[en] Parvalbumin (PV) neurons play an integral role in regulating neural dynamics and plasticity. Therefore, understanding the factors that regulate PV expression is important for revealing modulators of brain function. While the contribution of PV neurons to neural processes has been studied in mammals, relatively little is known about PV function in non-mammalian species, and discerning similarities in the regulation of PV across species can provide insight into evolutionary conservation in the role of PV neurons. Here we investigated factors that affect the abundance of PV in PV neurons in sensory and motor circuits of songbirds and rodents. In particular, we examined the degree to which perineuronal nets (PNNs), extracellular matrices that preferentially surround PV neurons, modulate PV abundance as well as how the relationship between PV and PNN expression differs across brain areas and species and changes over development. We generally found that cortical PV neurons that are surrounded by PNNs (PV+PNN neurons) are more enriched with PV than PV neurons without PNNs (PV-PNN neurons) across both rodents and songbirds. Interestingly, the relationship between PV and PNN expression in the vocal portion of the basal ganglia of songbirds (Area X) differed from that in other areas, with PV+PNN neurons having lower PV expression compared to PV-PNN neurons. These relationships remained consistent across development in vocal motor circuits of the songbird brain. Finally, we discovered a causal contribution of PNNs to PV expression in songbirds because degradation of PNNs led to a diminution of PV expression in PV neurons. These findings reveal a conserved relationship between PV and PNN expression in sensory and motor cortices and across songbirds and rodents and suggest that PV neurons could modulate plasticity and neural dynamics in similar ways across songbirds and rodents.
Disciplines :
Zoology Neurology
Author, co-author :
Wang, Angela S; Department of Biology, McGill University, Montreal, QC, Canada
Wan, Xinghaoyun; Department of Biology, McGill University, Montreal, QC, Canada ; Integrated Program in Neuroscience, McGill University, Montreal, QC, Canada
Storch, Daria-Salina; Department of Biology, McGill University, Montreal, QC, Canada
Li, Vivian Y; Department of Biology, McGill University, Montreal, QC, Canada
Balthazart, Jacques ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques
Cisneros-Franco, J Miguel; Integrated Program in Neuroscience, McGill University, Montreal, QC, Canada
de Villers-Sidani, Etienne; Integrated Program in Neuroscience, McGill University, Montreal, QC, Canada ; Centre for Research in Brain, Language and Music, McGill University, Montreal, QC, Canada
Sakata, Jon T; Department of Biology, McGill University, Montreal, QC, Canada ; Integrated Program in Neuroscience, McGill University, Montreal, QC, Canada ; Centre for Research in Brain, Language and Music, McGill University, Montreal, QC, Canada
Language :
English
Title :
Cross-species conservation in the regulation of parvalbumin by perineuronal nets.
The author(s) declare financial support was received for the research, authorship, and/or publication of this article. Research was supported by the Natural Sciences and Engineering Research Council (NSERC; #05016 to JTS and #04761 to EV-S), by the Fonds de recherche du Quebec - Nature et technologies (FRQNT; #284884 to JTS), the Canadian Institutes for Health Research (CIHR #438114 to EV-S) and the National Institute for Neurological Disorders and Stroke (NINDS RO1 NS104008 to JB), and funds from the Centre for Research for Brain, Language, and Music (CRBLM) to JTS.
Albéri L. Lintas A. Kretz R. Schwaller B. Villa A. E. P. (2013). The calcium-binding protein parvalbumin modulates the firing 1 properties of the reticular thalamic nucleus bursting neurons. J. Neurophysiol. 109, 2827–2841. doi: 10.1152/jn.00375.2012, PMID: 23486206
Alpár A. Gärtner U. Härtig W. Brückner G. (2006). Distribution of pyramidal cells associated with perineuronal nets in the neocortex of rat. Brain Res. 1120, 13–22. doi: 10.1016/j.brainres.2006.08.069, PMID: 16996045
Balmer T. S. (2016). Perineuronal nets enhance the excitability of fast-spiking neurons. eNeuro 3:ENEURO.0112-16.2016. doi: 10.1523/ENEURO.0112-16.2016, PMID: 27570824
Balmer T. S. Carels V. M. Frisch J. L. Nick T. A. (2009). Modulation of perineuronal nets and parvalbumin with developmental song learning. J. Neurosci. 29, 12878–12885. do i: 10.1523/JNEUROSCI.2974-09.2009. doi: 10.1523/JNEUROSCI.2974-09.2009
