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Parvalbumin and anxiety across development in female offspring of the MAM neurodevelopmental model of schizophrenia.

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Τίτλος: Parvalbumin and anxiety across development in female offspring of the MAM neurodevelopmental model of schizophrenia.
Συγγραφείς: Gurgel SE; Departments of Neuroscience, Psychiatry and Psychology, University of Pittsburgh, Pittsburgh, PA, USA; Stanford University School of Medicine, Stanford, CA, USA., Kumaran C; Departments of Neuroscience, Psychiatry and Psychology, University of Pittsburgh, Pittsburgh, PA, USA; Geisinger Commonwealth School of Medicine, Scranton, PA, USA., Uliana DL; Departments of Neuroscience, Psychiatry and Psychology, University of Pittsburgh, Pittsburgh, PA, USA. Electronic address: uliana@pitt.edu., Grace AA; Departments of Neuroscience, Psychiatry and Psychology, University of Pittsburgh, Pittsburgh, PA, USA.
Πηγή: Journal of psychiatric research [J Psychiatr Res] 2026 Oct; Vol. 201, pp. 507-517. Date of Electronic Publication: 2026 Jul 03.
Τύπος έκδοσης: Journal Article
Γλώσσα: English
Στοιχεία περιοδικού: Publisher: Pergamon Press Country of Publication: England NLM ID: 0376331 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1879-1379 (Electronic) Linking ISSN: 00223956 NLM ISO Abbreviation: J Psychiatr Res Subsets: MEDLINE
Imprint Name(s): Original Publication: Oxford : Pergamon Press
Ιατρικοί όροι (MeSH): Parvalbumins*/metabolism , Schizophrenia*/chemically induced , Schizophrenia*/metabolism , Schizophrenia*/physiopathology , Methylazoxymethanol Acetate*/pharmacology , Anxiety*/metabolism , Anxiety*/etiology , Anxiety*/physiopathology , Anxiety*/chemically induced , Prenatal Exposure Delayed Effects*/chemically induced , Prenatal Exposure Delayed Effects*/metabolism , Prenatal Exposure Delayed Effects*/physiopathology , Behavior, Animal*/physiology , Behavior, Animal*/drug effects , Interneurons*/metabolism, Perineuronal Nets/metabolism ; Hippocampus/metabolism ; Basolateral Nuclear Complex/metabolism ; Animals ; Female ; Disease Models, Animal ; Rats ; Pregnancy ; Male ; Rats, Sprague-Dawley ; Neurodevelopment
Περίληψη: Schizophrenia is a neurodevelopmental disorder often accompanied by heightened anxiety. The methylazoxymethanol acetate (MAM) rodent model has demonstrated that prenatal MAM exposure disrupts neurodevelopment and leads to schizophrenia-like deficits, including increased anxiety-like behaviors. While previous research has focused primarily on male subjects, this study investigates anxiety-like behaviors and parvalbumin (PV) interneuron and perineuronal net (PNN) expression in the basolateral amygdala (BLA), thalamic reticular nucleus (TRN), and ventral hippocampus (vHIP) in female MAM rats across postnatal development (PD31-PD75). We found that female MAM rats exhibited increased anxiety-like behaviors in adulthood (PD75), as evidenced by reduced time spent and entries in the open arms of the elevated plus maze and increased center exploration in the open field test. At PD31, an increase in the open arms time and margin exploration was observed in female MAM rats. Interestingly, a baseline hyperlocomotion was observed at PD31 and PD51 in the MAM condition. The TRN also showed reduced PNN density at PD31 and PV density at PD51 which indicates a possible deficit in inhibitory control. Interestingly, in contrast to prior work in males, the BLA did not show alterations in PV or PNN densities that would contribute to increased anxiety, suggesting a different mechanism of anxiety regulation in females compared to males. These findings highlight sex-specific neurodevelopmental alterations following prenatal MAM exposure, emphasizing the need for further research on female models of schizophrenia. Understanding these differences may improve targeted therapeutic strategies for anxiety and psychosis risk in schizophrenia.
(Copyright © 2026. Published by Elsevier Ltd.)
Competing Interests: Declaration of competing interest Sofia E. Gurgel, Cynthia Kumaran, and Daniela L. Uliana have nothing to disclose. Anthony A. Grace has received consulting fees from Alkermes, Takeda, Roche, Bristol-Meyers-Squib, Merck and Newron and research funding from Lundbeck, Newron and Merck. This work was supported by NIH MH57440 to AAG. We thank Nicole Macmurdo for technical support.
