Pharmacological studies of prepulse inhibition models of sensorimotor gating deficits in schizophrenia: a decade in review

Geyer, Mark A.; Krebs-Thomson, Kirsten; Braff, David L.; Swerdlow, Neal R.

doi:10.1007/s002130100811

Cited by 1,484Schizophrenia research and treatmentNeurotransmitter Receptor Influence on BehaviorNeuroscience and Neuropharmacology Research

Pharmacological studies of prepulse inhibition models of sensorimotor gating deficits in schizophrenia: a decade in review

Geyer, Mark A., Krebs-Thomson, Kirsten, Braff, David L., Swerdlow, Neal R.·2001·Psychopharmacology

DOI 10.1007/s002130100811

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Abstract

Rationale Patients with schizophrenia exhibit deficits in an operational measure of sensorimotor gating: prepulse inhibition (PPI) of startle. Similar deficits in PPI are produced in rats by pharmacological or developmental manipulations. These experimentally induced PPI deficits in rats are clearly not animal models of schizophrenia per se, but appear to provide models of sensorimotor gating deficits in schizophrenia patients that have face, predictive, and construct validity. In rodents, disruptions in PPI of startle are produced by: stimulation of D2 dopamine (DA) receptors, produced by amphetamine or apomorphine; activation of serotonergic systems, produced by serotonin (5-HT) releasers or direct agonists at multiple serotonin receptors; and blockade of N-methyl-D-aspartate (NMDA) receptors, produced by drugs such as phencyclidine (PCP). Accordingly, dopaminergic, serotonergic, and glutamatergic models of disrupted PPI have evolved and have been applied to the identification of potential antipsychotic treatments. In addition, some developmental manipulations, such as isolation rearing, have provided non-pharmacological animal models of the PPI deficits seen in schizophrenia.Objective This review summarizes and evaluates studies assessing the effects of systemic drug administrations on PPI in rats.Methods Studies examining systemic drug effects on PPI in rats prior to January 15, 2001 were compiled and organized into six annotated appendices. Based on this catalog of studies, the specific advantages and disadvantages of each of the four main PPI models used in the study of antipsychotic drugs were critically evaluated.Results Despite some notable inconsistencies, the literature provides strong support for significant disruptions in PPI in rats produced by DA agonists, 5-HT2 agonists, NMDA antagonists, and isolation rearing. Each of these models exhibits sensitivity to at least some antipsychotic medications. While the PPI model based on the effects of direct DA agonists is the most well-validated for the identification of known antipsychotics, the isolation rearing model also appears to be sensitive to both typical and atypical antipsychotics. The 5-HT PPI model is less generally sensitive to antipsychotic medications, but can provide insight into the contribution of serotonergic systems to the actions of newer antipsychotics that act upon multiple receptors. The deficits in PPI produced by NMDA antagonists appear to be more sensitive to clozapine-like atypical antipsychotics than to typical antipsychotics. Hence, despite some exceptions to this generalization, the NMDA PPI model might aid in the identification of novel or atypical antipsychotic medications.Conclusions Studies of drug effects on PPI in rats have generated four distinctive models that have utility in the identification of antipsychotic medications. Because each of these models has specific advantages and disadvantages, the choice of model to be used depends upon the question being addressed. This review should help to guide such decisions.

