation and arousal. Proc Natl Acad Sci USA 77(5):3033–3037PubMedPubMedCentralCrossRef
go back to reference Fritschy JM, Grzanna R (1989) Immunohistochemical analysis of the neurotoxic effects of DSP-4 identifies two populations of noradrenergic axon terminals. Neuroscience 30(1):181–197PubMedCrossRef Fritschy JM, Grzanna R (1989) Immunohistochemical analysis of the neurotoxic effects of DSP-4 identifies two populations of noradrenergic axon terminals. Neuroscience 30(1):181–197PubMedCrossRef
go back to reference Fritschy JM, Grzanna R, Pompeiano CDBaO (1991) Chapter 20 Selective effects of DSP-4 on locus coeruleus axons: are there pharmacologically different types of noradrenergic axons in the central nervous system? In: Progress in brain research, Elsevier, Amsterdam, pp 257–268 Fritschy JM, Grzanna R, Pompeiano CDBaO (1991) Chapter 20 Selective effects of DSP-4 on locus coeruleus axons: are there pharmacologically different types of noradrenergic axons in the central nervous system? In: Progress in brain research, Elsevier, Amsterdam, pp 257–268
go back to reference Funk GD, Parkis MA, Selvaratnam SR, Robinson DM, Miles GB, Peebles KC (2000) Synaptic control of motoneuron excitability inrodents:from monthstomilliseconds. Clin Exp Pharmacol Physiol 27:120–125PubMedCrossRef Funk GD, Parkis MA, Selvaratnam SR, Robinson DM, Miles GB, Peebles KC (2000) Synaptic control of motoneuron excitability inrodents:from monthstomilliseconds. Clin Exp Pharmacol Physiol 27:120–125PubMedCrossRef
go back to reference Gómez-Nieto R, Rubio ME, López DE (2008a) Cholinergic input from the ventral nucleus of the trapezoid body to cochlear root neurons in rats. J Comp Neurol 506(3):452–468PubMedCrossRef Gómez-Nieto R, Rubio ME, López DE (2008a) Cholinergic input from the ventral nucleus of the trapezoid body to cochlear root neurons in rats. J Comp Neurol 506(3):452–468PubMedCrossRef
go back to reference Gómez-Nieto R, Horta-Junior JAC, Castellano O, Herrero-Turrión MJ, Rubio ME, López DE (2008b) Neurochemistry of the afferents to the rat cochlear root nucleus: Possible synaptic modulation of the acoustic startle. Neuroscience 154(1):51–64PubMedPubMedCentralCrossRef Gómez-Nieto R, Horta-Junior JAC, Castellano O, Herrero-Turrión MJ, Rubio ME, López DE (2008b) Neurochemistry of the afferents to the rat cochlear root nucleus: Possible synaptic modulation of the acoustic startle. Neuroscience 154(1):51–64PubMedPubMedCentralCrossRef
go back to reference Gómez-Nieto R, Horta-Junior JAC, Castellano O, Sinex DG, López DE (2010) Auditory prepulse inhibition of neuronal activity in the rat cochlear root nucleus. In: López-Poveda EA, Palmer AR, Meddis R (eds.) The neurophysiological bases of auditory perception, pp 79–90 Gómez-Nieto R, Horta-Junior JAC, Castellano O, Sinex DG, López DE (2010) Auditory prepulse inhibition of neuronal activity in the rat cochlear root nucleus. In: López-Poveda EA, Palmer AR, Meddis R (eds.) The neurophysiological bases of auditory perception, pp 79–90
go back to reference Gómez-Nieto R, Sinex DG, C Horta-Junior JD, Castellano O, Herrero-Turrion JM, López DE (2014b) A fast cholinergic modulation of the primary acoustic startle circuit in rats. Brain Struct Funct 219(5):1555–1573. doi:10.1007/s00429-013-0585-8.PubMed Gómez-Nieto R, Sinex DG, C Horta-Junior JD, Castellano O, Herrero-Turrion JM, López DE (2014b) A fast cholinergic modulation of the primary acoustic startle circuit in rats. Brain Struct Funct 219(5):1555–1573. doi:10.​1007/​s00429-013-0585-8.PubMed
