Hyperactivity, decreased startle reactivity, and disrupted prepulse inhibition following disinhibition of the rat ventral hippocampus by the GABAA receptor antagonist picrotoxin

Bast, Tobias; Zhang, Wei-Ning; Feldon, Joram

doi:10.1007/s002130100775

Cited by 73Schizophrenia research and treatmentNeuroscience and Neuropharmacology ResearchNeurotransmitter Receptor Influence on Behavior

Hyperactivity, decreased startle reactivity, and disrupted prepulse inhibition following disinhibition of the rat ventral hippocampus by the GABAA receptor antagonist picrotoxin

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Bast, Tobias, Zhang, Wei-Ning, Feldon, Joram·2001·Psychopharmacology

DOI 10.1007/s002130100775

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Abstract

Rationale Functional imaging studies have revealed overactivity of the hippocampus in schizophrenic patients. Neuropathological data indicate that hyperactivity of excitatory hippocampal afferents and decreased hippocampal GABA transmission contribute to this overactivity. In rats, excitation of the ventral hippocampus, e.g. by NMDA, results in hyperactivity and disruption of sensorimotor gating measured as prepulse inhibition (PPI) of the acoustic startle response, behavioral effects related to psychotic symptoms in humans.Objective The present study examined whether disinhibition of the ventral hippocampus by the GABA(A) antagonist picrotoxin would result in similar psychosis-related behavioral disturbances (hyperactivity, decreased PPI) as NMDA stimulation.Methods and results Wistar rats received bilateral infusions of subconvulsive doses of picrotoxin (100 or 150 ng/0.5 microl per side) into the ventral hippocampus and were then immediately tested for open field locomotor activity or startle reactivity and PPI. Only the higher dose induced hyperactivity and decreased PPI. Both doses decreased acoustic startle reactivity to a similar extent. The decreased PPI appeared not to result from decreased startle reactivity, but was associated with a diminished potency of the prepulses to inhibit the startle reaction to the startle pulse, indicating a sensorimotor gating deficit. All effects were temporary, i.e. disappeared when the rats were tested 24 h after infusion.Conclusions Decreased GABAergic inhibition in the ventral hippocampus of rats yielded psychosis-related behavioral effects, very similar to those induced by NMDA stimulation. Thus, a concurrence of decreased GABAergic inhibition and increased afferent excitation in the hippocampus of schizophrenic patients might contribute to psychotic symptoms.

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Optogenetic or pharmacological stimulation of the vHIP increases anxiety-like behavior.
“while optogenetic or pharmacological stimulation of the region has the opposite effect (16–18).”
From Perineuronal nets, inhibitory interneurons and anxiety-related ventral hippocampal neuronal oscillations are altered by early life adversity (2019) · cites this paper as [16]

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“For example, infusion of picrotoxin, a g-aminobutyric acid (GABA) antagonist, into the mPFC or the bilateral ventral hippocampus (Bast et al., 2001) dose-dependently impaired PPI in rats (Japha and Koch, 1999).”
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“…by Flood et al. (2010) at 100 mg/kg since GABAA receptor antagonists as well as genetic deletion of GABAA receptors subunits are more commonly associated with disruption rather than potentiation of PPI (Bast et al. 2001; Hauser et al. 2005; Khalifa 2005; Yee et al. 2005a, b; Yeomans et al. 2010).”
Background
Acoustic Startle Responses and Prepulse Inhibition of Acoustic Startle Responses in Warsaw Alcohol High-Preferring (WHP) and Warsaw Alcohol Low-Preferring (WLP) Rats
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“GABAergic transmission has been implicated in the etiology of alcoholism and anxiety disorders and has been proposed to be responsible for individual differences in the ASR (Bast et al., 2001; Saba et al., 2011).”
Background
Hippocampal Disinhibition Reduces Contextual and Elemental Fear Conditioning While Sparing the Acquisition of Latent Inhibition
Williams, S. A., Gwilt, M., Hock, R. M., Taylor, C., Loayza, J., Stevenson, C. W., Cassaday, H. J., & Bast, T. (2022) · eNeuro · doi:10.1523/eneuro.0270-21.2021 · Cited by 10 · see citing works
“Lesions, temporary inactivation by the sodium channel blocker TTX, and NMDA stimulation of the VH have been found to disrupt both contextual and elemental fear conditioning (Bast et al., 2001b; Czerniawski et al., 2012; Kjelstrup et al., 2002; Maren, 1999; Zhang et al., 2001).”
BackgroundResult
Anxiolytic-Like Effects and Increase in Locomotor Activity Induced by Infusions of NMDA into the Ventral Hippocampus in Rat: Interaction with GABAergic System.
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Longitudinal Assessment of Working Memory Performance in the APPswe/PSEN1dE9 Mouse Model of Alzheimer’s Disease Using an Automated Figure-8-Maze
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Transient Inactivation of the Medial Prefrontal Cortex and Ventral Hippocampus Impairs Active Place Avoidance Retrieval on a Rotating Arena
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“, 2003), locomotion (Bast et al., 2001), and the response to stress (Herman et al.”
Background
Doctor of Philosophy (PhD)
Biss, M. (2015) · Cited by 3 · see citing works
Too Little and Too Much: Balanced Hippocampal, But Not Medial Prefrontal, Neural Activity Is Required for Intact Novel Object Recognition in Rats
Taylor, C. S. R., Renström, J. G., Loayza, J., Gwilt, M., Williams, S. A., Allen, R. G., Moran, P. M., Gigg, J., Neill, J. C., Harte, M., et al. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.1141-25.2025 · Cited by 3 · see citing works
“The muscimol dose (500 ng/0.5 µl) was based on previous studies investigating functional inhibition of the DH or VH on various behavioral tasks (Bast et al., 2001b; de Lima et al., 2006; McDonald et al., 2010; Oliveira et al., 2010; Zhang et al., 2014; Sawangjit et al., 2018).”
Influential
Monoallelic loss of the F-actin-binding protein radixin facilitates startle reactivity and pre-pulse inhibition in mice
Hausrat, T. J., Vogl, C., Neef, J., Schweizer, M., Yee, B. K., Strenzke, N., & Kneussel, M. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.987691 · Cited by 2 · see citing works
“It is further of relevance that an intra-hippocampal infusion of the GABAAR antagonist picrotoxin attenuates PPI, pointing to an involvement of hippocampal GABAAR activity in the modulation of PPI expression (Bast et al., 2001).”
Background
Chronic Pb 2+ Exposure Causes Hippocampal Network Hypersynchrony, Absence Seizures, and Sensorimotor DeficitsPreprint
Schultheiss, N. W., McGlothan, J. L., Guilarte, T. R., & Allen, T. A. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.06.30.181149 · Cited by 1 · see citing works
“To examine this possibility, we measured PPI of the acoustic startle response (ASR), a test of sensorimotor gating that is disrupted by HC damage (Pouzet et al., 1999; Bast et al., 2001a; 2001b; 2003), and a canonical dysfunction linked to schizophrenia.”
Hippocampal disinhibition reduces contextual and elemental fear conditioning while sparing the acquisition of latent inhibitionPreprint
Williams, S. A., Gwilt, M., Hock, R. M., Taylor, C., Loayza, J., Stevenson, C. W., Cassaday, H. J., & Bast, T. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.06.02.446736 · Cited by 1 · see citing works
Seizure and Behavioral Phenotyping of the Scn1a Mouse Model of Genetic Epilepsy with Febrile Seizures Plus
Helvig, A. W. (2022) · Digital Archive @ GSU · doi:10.57709/3503320
POST-WEANING SOCIAL ISOLATION AND SUBCHRONIC NMDA GLUTAMATE RECEPTOR BLOCKADE: EFFECTS ON LOCOMOTOR ACTIVITY AND GABA SIGNALLING IN THE RAT
Hickey, A. J. (2010) · QSpace (Queen's University Library)
A characterisation of hippocampal pathophysiology in autoimmune encephalitis : from synapse to circuit
Hunter, D. (2023) · doi:10.70675/ae0cf321z922dz4431z8e9czca6cbf457b2e