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Both apomorphine-induced and amphetamine-induced PPI disruptions in rats are blocked by DA D2 antagonists.
“both apomorphine-induced and amphetamine-induced PPI disruptions in rats are blocked by DA D2 antagonists [366].”
From Reward circuitry dysfunction in psychiatric and neurodevelopmental disorders and genetic syndromes: animal models and clinical findings (2012) · cites this paper as [366]
A weak tone initiates habituation of the reticular neurons' response to a successive louder tone, leading to prepulse inhibition of the acoustic startle response.
“A weak tone initiates habituation of the reticular neurons’ response to a successive louder tone, leading to the phenomenon of prepulse inhibition (PPI) of the acoustic startle response (7, 8).”
From Sensory Processing Dysfunction in the Personal Experience and Neuronal Machinery of Schizophrenia (2015) · cites this paper as [8]
For both PPI and P50 gating, despite the origin of the effect in reticular brain stem neurons, the response engages an entire network of brain circuits, the dopaminergic circuits of the basal ganglia for PPI and the basal cholinergic nuclei and cortex for P50 gating.
“For both PPI and P50 gating, despite the origin of the effect in reticular brain stem neurons, the response engages an entire network of brain circuits, the dopaminergic circuits of the basal ganglia for PPI and the basal cholinergic nuclei and cortex for P50 gating (8, 9).”
From Sensory Processing Dysfunction in the Personal Experience and Neuronal Machinery of Schizophrenia (2015) · cites this paper as [8]
Deficits in CHRNA7 null mutant mice for P50 gating and in NRG-1 null mutants for PPI have been reported.
“Deficits in CHRNA7 null mutant mice for P50 gating (32) and in NRG-1 null mutants for PPI have also been reported (8).”
From Sensory Processing Dysfunction in the Personal Experience and Neuronal Machinery of Schizophrenia (2015) · cites this paper as [8]
Increased dopaminergic neurotransmission from stimulants and psychotomimetic antagonists of NMDARs such as phencyclidine induce the PPI/P50 deficit pharmacologically.
“Increased dopaminergic neurotransmission from stimulants and psychotomimetic antagonists of NMDARs such as phencyclidine (PCP) induce the deficit pharmacologically (8).”
From Sensory Processing Dysfunction in the Personal Experience and Neuronal Machinery of Schizophrenia (2015) · cites this paper as [8]

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Dose and time response analysis of apomorphine's effect on prepulse inhibition of acoustic startle
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NMDA receptor antagonists acting at the glycine B site in rat models for antipsychotic-like activity
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Dissociation Between Startle and Prepulse Inhibition in Rats Exposed to γ Radiation at Day 15 of Embryogeny
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Subchronically applied phencyclidine fails to disrupt prepulse inhibition in rats
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Wadenberg, M.-L. G., Sills, T. L., Fletcher, P., et al. (2000) · Biological Psychiatry · doi:10.1016/s0006-3223(99)00267-x · Cited by 9 · see citing works

