Abstract
Rationale
Under some conditions, external sensory noise enhances cognitive functions, a phenomenon possibly involving stochastic resonance and/or enhanced central dopamine transmission. Prepulse inhibition (PPI) of the startle reflex is a robust measure of sensorimotor gating and can be modulated by activity in the cortex and basal ganglia, including the central dopamine pathways.
Objectives
Previous empirical studies suggest a differential effect of acoustic noise in normal children and children with attention-deficit hyperactivity disorder (ADHD). This study investigated the effect of acoustic noise on PPI and if dopamine transmission interacts with acoustic noise effects in a rat ADHD model.
Methods
The effect of background acoustic noise on acoustic startle response and PPI were measured with a constant prepulse to background noise ratio of 9 dB(A). Spontaneously hypertensive (SH) rats were used as the ADHD model and compared with Wistar and Sprague–Dawley rats. Microdialysis, methylphenidate treatment and 6-OHDA lesions were used to investigate interaction with dopamine transmission.
Results
Background noise facilitated PPI differently in SH rats and controls. The prefrontal cortex in SH rats had low basal dopamine concentrations, a high DOPAC/dopamine ratio and blunted dopamine release during PPI testing. Methylphenidate had small, but strain-specific, effects on startle and PPI. Bilateral 6-hydroxydopamine lesions did not alter startle or PPI.
Conclusions
Prefrontal dopamine transmission is altered in SH rats during the sensorimotor gating task of PPI of the acoustic startle, indicating increased dopamine reuptake in this ADHD rat model. We propose that noise benefit could be explored as a non-pharmacological alternative for treating neuropsychiatric disorders.
Similar content being viewed by others
Abbreviations
- ADHD:
-
Attention-deficit hyperactivity disorder
- PPI:
-
Prepulse inhibition
- DA:
-
Dopamine
- DAT:
-
Dopamine transporter
- SH:
-
Spontaneously hypertensive
References
Bergquist F, Ludwig M, Dutia MB (2008) Role of the commissural inhibitory system in vestibular compensation in the rat. J Physiol 586:4441–4452
Bialek W, Rieke F (1992) Reliability and information transmission in spiking neurons. Trends Neurosci 15:428–434
Braff D, Geyer M, Swerdlow N (2001) Human studies of prepulse inhibition of startle: normal subjects, patient groups, and pharmacological studies. Psychopharmacol Berl 156:234–258
Carboni E, Silvagni A, Valentini V, Di Chiara G (2003) Effect of amphetamine, cocaine and depolarization by high potassium on extracellular dopamine in the nucleus accumbens shell of SHR rats. An in vivo microdialysis study. Neurosci Biobehav Rev 27:653–659
Castellanos FX, Fine EJ, Kaysen D, Marsh WL, Rapoport JL, Hallett M (1996) Sensorimotor gating in boys with Tourette’s syndrome and ADHD: preliminary results. Biol Psychiatry 39:33–41
Cheon K, Ryu YH, Kim Y, Namkoong K, Kim C, Lee JD (2003) Dopamine transporter density in the basal ganglia assessed with [123I]IPT SPET in children with attention deficit hyperactivity disorder. Eur J Nucl Med Mol Imaging 30:306–311
Cragg SJ, Rice ME (2004) DAncing past the DAT at a DA synapse. Trends Neurosci 27:270–277
Csomor PA, Yee BK, Vollenweider FX, Feldon J, Nicolet T, Quednow BB (2008) On the influence of baseline startle reactivity on the indexation of prepulse inhibition. Behav Neurosci 122:885–900
DasBanerjee T, Middleton FA, Berger DF, Lombardo JP, Sagvolden T, Faraone SV (2008) A comparison of molecular alterations in environmental and genetic rat models of ADHD: a pilot study. Am J Med Genet B Neuropsychiatr Genet 147B:1554–1563