go back to reference Grant SJ, Aston-Jones G, Redmond DE Jr (1988) Responses of primate locus coeruleus neurons to simple and complex sensory stimuli. Brain Res Bull 21(3):401–410PubMedCrossRef Grant SJ, Aston-Jones G, Redmond DE Jr (1988) Responses of primate locus coeruleus neurons to simple and complex sensory stimuli. Brain Res Bull 21(3):401–410PubMedCrossRef
go back to reference Grzanna R, Berger U, Fritschy JM, Geffard M (1989) Acute action of DSP-4 on central norepinephrine axons: biochemical and immunohistochemical evidence for differential effects. J Histochem Cytochem 37(9):1435–1442PubMedCrossRef Grzanna R, Berger U, Fritschy JM, Geffard M (1989) Acute action of DSP-4 on central norepinephrine axons: biochemical and immunohistochemical evidence for differential effects. J Histochem Cytochem 37(9):1435–1442PubMedCrossRef
go back to reference Guimaraes S, Moura D (2001) Vascular adrenoceptors: an update. Pharmacol Rev 53(2):319–356PubMed Guimaraes S, Moura D (2001) Vascular adrenoceptors: an update. Pharmacol Rev 53(2):319–356PubMed
go back to reference Heal DJ, Butler SA, Prow MR, Buckett WR (1993) Quantification of presynaptic alpha-2-adrenoceptors in rat brain after short-term DSP-4 lesioning. Eur J Pharmacol 249(1):37–41PubMedCrossRef Heal DJ, Butler SA, Prow MR, Buckett WR (1993) Quantification of presynaptic alpha-2-adrenoceptors in rat brain after short-term DSP-4 lesioning. Eur J Pharmacol 249(1):37–41PubMedCrossRef
go back to reference Heckman CJ, Mottram C, Quinlan K, Theiss R, Schuster J (2009) Motoneuron excitability: the importance of neuromodulatory inputs. Clin Neurophysiol 120:2040–2054PubMedCrossRef Heckman CJ, Mottram C, Quinlan K, Theiss R, Schuster J (2009) Motoneuron excitability: the importance of neuromodulatory inputs. Clin Neurophysiol 120:2040–2054PubMedCrossRef
go back to reference Hoffman HS, Ison JR (1980) Reflex modification in the domain of startle: I. Some empirical findings and their implications for how the nervous system processes sensory input. Psychol Rev 87(2):175–189PubMedCrossRef Hoffman HS, Ison JR (1980) Reflex modification in the domain of startle: I. Some empirical findings and their implications for how the nervous system processes sensory input. Psychol Rev 87(2):175–189PubMedCrossRef
go back to reference Hormigo S, Gómez-Nieto R, Castellano O, Herrero-Turrion MJ, López DE, E Horta, Junior JdAdC (2015) The noradrenergic projection from the locus coeruleus to the cochlear root neurons in rats. Brain Struct Funct, 220(3):1477–1496. doi:10.1007/s00429-014-0739-3 PubMedCrossRef Hormigo S, Gómez-Nieto R, Castellano O, Herrero-Turrion MJ, López DE, E Horta, Junior JdAdC (2015) The noradrenergic projection from the locus coeruleus to the cochlear root neurons in rats. Brain Struct Funct, 220(3):1477–1496. doi:10.​1007/​s00429-014-0739-3 PubMedCrossRef
go back to reference Huang H-P, Zhu F-P, Chen X-W, Xu Z-QD, Zhang CX, Zhou Z (2012) Physiology of quantal norepinephrine release from somatodendritic sites of neurones in locus coeruleus. Front Mol Neurosci 5:1–5. doi:10.3389/fnmol.2012.00029 CrossRef Huang H-P, Zhu F-P, Chen X-W, Xu Z-QD, Zhang CX, Zhou Z (2012) Physiology of quantal norepinephrine release from somatodendritic sites of neurones in locus coeruleus. Front Mol Neurosci 5:1–5. doi:10.​3389/​fnmol.​2012.​00029 CrossRef
go back to reference Jones BE (1991) Noradrenergic locus coeruleus neurons: their distant connections and their relationship to neighboring (including cholinergic and GABAergic) neurons of the central gray and reticular formation. Prog Brain Res 88:15–30PubMedCrossRef Jones BE (1991) Noradrenergic locus coeruleus neurons: their distant connections and their relationship to neighboring (including cholinergic and GABAergic) neurons of the central gray and reticular formation. Prog Brain Res 88:15–30PubMedCrossRef
