Biological Cybernetics

, Volume 106, Issue 3, pp 169–176 | Cite as

A computational model for the modulation of the prepulse inhibition of the acoustic startle reflex

  • David Fernando Ramirez-Moreno
  • Terrence Joseph Sejnowski
Original Paper

Abstract

The acoustic startle reflex (ASR), a defensive response, is a contraction of the skeletal and facial muscles in response to an abrupt, intense (> 80 db) auditory stimulus, which has been extensively studied in rats and humans. Prepulse inhibition (PPI) of ASR is the normal suppression of the startle reflex when an intense stimulus is preceded by a weak non-starting pre-stimulus. PPI, a measure of sensory motor gating, is impaired in various neuropsychiatric disorders, including schizophrenia, and is modulated by cognitive and emotional contexts such as fear and attention. We have modeled the fear modulation of PPI of ASR based on its anatomical substrates and taking into account data from behaving rats and humans. The model replicates the principal features of both phenomena and predicts underlying neural mechanisms. In addition, the model yields testable predictions.

Keywords

Acoustic startle reflex Prepulse inhibition Fear modulation PPI computational model 

Abbreviations

ASR

Acoustic startle reflex

PPI

Prepulse inhibition

C

Cochlea

CRN

Cochlear root nucleus

NRPC

Nucleus reticularis pontine caudalis

MN

Motor neuron

IC

Inferior colliculus

SC

Superior colliculus

PTN

Pontine tegmental nucleus

AM

Amygdala

MOD

Modulatory structure

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bast T et al (2001) Hyperactivity, decreased startle reactivity, and disrupted prepulse inhibition following disinhibition of the rat ventral hippocampus by the GABAA receptor antagonist picrotoxin. Psychopharmacology 156(2–3): 225–233PubMedCrossRefGoogle Scholar
  2. Braff DL et al (2001) Human studies of prepulse inhibition of startle: normal subjects, patient groups, and pharmacological studies. Psychopharmacology (Berl) 156: 234–258CrossRefGoogle Scholar
  3. Davis M (2006) Neural systems involved in fear and anxiety measured with fear—potentiated startle. Am Psychol 61: 741–756PubMedCrossRefGoogle Scholar
  4. Depoortere R et al (1997) Potentiation of prepulse inhibition of the startle reflex in rats: pharmacological evaluation of the procedure as a model for detecting antipsychotic activity. Psycopharmacology (Berl) 132(4): 366–374CrossRefGoogle Scholar
  5. Fendt M et al (2001) Brain stem circuits mediating prepulse inhibition of the startle reflex. Psychopharmacology 156: 216–224PubMedCrossRefGoogle Scholar
  6. Geyer MA et al (2001) Pharmacological studies of prepulse inhibition models of sensorimotor-gating deficits in schizophrenia: a decade in review. Psychopharmacology 156: 117–154PubMedCrossRefGoogle Scholar
  7. Grillon C (1998) Effect of darkness on acoustic startle in Vietnam veterans with PTSD. Am J Psychiatry 155: 812–817PubMedGoogle Scholar
  8. Grillon C et al (1997) Darkness facilitates the acoustic startle reflex in humans. Biol Psychiatry 42(6): 453–460PubMedCrossRefGoogle Scholar
  9. Heekeren K et al (2004) Attentional modulation of prepulse inhibition: a new startle paradigm. Neuropsychobiology 49: 88–93PubMedCrossRefGoogle Scholar
  10. 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: 175–189PubMedCrossRefGoogle Scholar
  11. Hoffman HS, Searle JL (1965) Acoustic variables in the modification of startle reaction in the rat. J Comp Physiol Psychol 60(1): 53–58PubMedCrossRefGoogle Scholar
  12. Ishii D et al (2010) Enhancement of acoustic prepulse inhibition by contextual fear conditioning in mice is maintained even after contextual fear extinction. Prog Neuropsychopharmacol Biol Psychiatry 34: 183–188PubMedCrossRefGoogle Scholar
  13. Iversen S et al (2000) Emotional states and feelings. In: Kandel E, Schwartz JH, Jessell TM (eds) Principles of neuroscience, 4th edn. McGraw-Hill, New York, pp 982–998Google Scholar
  14. Koch M (1999) The neurobiology of startle. Prog Neurobiol 59: 107–128PubMedCrossRefGoogle Scholar