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Psychedelics
Nichols, D. E. (2016) · Pharmacological Reviews · doi:10.1124/pr.115.011478 · Cited by 1,762 · see citing works
The tail suspension test as a model for assessing antidepressant activity: Review of pharmacological and genetic studies in mice
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Behavioural and neurochemical effects of post-weaning social isolation in rodents—Relevance to developmental neuropsychiatric disorders
Fone, K. C. F., & Porkess, M. V. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.03.003 · Cited by 864 · see citing works
Realistic expectations of prepulse inhibition in translational models for schizophrenia research
Swerdlow, N. R., Weber, M., Qu, Y., Light, G. A., & Braff, D. L. (2008) · Psychopharmacology · doi:10.1007/s00213-008-1072-4 · Cited by 529 · see citing works
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Multiple mechanisms involved in the large-spectrum therapeutic potential of cannabidiol in psychiatric disorders
Campos, A. C., Moreira, F. A., Gomes, F. V., Del Bel, E. A., & Guimarães, F. S. (2012) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2011.0389 · Cited by 475 · see citing works
Behavioral phenotyping strategies for mutant mice
Crawley, J. N. (2008) · Neuron · doi:10.1016/j.neuron.2008.03.001 · Cited by 439 · see citing works
Convergence of biological and psychological perspectives on cognitive coordination in schizophrenia
Phillips, W. A., & Silverstein, S. M. (2003) · Behavioral and Brain Sciences · doi:10.1017/s0140525x03000025 · Cited by 445 · see citing works
Autism as a disorder of neural information processing: Directions for research and targets for therapy
Belmonte, M. K., Cook, E. H., Anderson, G. M., Rubenstein, J. L. R., Greenough, W. T., Beckel-Mitchener, A., Courchesne, E., Boulanger, L. M., Powell, S. B., Levitt, P. R., et al. (2004) · Molecular Psychiatry · doi:10.1038/sj.mp.4001499 · Cited by 442 · see citing works
Sensory Processing Dysfunction in the Personal Experience and Neuronal Machinery of Schizophrenia
Javitt, D. C., & Freedman, R. (2015) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2014.13121691 · Cited by 403 · see citing works
Startle Gating Deficits in a Large Cohort of Patients With Schizophrenia: Relationship to Medications, Symptoms, Neurocognition, and Level of Function
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Molecular aspects of glutamate dysregulation: implications for schizophrenia and its treatment
Konradi, C., & Heckers, S. (2003) · Pharmacology & Therapeutics · doi:10.1016/s0163-7258(02)00328-5 · Cited by 336 · see citing works
Removing Obstacles in Neuroscience Drug Discovery: The Future Path for Animal Models
Markou, A., Chiamulera, C., Geyer, M. A., Tricklebank, M., & Steckler, T. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2008.173 · Cited by 328 · see citing works
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Modeling madness in mice: one piece at a time
Arguello, P. A., & Gogos, J. A. (2006) · Neuron · doi:10.1016/j.neuron.2006.09.023 · Cited by 309 · see citing works
Reward circuitry dysfunction in psychiatric and neurodevelopmental disorders and genetic syndromes: animal models and clinical findings
Dichter, G. S., Damiano, C. A., & Allen, J. A. (2012) · Journal of Neurodevelopmental Disorders · doi:10.1186/1866-1955-4-19 · Cited by 299 · see citing works
Sensorimotor gating abnormalities in young males with fragile X syndrome and Fmr1-knockout mice.
Frankland, P. W., Wang, Y., Rosner, B., Shimizu, T., Balleine, B. W., Dykens, E. M., Ornitz, E. M., & Silva, A. J. (2004) · Molecular Psychiatry · doi:10.1038/sj.mp.4001432 · Cited by 275 · see citing works
Linking microcircuit dysfunction to cognitive impairment: Effects of disinhibition associated with schizophrenia in a cortical working memory model
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The 5-HT7 receptor and disorders of the nervous system: an overview
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Adolescent cannabis use and psychosis: epidemiology and neurodevelopmental models
Malone, D. T., Hill, M. N., & Rubino, T. (2010) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2010.00721.x · Cited by 237 · see citing works
Bupropion enhances brain reward function and reverses the affective and somatic aspects of nicotine withdrawal in the rat
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Prepulse inhibition and genetic mouse models of schizophrenia