go back to reference Jonsson G, Hallman H, Ponzio F, Ross S (1981) DSP4 (N-(2-chloroethyl)-N-ethyl-2-bromobenzylamine—a useful denervation tool for central and peripheral noradrenaline neurons. Eur J Pharmacol 72(2–3):173–188PubMedCrossRef Jonsson G, Hallman H, Ponzio F, Ross S (1981) DSP4 (N-(2-chloroethyl)-N-ethyl-2-bromobenzylamine—a useful denervation tool for central and peripheral noradrenaline neurons. Eur J Pharmacol 72(2–3):173–188PubMedCrossRef
go back to reference Kable JW, Murrin LC, Bylund DB (2000) In vivo gene modification elucidates subtype-specific functions of alpha(2)-adrenergic receptors. J Pharmacol Exp Ther 293(1):1–7PubMed Kable JW, Murrin LC, Bylund DB (2000) In vivo gene modification elucidates subtype-specific functions of alpha(2)-adrenergic receptors. J Pharmacol Exp Ther 293(1):1–7PubMed
go back to reference Keay KA, Redgrave P, Dean P (1988) Cardiovascular and respiratory changes elicited by stimulation of rat superior colliculus. Brain Res Bull 20(1):13–26PubMedCrossRef Keay KA, Redgrave P, Dean P (1988) Cardiovascular and respiratory changes elicited by stimulation of rat superior colliculus. Brain Res Bull 20(1):13–26PubMedCrossRef
go back to reference Klepper A, Herbert H (1991) Distribution and origin of noradrenergic and serotonergic fibers in the cochlear nucleus and inferior colliculus of the rat. Brain Res 557(1–2):190–201PubMedCrossRef Klepper A, Herbert H (1991) Distribution and origin of noradrenergic and serotonergic fibers in the cochlear nucleus and inferior colliculus of the rat. Brain Res 557(1–2):190–201PubMedCrossRef
go back to reference Landis C, Hunt WA (1939) The startle pattern. Ferrar & Rinehart, New York Landis C, Hunt WA (1939) The startle pattern. Ferrar & Rinehart, New York
go back to reference Lee Y, López DE, Meloni EG, Davis M (1996) A primary acoustic startle pathway: obligatory role of cochlear root neurons and the nucleus reticularis pontis caudalis. J Neurosci 16(11):3775–3789PubMed Lee Y, López DE, Meloni EG, Davis M (1996) A primary acoustic startle pathway: obligatory role of cochlear root neurons and the nucleus reticularis pontis caudalis. J Neurosci 16(11):3775–3789PubMed
go back to reference Lehmann J, Pryce CR, Feldon J (1999) Sex differences in the acoustic startle response and prepulse inhibition in Wistar rats. Behav Brain Res 104(1–2):113–117PubMedCrossRef Lehmann J, Pryce CR, Feldon J (1999) Sex differences in the acoustic startle response and prepulse inhibition in Wistar rats. Behav Brain Res 104(1–2):113–117PubMedCrossRef
go back to reference Li F, De Godoy Mr, Rattan S (2004) Role of adenylate and guanylate cyclases in beta1-, beta2-, and beta3-adrenoceptor-mediated relaxation of internal anal sphincter smooth muscle. J Pharmacol Exp Ther 308(3):1111–1120PubMedCrossRef Li F, De Godoy Mr, Rattan S (2004) Role of adenylate and guanylate cyclases in beta1-, beta2-, and beta3-adrenoceptor-mediated relaxation of internal anal sphincter smooth muscle. J Pharmacol Exp Ther 308(3):1111–1120PubMedCrossRef
go back to reference Li L, Du Y, Li N, Wu X, Wu Y (2009) Top-down modulation of prepulse inhibition of the startle reflex in humans and rats. Neurosci Biobehav 33(8):1157–1167.CrossRef Li L, Du Y, Li N, Wu X, Wu Y (2009) Top-down modulation of prepulse inhibition of the startle reflex in humans and rats. Neurosci Biobehav 33(8):1157–1167.CrossRef
