A Neonatal Ventral Hippocampal Lesion Causes Functional Deficits in Adult Prefrontal Cortical Interneurons

Tseng, Kuei Y.; Lewis, Barbara L.; Hashimoto, Takanori; Sesack, Susan R.; Kloc, Michelle; Lewis, David A.; O'Donnell, Patricio

doi:10.1523/jneurosci.4166-08.2008

Cited by 144Schizophrenia research and treatmentNeuroscience and Neuropharmacology ResearchNeurotransmitter Receptor Influence on Behavior

A Neonatal Ventral Hippocampal Lesion Causes Functional Deficits in Adult Prefrontal Cortical Interneurons

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Tseng, Kuei Y., Lewis, Barbara L., Hashimoto, Takanori, Sesack, Susan R., Kloc, Michelle, Lewis, David A., O'Donnell, Patricio·2008·The Journal of Neuroscience

DOI 10.1523/jneurosci.4166-08.2008PMC PMC2676938

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Abstract

Animals with a neonatal ventral hippocampal lesion (NVHL) develop abnormal behaviors during or after adolescence, suggesting that early insults can have delayed consequences. Many of these behaviors depend on the prefrontal cortex (PFC), and we have reported that PFC pyramidal neurons of adult rats with an NVHL respond to stimulation of the ventral tegmental area with an increase in firing instead of the characteristic decrease. As the dopamine modulation of cortical interneurons matures during adolescence, these findings raise the possibility that maturation of local inhibitory circuits within the PFC may have been altered in NVHL rats. Here, we assessed the state of PFC interneurons in NVHL rats with in situ hybridization measures of the mRNAs for the calcium binding protein parvalbumin (PV) and the GABA synthesizing enzyme GAD 67, as well as with electrophysiological measures of interneuron function. Although no differences were observed with PV or GAD 67, whole-cell recordings in slices revealed abnormal responses to the D 2 agonist quinpirole in interneurons from NVHL rats. The loss of D 2 modulation of local inhibition in slices from NVHL rats was also evident in the absence of a lasting component in the D 2 attenuation of excitatory synaptic responses in pyramidal neurons, which in sham treated rats was picrotoxin sensitive. The results suggest that the neonatal lesion causes improper maturation, but not loss, of PFC interneurons during adolescence, a finding consistent with current interpretations of imaging data in schizophrenia that suggest a hyperactive, “noisy” cortex underlying dysfunction in the PFC and other cortical areas.

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Recordings in brain slices revealed increased excitability of pyramidal neurons and a deficient activation of fast-spiking GABA interneurons by D2 agonists in the PFC of NVHL rats.
“Recordings in brain slices revealed increased excitability of pyramidal neurons 52 and a deficient activation of fast-spiking GABA interneurons by D 2 agonists 53 in the PFC of NVHL rats.”
From Adolescent Onset of Cortical Disinhibition in Schizophrenia: Insights From Animal Models (2011) · cites this paper as [53]

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Long-Lasting Rescue of Network and Cognitive Dysfunction in a Genetic Schizophrenia Model
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Distinct cortical and striatal actions of a β-arrestin–biased dopamine D2 receptor ligand reveal unique antipsychotic-like properties
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GABAergic modulation of the 40 Hz auditory steady-state response in a rat model of schizophrenia
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Maternal immune activation by polyriboinosinic-polyribocytidilic acid injection produces synaptic dysfunction but not neuronal loss in the hippocampus of juvenile rat offspring
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Neonatal hippocampal lesion alters the functional maturation of the prefrontal cortex and the early cognitive development in pre-juvenile rats
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Dopamine Modulation of GABAergic Function Enables Network Stability and Input Selectivity for Sustaining Working Memory in a Computational Model of the Prefrontal Cortex
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Hippocampal Volume Development in Healthy Siblings of Childhood-Onset Schizophrenia Patients
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Altered Dopamine Modulation of Inhibition in the Prefrontal Cortex of Cocaine-Sensitized Rats
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The effect of perinatal brain injury on dopaminergic function and hippocampal volume in adult life
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Authors: Tseng, K. Y., Lewis, B. L., Hashimoto, T., Sesack, S. R., Kloc, M., Lewis, D. A., & O'Donnell, P.
Affiliations: Albany Medical College (US)
University of Maryland, Baltimore (US)
University of Pittsburgh (US)
ORCID: Hashimoto, Takanori
Sesack, Susan R.
Kloc, Michelle
Lewis, David A.
Venue: The Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 2008-11-26
Volume: 28
Issue: 48
Pages: 12691-12699
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.4166-08.2008
PMC: PMC2676938
OpenAlex: W2008537040
Cited by: 144
References: 68
Citations by year: 2026: 2 · 2025: 2 · 2023: 4 · 2022: 1 · 2021: 2 · 2020: 3 · 2019: 6 · 2018: 3 · 2017: 5 · 2016: 11 · 2015: 9 · 2014: 12 · 2013: 14 · 2012: 13
FWCI: 12.88
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-sa
creativecommons.org/licenses/by-nc-sa/4.0/ (vor, 181 d)
Locations: Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
Funders: National Institutes of Health (MH57683)
National Institute of Mental Health (MH-51234, MH57683, R56MH057683, R01MH057683, R01MH051234)
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: parvalbumin, GAD67, dopamine D2 receptor, quinpirole, local inhibition, pyramidal neurons, adolescence, schizophrenia, inhibitory circuits
MeSH terms: Aging, Animals, Animals, Newborn, Denervation, gamma-Aminobutyric Acid, Glutamate Decarboxylase, Hippocampus, Interneurons, Male, Neural Inhibition, Neural Pathways, Organ Culture Techniques, Parvalbumins, RNA, Messenger, Schizophrenia, Biomarkers, Rats, Sprague-Dawley, Prefrontal Cortex, Pyramidal Cells, Patch-Clamp Techniques, Dopamine Agonists, Rats, Neurogenesis

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A Neonatal Ventral Hippocampal Lesion Causes Functional Deficits in Adult Prefrontal Cortical Interneurons

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