Davids E, Zhang K, Tarazi FI, Baldessarini RJ (2003) Animal models of attention-deficit hyperactivity disorder. Brain Res Rev 42:1–21
Davis M, Mansbach RS, Swerdlow NR, Campeau S, Braff DL, Geyer MA (1990) Apomorphine disrupts the inhibition of acoustic startle induced by weak prepulses in rats. Psychopharmacology 102:1–4
Dougherty D, Bonab A, Spencer TJ, Rauch SL, Madras BK, Fischman AJ (1999) Dopamine transporter density in patients with attention deficit hyperactivity disorder. Lancet 354:2132–2133
Dresel S, Krause J, Krause KH, LaFougere C, Brinkbaumer K, Kung HF, Hahn K, Tatsch K (2000) Attention deficit hyperactivity disorder: binding of [(TC)-T-99 m]TRODAT-1 to the dopamine transporter before and after methylphenidate treatment. Eur J Nucl Med Mol Imaging 27:1518–1524
Faraone S, Perlis R, Doyle A, Smoller J, Goralnick J, Holmgren M, Sklar P (2005) Molecular genetics of attention-deficit/hyperactivity disorder. Biol Psychiatry 57:1313–1323
Feifel D, Minassian A, Perry W (2009) Prepulse inhibition of startle in adults with ADHD. J Psychiatr Res 43:484–489
Fejgin K, Pålsson E, Wass C, Finnerty N, Lowry J, Klamer D (2009) Prefrontal GABA(B) receptor activation attenuates phencyclidine-induced impairments of prepulse inhibition: involvement of nitric oxide. Neuropsychopharmacol 34:1673–1684
Flaten MA, Nordmark E, Elden A (2005) Effects of background noise on the human startle reflex and prepulse inhibition. Psychophysiology 42:298–305
Franklin JC, Moretti NA, Blumenthal TD (2007) Impact of stimulus signal-to-noise ratio on prepulse inhibition of acoustic startle. Psychophysiology 44:339–342
Gewirtz JC, Davis M (1995) Habituation of prepulse inhibition of the startle reflex using an auditory prepulse close to background noise. Behav Neurosci 109:388–395
Ghosh A, Rho Y, McIntosh AR, Kötter R, Jirsa VK, Friston KJ (2008) Noise during rest enables the exploration of the brain’s dynamic repertoire. PLoS Comput Biol 4:e1000196
Glowa J, Hansen C (1994) Differences in response to an acoustic startle stimulus among forty-six rat strains. Behav Genet 24:79–84
Hänggi P (2002) Stochastic resonance in biology how noise can enhance detection of weak signals and help improve biological information processing. Chemphyschem 3:285–290
Hanlon M, Karayanidis F, Schall U (2009) Intact sensorimotor gating in adult attention deficit hyperactivity disorder. Int J Neuropsychopharmacol 12:701–707
Hawk LW, Yartz AR, Pelham WE, Lock TM (2003) The effects of methylphenidate on prepulse inhibition during attended and ignored prestimuli among boys with attention-deficit hyperactivity disorder. Psychopharmacol Berl 165:118–127
Heal D, Smith S, Kulkarni R, Rowley H (2008) New perspectives from microdialysis studies in freely moving, spontaneously hypertensive rats on the pharmacology of drugs for the treatment of ADHD. Pharmacol Biochem Behav 90:184–197
Hoenig K, Hochrein A, Quednow BB, Maier W, Wagner M (2005) Impaired prepulse inhibition of acoustic startle in obsessive-compulsive disorder. Biol Psychiatry 57:1153–1158
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 87:175–189
Kinkead B, Selz KA, Owens MJ, Mandell AJ (2006) Algorithmically designed peptides ameliorate behavioral defects in animal model of ADHD by an allosteric mechanism. J Neurosci Meth 151:68–81
Kosko B (2006) Noise. Viking Press, New York
Krause K, Dresel SH, Krause J, la Fougere C, Ackenheil M (2003) The dopamine transporter and neuroimaging in attention deficit hyperactivity disorder. Neurosci Biobehav Rev 27:605–613