Powell, S. B., Zhou, X., & Geyer, M. A. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.04.021 · Cited by 218 · see citing works
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The β3 Nicotinic Receptor Subunit: A Component of α-Conotoxin MII-Binding Nicotinic Acetylcholine Receptors that Modulate Dopamine Release and Related Behaviors
Cui, C., Booker, T. K., Allen, R. S., Grady, S. R., Whiteaker, P., Marks, M. J., Salminen, O., Tritto, T., Butt, C. M., Allen, W. R., et al. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-35-11045.2003 · Cited by 213 · see citing works
Cntnap4 differentially contributes to GABAergic and dopaminergic synaptic transmission
Karayannis, T., Au, E., Patel, J. C., Kruglikov, I., Markx, S., Delorme, R., Héron, D., Salomon, D., Glessner, J., Restituito, S., et al. (2014) · Nature · doi:10.1038/nature13248 · Cited by 183 · see citing works
Sub-chronic psychotomimetic phencyclidine induces deficits in reversal learning and alterations in parvalbumin-immunoreactive expression in the rat
Abdul-Monim, Z., Neill, J. C., & Reynolds, G. P. (2007) · Journal of Psychopharmacology · doi:10.1177/0269881107067097 · Cited by 206 · see citing works
What the Laboratory Rat has Taught us About Social Play Behavior: Role in Behavioral Development and Neural Mechanisms
Vanderschuren, L. J. M. J., & Trezza, V. (2013) · Current Topics in Behavioral Neurosciences · doi:10.1007/978-3-662-45758-0_268 · Cited by 200 · see citing works
Serotonin 5-HT7 receptor agents: structure-activity relationships and potential therapeutic applications in central nervous system disorders
Leopoldo, M., Lacivita, E., Berardi, F., Perrone, R., & Hedlund, P. B. (2011) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2010.08.013 · Cited by 198 · see citing works
Impaired sensorimotor gating in unmedicated adults with obsessive-compulsive disorder
Ahmari, S. E., Risbrough, V. B., Geyer, M. A., & Simpson, H. B. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2011.308 · Cited by 189 · see citing works
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Type III Neuregulin-1 Is Required for Normal Sensorimotor Gating, Memory-Related Behaviors, and Corticostriatal Circuit Components
Chen, Y.-J. J., Johnson, M. A., Lieberman, M. D., Goodchild, R. E., Schobel, S., Lewandowski, N., Rosoklija, G., Liu, R.-C., Gingrich, J. A., Small, S., et al. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1815-08.2008 · Cited by 188 · see citing works
Clozapine and Haloperidol Differently Suppress the MK-801-Increased Glutamatergic and Serotonergic Transmission in the Medial Prefrontal Cortex of the Rat
López-Gil, X., Babot, Z., Amargós-Bosch, M., Suñol, C., Artigas, F., & Adell, A. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301356 · Cited by 183 · see citing works
Glutamatergic Synaptic Dysregulation in Schizophrenia: Therapeutic Implications
Coyle, J. T., Basu, A., Benneyworth, M., Balu, D., & Konopaske, G. (2012) · Handbook of Experimental Pharmacology · doi:10.1007/978-3-642-25758-2_10 · Cited by 180 · see citing works
Influence of naturally occurring variations in maternal care on prepulse inhibition of acoustic startle and the medial prefrontal cortical dopamine response to stress in adult rats
Zhang, T. Y., Chrétien, P., Meaney, M. J., & Gratton, A. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.3293-04.2005 · Cited by 174 · see citing works
Current animal models of obsessive compulsive disorder: a critical review
Joel, D. (2006) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2005.11.006 · Cited by 168 · see citing works
The family of sensorimotor gating disorders: Comorbidities or diagnostic overlaps?
Geyer, M. A. (2006) · Neurotoxicity Research · doi:10.1007/bf03033358 · Cited by 159 · see citing works
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Translating cognition from animals to humans
Keeler, J. F., & Robbins, T. W. (2011) · Biochemical Pharmacology · doi:10.1016/j.bcp.2010.12.028 · Cited by 137 · see citing works
Reduced expression of the NMDA receptor-interacting protein SynGAP causes behavioral abnormalities that model symptoms of Schizophrenia
Guo, X., Hamilton, P. J., Reish, N. J., Sweatt, J. D., Miller, C. A., & Rumbaugh, G. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2008.223 · Cited by 120 · see citing works
Bayesian estimation of synaptic physiology from the spectral responses of neural masses
Moran, R. J., Stephan, K. E., Kiebel, S. J., Rombach, N., O'Connor, W. T., Murphy, K. J., Reilly, R. B., & Friston, K. J. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.01.025 · Cited by 126 · see citing works