References: Dev Psychobiol. 2010 Dec;52(8):731-9. (PMID: 21117243)
Behav Brain Res. 2009 Dec 7;204(2):306-12. (PMID: 19716984)
Lancet. 2022 Jan 29;399(10323):473-486. (PMID: 35093231)
Schizophr Bull. 2001;27(3):457-76. (PMID: 11596847)
Br J Psychiatry. 2005 May;186:386-93. (PMID: 15863742)
Mol Psychiatry. 2023 Dec;28(12):4954-4967. (PMID: 37419975)
Learn Mem. 2016 Jan 15;23(2):51-60. (PMID: 26773098)
Int J Dev Neurosci. 2011 May;29(3):207-13. (PMID: 20727962)
Mol Psychiatry. 2021 Dec;26(12):7679-7689. (PMID: 34193975)
Eur J Neurosci. 2021 Jun;53(12):3988-4004. (PMID: 32510674)
Aust N Z J Psychiatry. 2005 Nov-Dec;39(11-12):964-71. (PMID: 16343296)
Brain Struct Funct. 2020 Nov;225(8):2495-2507. (PMID: 32914251)
Mol Psychiatry. 2023 Feb;28(2):611-624. (PMID: 36224257)
Nat Rev Neurosci. 2016 Aug;17(8):524-32. (PMID: 27256556)
Sci Rep. 2016 Nov 23;6:37580. (PMID: 27876866)
Schizophr Res. 2025 Nov;285:155-164. (PMID: 41014918)
Methods Mol Biol. 2019;1916:99-103. (PMID: 30535687)
J Neurosci. 2016 Jul 6;36(27):7246-52. (PMID: 27383598)
Behav Brain Res. 2019 Apr 19;362:258-265. (PMID: 30660776)
J Clin Psychiatry. 1999 Nov;60(11):747-51. (PMID: 10584762)
Int Rev Neurobiol. 2007;78:1-39. (PMID: 17349856)
Neuropsychopharmacology. 2025 Oct;50(11):1631-1642. (PMID: 40764757)
Int Rev Psychiatry. 2010;22(5):417-28. (PMID: 21047156)
Schizophr Res. 2012 Mar;135(1-3):170-4. (PMID: 22226904)
J Abnorm Psychol. 2010 May;119(2):401-8. (PMID: 20455612)
Eur Neuropsychopharmacol. 2024 May;82:44-52. (PMID: 38490084)
Nat Protoc. 2007;2(2):322-8. (PMID: 17406592)
Eur Neuropsychopharmacol. 2019 Oct;29(10):1127-1137. (PMID: 31371105)
Int J Neuropsychopharmacol. 2014 Oct;17(10):1609-19. (PMID: 24787547)
Psychol Med. 2013 Feb;43(2):259-68. (PMID: 22651857)
Front Psychiatry. 2021 Aug 31;12:711065. (PMID: 34531768)
Arch Gen Psychiatry. 2009 Jan;66(1):13-20. (PMID: 19124684)
J Neurosci Methods. 1980 Dec;3(2):129-49. (PMID: 6110810)
Eur J Neurosci. 2018 Nov;48(10):3255-3272. (PMID: 30107061)
Nat Commun. 2019 Oct 11;10(1):4637. (PMID: 31604913)
Lancet. 1995 Aug 19;346(8973):477-81. (PMID: 7637483)
Brain Struct Funct. 2014 Jan;219(1):395-406. (PMID: 23400698)
Gen Psychiatr. 2022 Aug 30;35(4):e100823. (PMID: 36118418)
Biol Psychiatry. 2006 Aug 1;60(3):253-64. (PMID: 16581031)
Neuropsychopharmacology. 2004 Nov;29(11):2052-64. (PMID: 15199377)
Neuropsychopharmacology. 2016 Sep;41(10):2455-62. (PMID: 27000940)
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Neuropsychopharmacology. 2013 Sep;38(10):1881-8. (PMID: 23612434)
Mol Psychiatry. 2020 Dec;25(12):3278-3291. (PMID: 31488866)
Grant Information: R01 MH057440 United States MH NIMH NIH HHS
Contributed Indexing: Keywords: Anxiety; Females; Parvalbumin; Schizophrenia
Substance Nomenclature: 0 (Parvalbumins)
592-62-1 (Methylazoxymethanol Acetate)
Entry Date(s): Date Created: 20260707 Date Completed: 20260811 Latest Revision: 20261001
Update Code: 20261001
PubMed Central ID: PMC13617632
DOI: 10.1016/j.jpsychires.2026.07.002
PMID: 42413186
Βάση Δεδομένων: MEDLINE
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  Data: Parvalbumin and anxiety across development in female offspring of the MAM neurodevelopmental model of schizophrenia.