Picrotoxin in the medial prefrontal cortex impairs sensorimotor gating in rats: reversal by haloperidol
Japha, K., & Koch, M. (1999) · Psychopharmacology · doi:10.1007/s002130051017 · Cited by 77 · see citing works
Prepulse inhibition in rats with temporary inhibition/inactivation of ventral or dorsal hippocampus
Zhang, W.-N., Bast, T., & Feldon, J. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)00936-x · Cited by 56 · see citing works
Hippocampal Neural Disinhibition Causes Attentional and Memory Deficits
McGarrity, S., Mason, R., Fone, K. C. F., Pezze, M. A., & Bast, T. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw247 · Cited by 50 · see citing works
Neuro-behavioural impact of changes in hippocampal neural activity
Williams, S. A. (2021) · Nottingham ePrints (University of Nottingham)
Parvalbumin and GAD65 Interneuron Inhibition in the Ventral Hippocampus Induces Distinct Behavioral Deficits Relevant to Schizophrenia
Nguyen, R., Morrissey, M. D., Mahadevan, V., Cajanding, J. D., Woodin, M. A., Yeomans, J. S., Takehara‐Nishiuchi, K., & Kim, J. C. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.2204-14.2014 · Cited by 94 · see citing works

Authors: Bast, T., Zhang, W.-N., & Feldon, J.
Affiliations: ETH Zurich (CH)
ORCID: Bast, Tobias
Venue: Psychopharmacology
Publisher: Springer Science and Business Media LLC
Published: 2001-06-22
Volume: 156
Issue: 2-3
Pages: 225-233
ISSN: 0033-3158 (ISSN-L)
1432-2072
DOI: 10.1007/s002130100775
OpenAlex: W2076775404
Cited by: 73
References: 73
Citations by year: 2025: 1 · 2023: 1 · 2022: 4 · 2021: 4 · 2020: 3 · 2019: 2 · 2018: 1 · 2017: 2 · 2016: 3 · 2015: 1 · 2014: 4 · 2013: 2 · 2012: 7
FWCI: 4.08
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.springer.com/tdm (tdm)
Locations: Psychopharmacology (publishedVersion)
PubMed (publishedVersion)
reroDoc Digital Library (submittedVersion)
Repository for Publications and Research Data (ETH Zurich) (submittedVersion, other-oa)
ETH Zürich Research Collection
Funders: Eidgenössische Technische Hochschule Zürich
Topics: Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords: ventral hippocampus, picrotoxin, GABA-A receptor antagonism, hyperactivity, acoustic startle response, prepulse inhibition, sensorimotor gating, schizophrenia, NMDA stimulation, GABAergic inhibition
MeSH terms: Animals, Dose-Response Relationship, Drug, Hippocampus, Hyperkinesis, Male, Microinjections, Motor Activity, Picrotoxin, Pilot Projects, Reflex, Startle, Rats, Wistar, GABA Antagonists, Rats, GABA-A Receptor Antagonists

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Hyperactivity, decreased startle reactivity, and disrupted prepulse inhibition following disinhibition of the rat ventral hippocampus by the GABAA receptor antagonist picrotoxin

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