Topographic pharmaco‐EEG mapping of the effects of the South American psychoactive beverage ayahuasca in healthy volunteers
Riba, J., Anderer, P., Morte, A., Urbano, G., Jané, F., Saletu, B., & Barbanoj, M. J. (2002) · British Journal of Clinical Pharmacology · doi:10.1046/j.1365-2125.2002.01609.x · Cited by 125 · see citing works
Perception Measurement in Clinical Trials of Schizophrenia: Promising Paradigms From CNTRICS
Green, M. F., Butler, P. D., Chen, Y., Geyer, M. A., Silverstein, S., Wynn, J. K., Yoon, J. H., & Zemon, V. (2009) · Schizophrenia Bulletin · doi:10.1093/schbul/sbn156 · Cited by 113 · see citing works
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Genetic contributions to behavioural diversity at the gene-environment interface
Bendesky, A., & Bargmann, C. I. (2011) · Nature Reviews Genetics · doi:10.1038/nrg3065 · Cited by 103 · see citing works
A Review of Oxytocin’s Effects on the Positive, Negative, and Cognitive Domains of Schizophrenia
Feifel, D., Shilling, P. D., & MacDonald, K. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.07.025 · Cited by 110 · see citing works
Dopamine D1 Rather than D2 Receptor Agonists Disrupt Prepulse Inhibition of Startle in Mice
Ralph-Williams, R. J., Lehmann-Masten, V., & Geyer, M. A. (2003) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300017 · Cited by 105 · see citing works
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The Selective Serotonin-2A Receptor Antagonist M100907 Reverses Behavioral Deficits in Dopamine Transporter Knockout Mice
Barr, A. M., Lehmann-Masten, V., Paulus, M., Gainetdinov, R. R., Caron, M. G., & Geyer, M. A. (2004) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300343 · Cited by 103 · see citing works
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Sleep deprivation disrupts prepulse inhibition and induces psychosis-like symptoms in healthy humans
Petrovsky, N., Ettinger, U., Hill, A., Frenzel, L., Meyhofer, I., Wagner, M., Backhaus, J., & Kumari, V. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0904-14.2014 · Cited by 102 · see citing works
Chronic reductions in serotonin transporter function prevent 5-HT1B-induced behavioral effects in mice
Shanahan, N. A., Holick Pierz, K. A., Masten, V. L., Waeber, C., Ansorge, M., Gingrich, J. A., Geyer, M. A., Hen, R., & Dulawa, S. C. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.09.026 · Cited by 102 · see citing works
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Epigenetic changes at gene promoters in response to immune activation in utero
Tang, B., Jia, H., Kast, R. J., & Thomas, E. A. (2013) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2013.01.086 · Cited by 91 · see citing works
Prepulse Inhibition and P50 Suppression Are Both Deficient but not Correlated in Schizophrenia Patients
Braff, D. L., Light, G. A., & Swerdlow, N. R. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.08.015 · Cited by 90 · see citing works
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The effects of methylphenidate on prepulse inhibition during attended and ignored prestimuli among boys with attention-deficit hyperactivity disorder
Hawk, L. W., Yartz, A. R., Pelham, W. E., & Lock, T. M. (2003) · Psychopharmacology · doi:10.1007/s00213-002-1235-7 · Cited by 89 · see citing works
Cannabidiol attenuates sensorimotor gating disruption and molecular changes induced by chronic antagonism of NMDA receptors in mice
Gomes, F. V., Issy, A. C., Ferreira, F. R., Viveros, M.-P., Del Bel, E. A., & Guimarães, F. S. (2015) · International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyu041 · Cited by 89 · see citing works
Glycine transport inhibitors in the treatment of schizophrenia
Javitt, D. C. (2012) · Handbook of experimental pharmacology · doi:10.1007/978-3-642-25758-2_12 · Cited by 83 · see citing works
Dopamine depletion of the nucleus accumbens reverses isolation-induced deficits in prepulse inhibition in rats
Powell, S. B., Geyer, M. A., Preece, M. A., Pitcher, L. K., Reynolds, G. P., & Swerdlow, N. R. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00122-2 · Cited by 82 · see citing works
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Negative and Nonemotional Interference with Visual Working Memory in Schizophrenia
Anticevic, A., Repovs, G., Corlett, P. R., & Barch, D. M. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.07.010 · Cited by 75 · see citing works