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  Data: Schizophrenia is a neurodevelopmental disorder often accompanied by heightened anxiety. The methylazoxymethanol acetate (MAM) rodent model has demonstrated that prenatal MAM exposure disrupts neurodevelopment and leads to schizophrenia-like deficits, including increased anxiety-like behaviors. While previous research has focused primarily on male subjects, this study investigates anxiety-like behaviors and parvalbumin (PV) interneuron and perineuronal net (PNN) expression in the basolateral amygdala (BLA), thalamic reticular nucleus (TRN), and ventral hippocampus (vHIP) in female MAM rats across postnatal development (PD31-PD75). We found that female MAM rats exhibited increased anxiety-like behaviors in adulthood (PD75), as evidenced by reduced time spent and entries in the open arms of the elevated plus maze and increased center exploration in the open field test. At PD31, an increase in the open arms time and margin exploration was observed in female MAM rats. Interestingly, a baseline hyperlocomotion was observed at PD31 and PD51 in the MAM condition. The TRN also showed reduced PNN density at PD31 and PV density at PD51 which indicates a possible deficit in inhibitory control. Interestingly, in contrast to prior work in males, the BLA did not show alterations in PV or PNN densities that would contribute to increased anxiety, suggesting a different mechanism of anxiety regulation in females compared to males. These findings highlight sex-specific neurodevelopmental alterations following prenatal MAM exposure, emphasizing the need for further research on female models of schizophrenia. Understanding these differences may improve targeted therapeutic strategies for anxiety and psychosis risk in schizophrenia.<br /> (Copyright © 2026. Published by Elsevier Ltd.)
– Name: Abstract
  Label: Competing Interests
  Group: Ab
  Data: Declaration of competing interest Sofia E. Gurgel, Cynthia Kumaran, and Daniela L. Uliana have nothing to disclose. Anthony A. Grace has received consulting fees from Alkermes, Takeda, Roche, Bristol-Meyers-Squib, Merck and Newron and research funding from Lundbeck, Newron and Merck. This work was supported by NIH MH57440 to AAG. We thank Nicole Macmurdo for technical support.
– Name: Ref
  Label: References
  Group: RefInfo
  Data: Dev Psychobiol. 2010 Dec;52(8):731-9. (PMID: <searchLink fieldCode="PM" term="%2221117243%22">21117243)</searchLink><br />Behav Brain Res. 2009 Dec 7;204(2):306-12. (PMID: <searchLink fieldCode="PM" term="%2219716984%22">19716984)</searchLink><br />Lancet. 2022 Jan 29;399(10323):473-486. (PMID: <searchLink fieldCode="PM" term="%2235093231%22">35093231)</searchLink><br />Schizophr Bull. 2001;27(3):457-76. (PMID: <searchLink fieldCode="PM" term="%2211596847%22">11596847)</searchLink><br />Br J Psychiatry. 2005 May;186:386-93. (PMID: <searchLink fieldCode="PM" term="%2215863742%22">15863742)</searchLink><br />Mol Psychiatry. 2023 Dec;28(12):4954-4967. (PMID: <searchLink fieldCode="PM" term="%2237419975%22">37419975)</searchLink><br />Learn Mem. 2016 Jan 15;23(2):51-60. (PMID: <searchLink fieldCode="PM" term="%2226773098%22">26773098)</searchLink><br />Int J Dev Neurosci. 2011 May;29(3):207-13. (PMID: <searchLink fieldCode="PM" term="%2220727962%22">20727962)</searchLink><br />Mol Psychiatry. 2021 Dec;26(12):7679-7689. (PMID: <searchLink fieldCode="PM" term="%2234193975%22">34193975)</searchLink><br />Eur J Neurosci. 2021 Jun;53(12):3988-4004. (PMID: <searchLink fieldCode="PM" term="%2232510674%22">32510674)</searchLink><br />Aust N Z J Psychiatry. 2005 Nov-Dec;39(11-12):964-71. (PMID: <searchLink fieldCode="PM" term="%2216343296%22">16343296)</searchLink><br />Brain Struct Funct. 2020 Nov;225(8):2495-2507. (PMID: <searchLink fieldCode="PM" term="%2232914251%22">32914251)</searchLink><br />Mol Psychiatry. 2023 Feb;28(2):611-624. (PMID: <searchLink fieldCode="PM" term="%2236224257%22">36224257)</searchLink><br />Nat Rev Neurosci. 2016 Aug;17(8):524-32. (PMID: <searchLink fieldCode="PM" term="%2227256556%22">27256556)</searchLink><br />Sci Rep. 2016 Nov 23;6:37580. 