go back to reference Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2alpha-CT method. Methods 25(4):402–408PubMedCrossRef Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2alpha-CT method. Methods 25(4):402–408PubMedCrossRef
go back to reference Logue MP, Growdon JH, Coviella ILG, Wurtman RJ (1985) Differential effects of DSP-4 administration on regional brain norepinephrine turnover in rats. Life Sci 37(5):403–409PubMedCrossRef Logue MP, Growdon JH, Coviella ILG, Wurtman RJ (1985) Differential effects of DSP-4 administration on regional brain norepinephrine turnover in rats. Life Sci 37(5):403–409PubMedCrossRef
go back to reference López DE, Saldana E, Nodal FR, Merchán MA, Warr WB (1999) Projections of cochlear root neurons, sentinels of the auditory pathway in the rat. J Comp Neurol 415(2):160–174PubMedCrossRef López DE, Saldana E, Nodal FR, Merchán MA, Warr WB (1999) Projections of cochlear root neurons, sentinels of the auditory pathway in the rat. J Comp Neurol 415(2):160–174PubMedCrossRef
go back to reference Ma S, Mifflin SW, Cunningham JT, Morilak DA (2008) Chronic intermittent hypoxia sensitizes acute hypothalamic-pituitary adrenal stress reactivity and Fos induction in the rat locus coeruleus in response to subsequent immobilization stress. Neuroscience 154(4):1639–1647PubMedPubMedCentralCrossRef Ma S, Mifflin SW, Cunningham JT, Morilak DA (2008) Chronic intermittent hypoxia sensitizes acute hypothalamic-pituitary adrenal stress reactivity and Fos induction in the rat locus coeruleus in response to subsequent immobilization stress. Neuroscience 154(4):1639–1647PubMedPubMedCentralCrossRef
go back to reference Martire M, Pistritto G, Mores N, Agnati LF, Fuxe K (1995) Presynaptic A2-adrenoceptors and neuropeptide Y Y2 receptors inhibit [3H]noradrenaline release from rat hypothalamic synaptosomes via different mechanisms. Neurosci Lett 188(1):9–12PubMedCrossRef Martire M, Pistritto G, Mores N, Agnati LF, Fuxe K (1995) Presynaptic A2-adrenoceptors and neuropeptide Y Y2 receptors inhibit [3H]noradrenaline release from rat hypothalamic synaptosomes via different mechanisms. Neurosci Lett 188(1):9–12PubMedCrossRef
go back to reference Miao-Kun S (1995) Central neural organization and control of sympathetic nervous system in mammals. Prog Neurobiol 47(3):157–233CrossRef Miao-Kun S (1995) Central neural organization and control of sympathetic nervous system in mammals. Prog Neurobiol 47(3):157–233CrossRef
go back to reference Molina V, Montes C, Tamayo P, Villa R, Isabel Osuna M, Perez J, Sancho C, López-Albuquerque T, Cardoso A, Castellano O, López DE (2009) Correlation between prepulse inhibition and cortical perfusion during an attentional test in schizophrenia. A pilot study. Prog Neuropsychopharmacol Biol Psychiatry 33(1):53–61PubMedCrossRef Molina V, Montes C, Tamayo P, Villa R, Isabel Osuna M, Perez J, Sancho C, López-Albuquerque T, Cardoso A, Castellano O, López DE (2009) Correlation between prepulse inhibition and cortical perfusion during an attentional test in schizophrenia. A pilot study. Prog Neuropsychopharmacol Biol Psychiatry 33(1):53–61PubMedCrossRef
go back to reference Mulders WH, Robertson D (2001) Origin of the noradrenergic innervation of the superior olivary complex in the rat. J Chem Neuroanat 21(4):313–322PubMedCrossRef Mulders WH, Robertson D (2001) Origin of the noradrenergic innervation of the superior olivary complex in the rat. J Chem Neuroanat 21(4):313–322PubMedCrossRef