Beurdeley M. Spatazza J. Lee H. H. C. Sugiyama S. Bernard C. Di Nardo A. A. et al. (2012). Otx2 binding to perineuronal nets persistently regulates plasticity in the mature visual cortex. J. Neurosci. 32, 9429–9437. doi: 10.1523/JNEUROSCI.0394-12.2012, PMID: 22764251
Brainard M. S. Doupe A. J. (2002). What songbirds teach us about learning. Nature 417, 351–358. doi: 10.1038/417351a, PMID: 12015616
Brainard M. S. Doupe A. J. (2013). Translating birdsong: songbirds as a model for basic and applied medical research. Annu. Rev. Neurosci. 36, 489–517. doi: 10.1146/annurev-neuro-060909-152826, PMID: 23750515
Braun K. Scheich H. Heizmann C. W. Hunziker W. (1991). Parvalbumin and calbindin-D28K immunoreactivity as developmental markers of auditory and vocal motor nuclei of the zebra finch. Neuroscience 40, 853–869. doi: 10.1016/0306-4522(91)90017-i, PMID: 2062443
Braun K. Scheich H. Schachner M. Heizmann C. W. (1985). Distribution of parvalbumin, cytochrome oxidase activity and 14C-2-deoxyglucose uptake in the brain of the zebra finch. Cell Tissue Res. 240, 101–115. doi: 10.1007/BF00217563
Carceller H. Guirado R. Ripolles-Campos E. Teruel-Marti V. Nacher J. (2020). Perineuronal nets regulate the inhibitory perisomatic input onto parvalbumin interneurons and γ activity in the prefrontal cortex. J. Neurosci. 40, 5008–5018. doi: 10.1523/JNEUROSCI.0291-20.2020, PMID: 32457072
Cardin J. A. Carlén M. Meletis K. Knoblich U. Zhang F. Deisseroth K. et al. (2009). Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459, 663–667. doi: 10.1038/nature08002, PMID: 19396156
Carrillo G. D. Doupe A. J. (2004). Is the songbird area X striatal, pallidal, or both? An anatomical study. J. Comp. Neurol. 473, 415–437. doi: 10.1002/cne.20099
Carulli D. Broersen R. De Winter F. Muir E. M. Mešković M. De Waal M. et al. (2020). Cerebellar plasticity and associative memories are controlled by perineuronal nets. Proc. Natl. Acad. Sci. U. S. A. 117, 6855–6865. doi: 10.1073/pnas.1916163117, PMID: 32152108
Carulli D. Pizzorusso T. Kwok J. C. F. Putignano E. Poli A. Forostyak S. et al. (2010). Animals lacking link protein have attenuated perineuronal nets and persistent plasticity. Brain 133, 2331–2347. doi: 10.1093/brain/awq145, PMID: 20566484
Cisneros-Franco J. M. de Villers-Sidani É. (2019). Reactivation of critical period plasticity in adult auditory cortex through chemogenetic silencing of parvalbumin-positive interneurons. Proc. Natl. Acad. Sci. U. S. A. 116, 26329–26331. doi: 10.1073/pnas.1913227117, PMID: 31843881
Cisneros-Franco J. M. Ouellet L. Kamal B. de Villers-Sidani É. (2018). A brain without brakes: reduced inhibition is associated with enhanced but dysregulated plasticity in the aged rat auditory cortex. eNeuro:5. doi: 10.1523/ENEURO.0051-18.2018
Cisneros-Franco J. M. Voss P. Thomas M. E. de Villers-Sidani É. (2020). “Chapter 8 – critical periods of brain development” in Handbook of clinical neurology neurocognitive development: normative development. eds. Gallagher A. Bulteau C. Cohen D. Michaud J. L. (Netherlands: Elsevier), 75–88.
Colquitt B. M. Merullo D. P. Konopka G. Roberts T. F. Brainard M. S. (2021). Cellular transcriptomics reveals evolutionary identities of songbird vocal circuits. Science 371:eabd9704. doi: 10.1126/science.abd9704, PMID: 33574185
Cornez G. Collignon C. Müller W. Cornil C. A. Ball G. F. Balthazart J. (2020a). Development of perineuronal nets during ontogeny correlates with sensorimotor vocal learning in canaries. eNeuro 7:ENEURO.0361-19.2020. doi: 10.1523/ENEURO.0361-19.2020
Cornez G. Jonckers E. Ter Haar S. M. Van Der Linden A. Cornil C. A. Balthazart J. (2018). Timing of perineuronal net development in the zebra finch song control system correlates with developmental song learning. Proc. R. Soc. B 285:20180849. doi: 10.1098/rspb.2018.0849, PMID: 30051835
Cornez G. Langro J. Cornil C. A. Balthazart J. Lynch K. S. (2020b). Comparing perineuronal nets and parvalbumin development between blackbird species with differences in early developmental song exposure. J. Exp. Biol. 223:jeb. 212910. doi: 10.1242/jeb.212910, PMID: 31767738
Cornez G. Madison F. N. Van Der Linden A. Cornil C. Yoder K. M. Ball G. F. et al. (2017). Perineuronal nets and vocal plasticity in songbirds: a proposed mechanism to explain the difference between closed-ended and open-ended learning: perineuronal nets and singing plasticity in songbirds. Devel Neurobio 77, 975–994. doi: 10.1002/dneu.22485, PMID: 28170164