Larisch R, Sitte W, Antke C, Nikolaus S, Franz M, Tress W, Müller H (2006) Striatal dopamine transporter density in drug naive patients with attention-deficit/hyperactivity disorder. Nucl Med Commun 27:267–270
Li S, von Oertzen T, Lindenberger U (2006) A neurocomputational model of stochastic resonance and aging. Neurocomputing 69:1553–1560
Lindgren HS, Andersson DR, Lagerkvist S, Nissbrandt H, Cenci MA (2010) l-DOPA-induced dopamine efflux in the striatum and the substantia nigra in a rat model of Parkinson's disease: temporal and quantitative relationship to the expression of dyskinesia. J Neurochem 112:1465–1476
Manjarrez E, Mendez I, Martinez L, Flores A, Mirasso C (2007) Effects of auditory noise on the psychophysical detection of visual signals: cross-modal stochastic resonance. Neurosci Lett 415:231–236
McDonnell MD, Abbott D (2009) What is stochastic resonance? Definitions, misconceptions, debates, and its relevance to biology. PLoS Comput Biol 5:e1000348
Moss F, Ward L, Sannita W (2004) Stochastic resonance and sensory information processing: a tutorial and review of application. Clin Neurophysiol 115:267–281
Ornitz EM, Hanna GL, Detraversay J (1992) Prestimulation-induced startle modulation in attention-deficit hyperactiviy disorder and nocturnal enuresis. Psychophysiology 29:437–451
Pan W, Soma R, Kwak S, Yamamoto Y (2008) Improvement of motor functions by noisy vestibular stimulation in central neurodegenerative disorders. J Neurol 255:1657–1661
Perry W, Minassian A, Lopez B, Maron L, Lincoln A (2007) Sensorimotor gating deficits in adults with autism. Biol Psychiatry 61:482–486
Prince J (2008) Catecholamine dysfunction in attention-deficit/hyperactivity disorder: an update. J Clin Psychopharmacol 28(3 Suppl 2):S39–S35
Priplata A et al (2006) Noise-enhanced balance control in patients with diabetes and patients with stroke. Ann Neurol 59:4–12
Rodríguez M, Barroso-Chinea P, Abdala P, Obeso J, González-Hernández T (2001) Dopamine cell degeneration induced by intraventricular administration of 6-hydroxydopamine in the rat: similarities with cell loss in Parkinson’s disease. Exp Neurol 169:163–181
Russell VA (2007) Reprint of “Neurobiology of animal models of attention-deficit hyperactivity disorder”. J Neurosci Meth 166:I–XIV
Sagvolden T, Pettersen M, Larsen M (1993) Spontaneously hypertensive rats (SHR) as a putative animal model of childhood hyperkinesis: SHR behavior compared to four other rat strains. Physiol Behav 54:1047–1055
Sagvolden T, Russell VA, Aase H, Johansen EB, Farshbaf M (2005) Rodent models of attention-deficit/hyperactivity disorder. Biol Psychiatry 57:1239–1247
Sagvolden T et al (2009) The spontaneously hypertensive rat model of ADHD—the importance of selecting the appropriate reference strain. Neuropharmacology 57:619–626
Sandner G, Canal NM (2007) Relationship between PPI and baseline startle response. Cogn Neurodyn 27:37
Schmajuk N, Larrauri J, Hagenbuch N, Levin E, Feldon J, Yee B (2006) Startle and prepulse inhibition as a function of background noise: a computational and experimental analysis. Behav Brain Res 170:182–196
Sikström S, Söderlund G (2007) Stimulus-dependent dopamine release in attention-deficit/hyperactivity disorder. Psychol Rev 114:1047–1075
Simonotto E et al (1999) fMRI studies of visual cortical activity during noise stimulation. Neurocomputing 26-27:511–516
Söderlund G, Sikström S, Smart A (2007) Listen to the noise: noise is beneficial for cognitive performance in ADHD. J Child Psychol Psychiatry 48:840–847