go back to reference Noga BR, Johnson DM, Riesgo MI, Pinzon A (2011) Locomotor-activated neuronsof the cat. II. Noradrenergic innervation and colocalization with NEα1a and NEα2b receptors in the thoraco-lumbar spinal cord. J Neurophysiol 105(4):1835–1849PubMedPubMedCentralCrossRef Noga BR, Johnson DM, Riesgo MI, Pinzon A (2011) Locomotor-activated neuronsof the cat. II. Noradrenergic innervation and colocalization with NEα1a and NEα2b receptors in the thoraco-lumbar spinal cord. J Neurophysiol 105(4):1835–1849PubMedPubMedCentralCrossRef
go back to reference Page ME, Akaoka H, Aston-Jones G, Valentino RJ (1992) Bladder distention activates noradrenergic locus coeruleus neurons by an excitatory amino acid mechanism. Neuroscience 51(3):555–563PubMedCrossRef Page ME, Akaoka H, Aston-Jones G, Valentino RJ (1992) Bladder distention activates noradrenergic locus coeruleus neurons by an excitatory amino acid mechanism. Neuroscience 51(3):555–563PubMedCrossRef
go back to reference Paxinos G, Watson C (2005) The rat brain in stereotaxic coordinates: the new coronal set—161 diagrams, 5th edn. Academic Press, San Diego Paxinos G, Watson C (2005) The rat brain in stereotaxic coordinates: the new coronal set—161 diagrams, 5th edn. Academic Press, San Diego
go back to reference Pinos H, Collado P, Rodriguez-Zafra M, Rodriguez C, Segovia S, Guillamon A (2001) The development of sex differences in the locus coeruleus of the rat. Brain Res Bull 56(1):73–78PubMedCrossRef Pinos H, Collado P, Rodriguez-Zafra M, Rodriguez C, Segovia S, Guillamon A (2001) The development of sex differences in the locus coeruleus of the rat. Brain Res Bull 56(1):73–78PubMedCrossRef
go back to reference Rosario LA, Abercrombie ED (1999) Individual differences in behavioral reactivity: correlation with stress-induced norepinephrine efflux in the hippocampus of Sprague-Dawley rats. Brain Res Bull 48(6):595–602PubMedCrossRef Rosario LA, Abercrombie ED (1999) Individual differences in behavioral reactivity: correlation with stress-induced norepinephrine efflux in the hippocampus of Sprague-Dawley rats. Brain Res Bull 48(6):595–602PubMedCrossRef
go back to reference Ross SB (1985) DSP4 and behavioural experiments. Trends Pharmacol Sci 6:237–237CrossRef Ross SB (1985) DSP4 and behavioural experiments. Trends Pharmacol Sci 6:237–237CrossRef
go back to reference Ross SB, Johansson JG, Lindborg B, Dahlbom R (1973) Cyclizing compounds. I. Tertiary N-(2-bromobenzyl)-N-haloalkylamines with adrenergic blocking action. Acta Pharm Suec 10(1):29–42PubMed Ross SB, Johansson JG, Lindborg B, Dahlbom R (1973) Cyclizing compounds. I. Tertiary N-(2-bromobenzyl)-N-haloalkylamines with adrenergic blocking action. Acta Pharm Suec 10(1):29–42PubMed
go back to reference Sallinen J, Haapalinna A, Viitamaa T, Kobilka BK, Scheinin M (1998) d-amphetamine and l-5-hydroxytryptophan-induced behaviours in mice with genetically-altered expression of the alpha-2C-adrenergic receptor subtype. Neuroscience 86(3):959–965PubMedCrossRef Sallinen J, Haapalinna A, Viitamaa T, Kobilka BK, Scheinin M (1998) d-amphetamine and l-5-hydroxytryptophan-induced behaviours in mice with genetically-altered expression of the alpha-2C-adrenergic receptor subtype. Neuroscience 86(3):959–965PubMedCrossRef
go back to reference Sara SJ, Segal M (1991) Plasticity of sensory responses of locus coeruleus neurons in the behaving rat: implications for cognition. Prog Brain Res 88:571–585PubMedCrossRef Sara SJ, Segal M (1991) Plasticity of sensory responses of locus coeruleus neurons in the behaving rat: implications for cognition. Prog Brain Res 88:571–585PubMedCrossRef
go back to reference Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3(6):1101–1108PubMedCrossRef Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3(6):1101–1108PubMedCrossRef