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(PMID: <searchLink fieldCode="PM" term="%2236118418%22">36118418)</searchLink><br />Biol Psychiatry. 2006 Aug 1;60(3):253-64. (PMID: <searchLink fieldCode="PM" term="%2216581031%22">16581031)</searchLink><br />Neuropsychopharmacology. 2004 Nov;29(11):2052-64. (PMID: <searchLink fieldCode="PM" term="%2215199377%22">15199377)</searchLink><br />Neuropsychopharmacology. 2016 Sep;41(10):2455-62. (PMID: <searchLink fieldCode="PM" term="%2227000940%22">27000940)</searchLink><br />Brain Res Bull. 2007 Mar 30;71(6):601-9. (PMID: <searchLink fieldCode="PM" term="%2217292803%22">17292803)</searchLink><br />Neurotox Res. 2008 Oct;14(2-3):97-104. (PMID: <searchLink fieldCode="PM" term="%2219073417%22">19073417)</searchLink><br />Neuropsychopharmacology. 2013 Sep;38(10):1881-8. (PMID: <searchLink fieldCode="PM" term="%2223612434%22">23612434)</searchLink><br />Mol Psychiatry. 2020 Dec;25(12):3278-3291. (PMID: <searchLink fieldCode="PM" term="%2231488866%22">31488866)</searchLink>
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      – Type: doi
        Value: 10.1016/j.jpsychires.2026.07.002
    Languages:
      – Code: eng
        Text: English
    PhysicalDescription:
      Pagination:
        StartPage: 507
    Subjects:
      – SubjectFull: Perineuronal Nets metabolism
        Type: general
      – SubjectFull: Hippocampus metabolism
        Type: general
      – SubjectFull: Basolateral Nuclear Complex metabolism
        Type: general
      – SubjectFull: Animals
        Type: general
      – SubjectFull: Female
        Type: general
      – SubjectFull: Disease Models, Animal
        Type: general
      – SubjectFull: Rats
        Type: general
      – SubjectFull: Pregnancy
        Type: general
      – SubjectFull: Male
        Type: general
      – SubjectFull: Rats, Sprague-Dawley
        Type: general
      – SubjectFull: Neurodevelopment
        Type: general
      – SubjectFull: Parvalbumins metabolism
        Type: general
      – SubjectFull: Schizophrenia chemically induced
        Type: general
      – SubjectFull: Schizophrenia metabolism
        Type: general
      – SubjectFull: Schizophrenia physiopathology
        Type: general
      – SubjectFull: Methylazoxymethanol Acetate pharmacology
        Type: general
      – SubjectFull: Anxiety metabolism
        Type: general
      – SubjectFull: Anxiety etiology
        Type: general
      – SubjectFull: Anxiety physiopathology
        Type: general
      – SubjectFull: Anxiety chemically induced
        Type: general
      – SubjectFull: Prenatal Exposure Delayed Effects chemically induced
        Type: general
      – SubjectFull: Prenatal Exposure Delayed Effects metabolism
        Type: general
      – SubjectFull: Prenatal Exposure Delayed Effects physiopathology
        Type: general
      – SubjectFull: Behavior, Animal physiology
        Type: general
      – SubjectFull: Behavior, Animal drug effects
        Type: general
      – SubjectFull: Interneurons metabolism
        Type: general
    Titles:
      – TitleFull: Parvalbumin and anxiety across development in female offspring of the MAM neurodevelopmental model of schizophrenia.
        Type: main
  BibRelationships:
    HasContributorRelationships:
      – PersonEntity:
          Name:
            NameFull: Gurgel SE
      – PersonEntity:
          Name:
            NameFull: Kumaran C
      – PersonEntity:
          Name:
            NameFull: Uliana DL
      – PersonEntity:
          Name:
            NameFull: Grace AA
    IsPartOfRelationships:
      – BibEntity:
          Dates:
            – D: 01
              M: 10
              Text: 2026 Oct
              Type: published
              Y: 2026
          Identifiers:
            – Type: issn-electronic
              Value: 1879-1379
          Numbering:
            – Type: volume
              Value: 201
          Titles:
            – TitleFull: Journal of psychiatric research
              Type: main
ResultId 1