Cannabidiol effects in the prepulse inhibition disruption induced by amphetamine
Pedrazzi, J. F. C., Issy, A. C., Gomes, F. V., Guimarães, F. S., & Del-Bel, E. A. (2015) · Psychopharmacology · doi:10.1007/s00213-015-3945-7 · Cited by 76 · see citing works
Protein phosphatase 2a and glycogen synthase kinase 3 signaling modulate prepulse inhibition of the acoustic startle response by altering cortical M-type potassium channel activity
Kapfhamer, D., Berger, K. H., Hopf, F. W., Seif, T., Kharazia, V., Bonci, A., & Heberlein, U. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1292-10.2010 · Cited by 71 · see citing works
The potential role of lamotrigine in schizophrenia
Large, C. H., Webster, E. L., & Goff, D. C. (2005) · Psychopharmacology · doi:10.1007/s00213-005-0020-9 · Cited by 69 · see citing works
Behavioral and molecular evidence for psychotropic effects in l-theanine
Wakabayashi, C., Numakawa, T., Ninomiya, M., Chiba, S., & Kunugi, H. (2012) · Psychopharmacology · doi:10.1007/s00213-011-2440-z · Cited by 65 · see citing works
Selective Prefrontal Disinhibition in a Roving Auditory Oddball Paradigm Under N-Methyl-D-Aspartate Receptor Blockade
Rosch, R. E., Auksztulewicz, R., Leung, P. D., Friston, K. J., & Baldeweg, T. (2019) · Biological Psychiatry: Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2018.07.003 · Cited by 56 · see citing works
Epigenetic mechanisms underlying <scp>NMDA</scp> receptor hypofunction in the prefrontal cortex of juvenile animals in the <scp>MAM</scp> model for schizophrenia
Gulchina, Y., Xu, S., Snyder, M. A., Elefant, F., & Gao, W. (2017) · Journal of Neurochemistry · doi:10.1111/jnc.14101 · Cited by 56 · see citing works
Atypical antipsychotics clozapine and quetiapine attenuate prepulse inhibition deficits in dopamine transporter knockout mice
Powell, S. B., Young, J. W., Ong, J. C., Caron, M. G., & Geyer, M. A. (2008) · Behavioural Pharmacology · doi:10.1097/fbp.0b013e32830dc110 · Cited by 57 · see citing works
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Optogenetic Recruitment of Dorsal Raphe Serotonergic Neurons Acutely Decreases Mechanosensory Responsivity in Behaving Mice
Dugué, G. P., Lörincz, M. L., Lottem, E., Audero, E., Matias, S., Correia, P. A., Léna, C., & Mainen, Z. F. (2014) · PLoS ONE · doi:10.1371/journal.pone.0105941 · Cited by 54 · see citing works
Predictably irrational: assaying cognitive inflexibility in mouse models of schizophrenia
Brigman, J. L. (2010) · Frontiers in Neuroscience · doi:10.3389/neuro.01.013.2010 · Cited by 52 · see citing works
Maternal overnutrition induces long-term cognitive deficits across several generations
Sarker, G., & Peleg-Raibstein, D. (2018) · Nutrients · doi:10.3390/nu11010007 · Cited by 52 · see citing works
Schizophrenia risk gene CAV1 is both pro-psychotic and required for atypical antipsychotic drug actions in vivo
Allen, J. A., Yadav, P. N., Setola, V, Farrell, M., & Roth, B. L. (2011) · Translational Psychiatry · doi:10.1038/tp.2011.35 · Cited by 37 · see citing works
Selective pharmacological augmentation of hippocampal activity produces a sustained antidepressant-like response without abuse-related or psychotomimetic effects
Carreno, F. R., Collins, G. T., Frazer, A., & Lodge, D. J. (2017) · International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyx003 · Cited by 31 · see citing works
HTS and Rational Drug Design to Generate a Class of 5‐HT2C‐Selective Ligands for Possible Use in Schizophrenia.
Kozikowski, A. P., Cho, S. J., Jensen, N. H., Allen, J. A., Svennebring, A. M., & Roth, B. L. (2010) · ChemMedChem · doi:10.1002/cmdc.201000186 · Cited by 28 · see citing works
Mouse model of neurological complications resulting from encephalitic alphavirus infection
Ronca, S. E., Smith, J., Koma, T., Miller, M. M., Yun, N., Dineley, K. T., & Paessler, S. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.00188 · Cited by 22 · see citing works
Effect of <scp>L</scp>‐theanine on sensorimotor gating in healthy human subjects
Ota, M., Wakabayashi, C., Matsuo, J., Kinoshita, Y., Hori, H., Hattori, K., Sasayama, D., Teraishi, T., Obu, S., Ozawa, H., et al. (2014) · Psychiatry and Clinical Neurosciences · doi:10.1111/pcn.12134 · Cited by 16 · see citing works
Peripherally administered oxytocin modulates latent inhibition in a manner consistent with antipsychotic drugs
Feifel, D., Shilling, P. D., Hillman, J., Maisel, M., Winfield, J., & Melendez, G. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.10.023 · Cited by 13 · see citing works