go back to reference Singewald N, Zhou G-Y, Schneider C (1995) Release of excitatory and inhibitory amino acids from the locus coeruleus of conscious rats by cardiovascular stimuli and various forms of acute stress. Brain Res 704(1):42–50PubMedCrossRef Singewald N, Zhou G-Y, Schneider C (1995) Release of excitatory and inhibitory amino acids from the locus coeruleus of conscious rats by cardiovascular stimuli and various forms of acute stress. Brain Res 704(1):42–50PubMedCrossRef
go back to reference Stevens DR, McCarley RW, Greene RW (1994) The mechanism of noradrenergic alpha 1 excitatory modulation of pontine reticular formation neurons. J Neurosci 14(11 Pt 1):6481–6487PubMed Stevens DR, McCarley RW, Greene RW (1994) The mechanism of noradrenergic alpha 1 excitatory modulation of pontine reticular formation neurons. J Neurosci 14(11 Pt 1):6481–6487PubMed
go back to reference Sullivan RM, Wilson DA, Lemon C, Gerhardt GA (1994) Bilateral 6-OHDA lesions of the locus coeruleus impair associative olfactory learning in newborn rats. Brain Res 643(1–2):306–309PubMedCrossRef Sullivan RM, Wilson DA, Lemon C, Gerhardt GA (1994) Bilateral 6-OHDA lesions of the locus coeruleus impair associative olfactory learning in newborn rats. Brain Res 643(1–2):306–309PubMedCrossRef
go back to reference Swaminath G, Lee TW, Kobilka B (2003) Identification of an allosteric binding site for Zn2+ on the beta-2 adrenergic receptor. J Biol Chem 278(1):352–356PubMedCrossRef Swaminath G, Lee TW, Kobilka B (2003) Identification of an allosteric binding site for Zn2+ on the beta-2 adrenergic receptor. J Biol Chem 278(1):352–356PubMedCrossRef
go back to reference Swerdlow NR, Geyer MA (1998) Using an animal model of deficient sensorimotor gating to study the pathophysiology and new treatments of schizophrenia. Schizophr Bull 24(2):285–301PubMedCrossRef Swerdlow NR, Geyer MA (1998) Using an animal model of deficient sensorimotor gating to study the pathophysiology and new treatments of schizophrenia. Schizophr Bull 24(2):285–301PubMedCrossRef
go back to reference Swerdlow NR, Braff DL, Geyer MA (2000) Animal models of deficient sensorimotor gating: what we know, what we think we know, and what we hope to know soon. Behav Pharmacol 11(3–4):185–204PubMedCrossRef Swerdlow NR, Braff DL, Geyer MA (2000) Animal models of deficient sensorimotor gating: what we know, what we think we know, and what we hope to know soon. Behav Pharmacol 11(3–4):185–204PubMedCrossRef
go back to reference Swerdlow NR, Hanlon FM, Henning L, Kim YK, Gaudet I, Halim ND (2001) Regulation of sensorimotor gating in rats by hippocampal NMDA: anatomical localization. Brain Res 898(2):195–203 (PubMed PMID: 11306005)PubMedCrossRef Swerdlow NR, Hanlon FM, Henning L, Kim YK, Gaudet I, Halim ND (2001) Regulation of sensorimotor gating in rats by hippocampal NMDA: anatomical localization. Brain Res 898(2):195–203 (PubMed PMID: 11306005)PubMedCrossRef
go back to reference Szabadi E (2013) Functional neuroanatomy of the central noradrenergic system. J Psychopharmacol 27(8):659–693PubMedCrossRef Szabadi E (2013) Functional neuroanatomy of the central noradrenergic system. J Psychopharmacol 27(8):659–693PubMedCrossRef
go back to reference Szot P, Miguelez C, White SS, Franklin A, Sikkema C, Wilkinson CW, Ugedo L, Raskind MA (2010) A comprehensive analysis of the effect of DSP4 on the locus coeruleus noradrenergic system in the rat. Neuroscience 166(1):279–291PubMedPubMedCentralCrossRef Szot P, Miguelez C, White SS, Franklin A, Sikkema C, Wilkinson CW, Ugedo L, Raskind MA (2010) A comprehensive analysis of the effect of DSP4 on the locus coeruleus noradrenergic system in the rat. Neuroscience 166(1):279–291PubMedPubMedCentralCrossRef