Söderlund G, Sikström S, Loftesnes JM, Sonuga-Barke EJ (2010) The effects of background white noise on memory performance in inattentive school children. Behav Brain Funct 6:55
Spencer TJ et al (2007) Further evidence of dopamine transporter dysregulation in adhd: a controlled pet imaging study using altropane. Biol Psychiatry 62:1059–1061
Stein RB, Gossen ER, Jones KE (2005) Neuronal variability: noise or part of the signal? Nat Rev Neurosci 6:389–397
Swerdlow N, Weber M, Qu Y, Light G, Braff D (2008) Realistic expectations of prepulse inhibition in translational models for schizophrenia research. Psychopharmacol Berl 199:331–388
Thompson TL, Moss RL (1997) Modulation of mesolimbic dopaminergic activity over the rat estrous cycle. Neurosci Lett 229:145–148
Timmerman W, Westerink B (1997) Brain microdialysis of GABA and glutamate: what does it signify? Synapse 27:242–261
Usher M, Feingold M (2000) Stochastic resonance in the speed of memory retrieval. Biol Cybern 83:L11–L16
Van den Buuse M (2004) Prepulse inhibition of acoustic startle in spontaneously hypertensive rats. Behav Brain Res 154:331–337
Vendruscolo L, Terenina-Rigaldie E, Raba F, Ramos A, Takahashi R, Mormede P (2006) A QTL on rat chromosome 7 modulates prepulse inhibition, a neuro-behavioral trait of ADHD, in a Lewis x SHR intercross. Behav Brain Funct 2:21
Volkow ND et al (2009) Evaluating dopamine reward pathway in ADHD: clinical implications. JAMA 302:1084–1091
Watanabe Y, Fujita M, Ito Y, Okada T, Kusuoka H, Nishimura T (1997) Brain dopamine transporter in spontaneously hypertensive rats. J Nucl Med 38:470–474
Wells C, Ward LM, Chua R, Timothy Inglis J (2005) Touch noise increases vibrotactile sensitivity in old and young. Psychol Sci 16:313–320
Westlund KN, Krakower TJ, Kwan S, Abell CW (1993) Intracellular distribution of monoamine oxidase A in selected regions of rat and monkey brain and spinal cord. Brain Res 612:221–230
Wilkinson D, Nicholls S, Pattenden C, Kilduff P, Milberg W (2008) Galvanic vestibular stimulation speeds visual memory recall. Exp Brain Res 189:243–248
Yamamoto Y, Struzik ZR, Soma R, Ohashi K, Kwak S (2005) Noisy vestibular stimulation improves autonomic and motor responsiveness in central neurodegenerative disorders. Ann Neurol 58:175–181
Yu XL, Lewis ER (1989) Studies with spike initiators: linearization by noise allows continuous signal modulation in neural networks. IEEE Trans Biomed Eng 36:36–43
Zeng FG, Fu QJ, Morse R (2000) Human hearing enhanced by noise. Brain Res 869:251–255
Acknowledgements
The Ethics Committee for Animal Experiments, Gothenburg, Sweden, approved all experimental procedures. Housing, handling and procedures complied with national Swedish law, principles of laboratory animal care and the European Communities Council Directive of November 24, 1986. The study was supported by the Swedish Research Council, grant VR 421-2007-2479, Parkinsonfonden and Svenska läkaresällskapet (the Swedish Medical Association).
Potential conflicts of interest
None.
Author information
Authors and Affiliations
Corresponding author
Additional information
An erratum to this article can be found at http://dx.doi.org/10.1007/s00213-010-2135-x
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Pålsson, E., Söderlund, G., Klamer, D. et al. Noise benefit in prepulse inhibition of the acoustic startle reflex. Psychopharmacology 214, 675–685 (2011). https://doi.org/10.1007/s00213-010-2074-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00213-010-2074-6