On the feasibility to detect and to quantify prepulse-elicited reaction in prepulse inhibition of the acoustic startle reflex in humans
Csomor, P., Vollenweider, F. X., Feldon, J., & Yee, B. K. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.03.020 · Cited by 24 · see citing works
Acoustic prepulses can facilitate the startle reflex in rats: Discrepancy between rat and human data resolved
Reijmers, L. G. J. E., & Peeters, B. W. M. M. (1994) · Brain Research Bulletin · doi:10.1016/0361-9230(94)90110-4 · Cited by 14 · see citing works
Effects of acoustic prepulses on the startle reflex in rats: a parametric analysis
Reijmers, L. G. J. E., & Peeters, B. W. M. M. (1994) · Brain Research · doi:10.1016/0006-8993(94)91204-1 · Cited by 70 · see citing works
Distinct forms of prepulse inhibition disruption distinguishable by the associated changes in prepulse-elicited reaction
Yee, B. K., & Feldon, J. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.11.049 · Cited by 31 · see citing works
Prepulse inhibition of the acoustic startle reflex in pigs and its disruption by d-amphetamine
Lind, N. M., Arnfred, S., Hemmingsen, R., & Hansen, A. K. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.04.014 · Cited by 27 · see citing works

Authors: Geyer, M. A., Krebs-Thomson, K., Braff, D. L., & Swerdlow, N. R.
Affiliations: University of California San Diego (US)
ORCID: Braff, David L.
Swerdlow, Neal R.
Venue: Psychopharmacology
Publisher: Springer Science and Business Media LLC
Published: 2001-06-22
Volume: 156
Issue: 2-3
Pages: 117-154
ISSN: 0033-3158 (ISSN-L)
1432-2072
DOI: 10.1007/s002130100811
OpenAlex: W2005756201
Cited by: 1,484
References: 194
Citations by year: 2026: 17 · 2025: 13 · 2024: 23 · 2023: 37 · 2022: 34 · 2021: 41 · 2020: 27 · 2019: 38 · 2018: 36 · 2017: 47 · 2016: 62 · 2015: 64 · 2014: 48 · 2013: 69 · 2012: 74
FWCI: 42.73
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Psychopharmacology (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute of Mental Health (MH 52885, MH42228, MH61326, R01MH061326, R01MH052885)
Topics: Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: prepulse inhibition, animal models of schizophrenia, dopamine D2 receptor agonist, amphetamine, apomorphine, NMDA receptor antagonists, phencyclidine, clozapine, atypical antipsychotics, isolation rearing, systemic drug administration
MeSH terms: Animals, Humans, Schizophrenia, Schizophrenic Psychology, Reflex, Startle

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Pharmacological studies of prepulse inhibition models of sensorimotor gating deficits in schizophrenia: a decade in review

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