go back to reference Valentino RJ, Van Bockstaele E (2008) Convergent regulation of locus coeruleus activity as an adaptive response to stress. Eur J Pharmacol 583(2–3):194–203PubMedPubMedCentralCrossRef Valentino RJ, Van Bockstaele E (2008) Convergent regulation of locus coeruleus activity as an adaptive response to stress. Eur J Pharmacol 583(2–3):194–203PubMedPubMedCentralCrossRef
go back to reference Valentino RJ, Foote SL, Aston-Jones G (1983) Corticotropin-releasing factor activates noradrenergic neurons of the locus coeruleus. Brain Res 270(2):363–367PubMedCrossRef Valentino RJ, Foote SL, Aston-Jones G (1983) Corticotropin-releasing factor activates noradrenergic neurons of the locus coeruleus. Brain Res 270(2):363–367PubMedCrossRef
go back to reference Valls-Sole J (2012) Assessment of excitability in brainstem circuits mediating the blink reflex and the startle reaction. Clin Neurophysiol 123(1):13–20PubMedCrossRef Valls-Sole J (2012) Assessment of excitability in brainstem circuits mediating the blink reflex and the startle reaction. Clin Neurophysiol 123(1):13–20PubMedCrossRef
go back to reference Valls-Solé J (1998) Acustic and somatosensory prepulse modulation of the blink reflex and the startle reaction. In: Brainstem reflexes and functions. Litofinter, S.A, Madrid, pp 119–131 Valls-Solé J (1998) Acustic and somatosensory prepulse modulation of the blink reflex and the startle reaction. In: Brainstem reflexes and functions. Litofinter, S.A, Madrid, pp 119–131
go back to reference Vicentic A, Robeva A, Rogge G, Uberti M, Minneman KP (2002) Biochemistry and pharmacology of epitope-tagged alpha-1-adrenergic receptor subtypes. J Pharmacol Exp Ther 302(1):58–65PubMedCrossRef Vicentic A, Robeva A, Rogge G, Uberti M, Minneman KP (2002) Biochemistry and pharmacology of epitope-tagged alpha-1-adrenergic receptor subtypes. J Pharmacol Exp Ther 302(1):58–65PubMedCrossRef
go back to reference Wamsley JK, Alburges ME, Hunt MAE, Bylund DB (1992) Differential localization of alpha-2-adrenergic receptor subtypes in brain. Pharmacol Biochem Behav 41(2):267–273PubMedCrossRef Wamsley JK, Alburges ME, Hunt MAE, Bylund DB (1992) Differential localization of alpha-2-adrenergic receptor subtypes in brain. Pharmacol Biochem Behav 41(2):267–273PubMedCrossRef
go back to reference Yeomans JS, Frankland PW (1995) The acoustic startle reflex: neurons and connections. Brain Res Brain Res Rev 21(3):301–314PubMedCrossRef Yeomans JS, Frankland PW (1995) The acoustic startle reflex: neurons and connections. Brain Res Brain Res Rev 21(3):301–314PubMedCrossRef
go back to reference Yeomans JS, Lee J, Yeomans MH, Steidl S, Li L (2006) Midbrain pathways for prepulse inhibition and startle activation in rat. Neuroscience 142(4):921–929PubMedCrossRef Yeomans JS, Lee J, Yeomans MH, Steidl S, Li L (2006) Midbrain pathways for prepulse inhibition and startle activation in rat. Neuroscience 142(4):921–929PubMedCrossRef
Metadata
Title
Morphological correlates of sex differences in acoustic startle response and prepulse inhibition through projections from locus coeruleus to cochlear root neurons
Authors
Sebastian Hormigo
Ricardo Gómez-Nieto
Consuelo Sancho
Javier Herrero-Turrión
Juan Carro
Dolores E. López
José de Anchieta de Castro e Horta-Júnior
Publication date
01-11-2017
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 8/2017
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-017-1415-1

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