  15. Koch M et al (1992) Loss of the acoustic startle response following neurotoxic lesions of the caudal pontine reticular formation: possible role of giant neurons. Neuroscience 49: 617–625PubMedCrossRefGoogle Scholar
  16. Koch M et al (1997) The acoustic startle response in rats—circuits mediating evocation, inhibition and potentiation. Behav Brain Res 89: 35–49PubMedCrossRefGoogle Scholar
  17. Lang PJ et al (1990) Emotion, attention, and the startle reflex. Psychol Rev 97: 377–395PubMedCrossRefGoogle Scholar
  18. Lang PJ, Davis M, Ohman A (2000) Fear and anxiety: animal models and human cognitive psychophysiology. J Affect Disord 61: 137–159PubMedCrossRefGoogle Scholar
  19. Lapicque L (1907) Recherches quantitatives sur l’excitation électrique des nerfs traitée comme une polarisation. J Physiol Pathol Gen 9: 620–635Google Scholar
  20. Lee Y et al (1996) A primary acoustic startle reflex pathway: obligatory role of cochlear root neurons and the nucleus reticularis pontis caudalis. J Neurosci 16(11): 3775–3789PubMedGoogle Scholar
  21. Leitner DS et al (1985) Role of the inferior colliculus in the inhibition of acoustic startle in the rat. Physiol Behav 34: 65–70PubMedCrossRefGoogle Scholar
  22. Leumann L et al (2001) A neural network approach to the acoustic startle reflex and prepulse inhibition. Brain Res Bull 56(2): 101–110PubMedCrossRefGoogle Scholar
  23. Li L et al (1998) Prepulse inhibition following lesions of the inferior colliculus: prepulse intensity functions. Physiol Behav 65: 133–139PubMedCrossRefGoogle Scholar
  24. Li L et al (2009) Top-down modulations of prepulse inhibition of the startle reflex in humans and rats. Neurosci Behav Rev 33: 1157–1167CrossRefGoogle Scholar
  25. Naka KI, Rushton WAH (1966) S-potentials from luminosity units in the retina of fish (Cyprinidae). J Physiol 185:587–599Google Scholar
  26. Plappert C, Pilz P, Schnitzler H (2004) Factors governing prepulse inhibition and prepulse facilitation of the acoustic startle response in mice. Behav Brain Res 152: 403–412PubMedCrossRefGoogle Scholar
  27. Schmajuk NA et al (2006) Startle and prepulse inhibition as a function of background noise: a computational and experimental analysis. Behav Brain Res 170: 182–196PubMedCrossRefGoogle Scholar
  28. Shepherd GM (2004) Introduction to synaptic circuits. In: Shepherd GM (ed) The synaptic organization of the brain, 5th edn. Oxford University Press, OxfordGoogle Scholar
  29. Swerdlow NR, Geyer MA (1993) Prepulse inhibition of acoustic startle in rats after lesions of the pedunculopontine tegmental nucleus. Behav Neurosci 107: 104–117PubMedCrossRefGoogle Scholar
  30. Swerdlow NR, Caine SB, Braff DL, Geyer MA (1992) The neural substrates of sensorimotor gating of the startle reflex: a review of recent findings and their implications. Psychopharmacology 6: 176–190CrossRefGoogle Scholar
  31. Swerdlow NR et al (2001) Neural circuit regulation of prepulse inhibition of startle in the rat: current knowledge and future challenges. Psychopharmacology 156: 194–215PubMedCrossRefGoogle Scholar
  32. Vogt BA (2005) Pain and emotion interactions in subregions of the cingulated gyrus. Nat Rev Neurosci 6: 533–544PubMedCrossRefGoogle Scholar
  33. Wilson C (2004) Basal ganglia. In: Shepherd G (ed) The synaptic organization of the brain, 5th edn. Oxford Press, Oxford, pp 361–415Google Scholar
  34. Winslow JT, Parr LA, Davis M (2002) Acoustic startle, prepulse inhibition, and fear-potentiated startle measured in rhesus monkeys. Biol Psychiatry 51: 859–866PubMedCrossRefGoogle Scholar
  35. Yeomans JS et al (2006) Midbrain pathways for prepulse inhibition and startle activation in rats. Neuroscience 142: 921–929PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • David Fernando Ramirez-Moreno
    • 1
  • Terrence Joseph Sejnowski
    • 2
    • 3
  1. 1.Departamento de FísicaUniversidad Autonoma de OccidenteCaliColombia
  2. 2.Computational Neurobiology Laboratory, Howard Hughes Medical Institute, Salk InstituteLa JollaUSA
  3. 3.Division of Biological SciencesUniversity of California San DiegoLa JollaUSA

Personalised recommendations