Cornez G. Ter Haar S. M. Cornil C. A. Balthazart J. (2015). Anatomically discrete sex differences in neuroplasticity in Zebra finches as reflected by Perineuronal nets. PLoS One 10:e0123199. do i: 10.1371/journal.pone.0123199. doi: 10.1371/journal.pone.0123199, PMID: 25848776
Cornez G. Valle S. Santos E. B. dos, Chiver I. Müller W. Ball G. F. et al. (2021). Perineuronal nets in HVC and plasticity in male canary song. PLoS One 16:e0252560. doi: 10.1371/journal.pone.0252560, PMID: 34449793
del Río J. A. de Lecea L. Ferrer I. Soriano E. (1994). The development of parvalbumin-immunoreactivity in the neocortex of the mouse. Dev. Brain Res. 81, 247–259. doi: 10.1016/0165-3806(94)90311-5, PMID: 7813046
Deng X. Gu L. Sui N. Guo J. Liang J. (2019). Parvalbumin interneuron in the ventral hippocampus functions as a discriminator in social memory. Proc. Natl. Acad. Sci. U. S. A. 116, 16583–16592. doi: 10.1073/pnas.1819133116, PMID: 31358646
Dityatev A. Brückner G. Dityateva G. Grosche J. Kleene R. Schachner M. (2007). Activity-dependent formation and functions of chondroitin sulfate-rich extracellular matrix of perineuronal nets. Devel Neurobio 67, 570–588. doi: 10.1002/dneu.20361, PMID: 17443809
Doupe A. J. Perkel D. J. Reiner A. Stern E. A. (2005). Birdbrains could teach basal ganglia research a new song. Trends Neurosci. 28, 353–363. doi: 10.1016/j.tins.2005.05.005, PMID: 15935486
Enwright J. F. Sanapala S. Foglio A. Berry R. Fish K. N. Lewis D. A. (2016). Reduced labeling of parvalbumin neurons and perineuronal nets in the dorsolateral prefrontal cortex of subjects with schizophrenia. Neuropsychopharmacology 41, 2206–2214. doi: 10.1038/npp.2016.24
Fader S. M. Imaizumi K. Yanagawa Y. Lee C. C. (2016). Wisteria floribunda agglutinin-labeled perineuronal nets in the mouse inferior colliculus, thalamic reticular nucleus and auditory cortex. Brain Sci. 6:13. doi: 10.3390/brainsci6020013, PMID: 27089371
Favuzzi E. Marques-Smith A. Deogracias R. Winterflood C. M. Sánchez-Aguilera A. Mantoan L. et al. (2017). Activity-dependent gating of parvalbumin interneuron function by the perineuronal net protein Brevican. Neuron 95, 639–655.e10. doi: 10.1016/j.neuron.2017.06.028, PMID: 28712654
Gobes S. M. H. Jennings R. B. Maeda R. K. (2019). The sensitive period for auditory-vocal learning in the zebra finch: consequences of limited-model availability and multiple-tutor paradigms on song imitation. Behav. Process. 163, 5–12. doi: 10.1016/j.beproc.2017.07.007, PMID: 28743517
Gogola J. V. Gores E. O. London S. E. (2019). Inhibitory cell populations depend on age, sex, and prior experience across a neural network for critical period learning. Sci. Rep. 9:19867. doi: 10.1038/s41598-019-56293-2, PMID: 31882750
Hara E. Rivas M. V. Ward J. M. Okanoya K. Jarvis E. D. (2012). Convergent differential regulation of parvalbumin in the brains of vocal learners. PLoS One 7:e29457. doi: 10.1371/journal.pone.0029457, PMID: 22238614
Hensch T. K. Fagiolini M. Mataga N. Stryker M. P. Baekkeskov S. Kash S. F. (1998). Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science 282, 1504–1508. doi: 10.1126/science.282.5393.1504, PMID: 9822384
Horn G. (2004). Pathways of the past: the imprint of memory. Nat. Rev. Neurosci. 5, 108–120. doi: 10.1038/nrn1324, PMID: 14735114
Hou X. Yoshioka N. Tsukano H. Sakai A. Miyata S. Watanabe Y. et al. (2017). Chondroitin sulfate is required for onset and offset of critical period plasticity in visual cortex. Sci. Rep. 7:12646. doi: 10.1038/s41598-017-04007-x
Hu H. Gan J. Jonas P. (2014). Fast-spiking, parvalbumin+ GABAergic interneurons: from cellular design to microcircuit function. Science 345:1255263. doi: 10.1126/science.1255263, PMID: 25082707
Kinney J. W. Davis C. N. Tabarean I. Conti B. Bartfai T. Behrens M. M. (2006). A specific role for NR2A-containing NMDA receptors in the maintenance of parvalbumin and GAD67 immunoreactivity in cultured interneurons. J. Neurosci. 26, 1604–1615. do i: 10.1523/JNEUROSCI.4722-05.2006. doi: 10.1523/JNEUROSCI.4722-05.2006, PMID: 16452684
Kumar S. Mohapatra A. N. Pundir A. S. Kumari M. Din U. Sharma S. et al. (2020). Blocking opioid receptors in a songbird cortical region modulates the acoustic features and levels of female-directed singing. Front. Neurosci. 14:554094. doi: 10.3389/fnins.2020.554094, PMID: 33071736
Leblois A. Perkel D. J. (2020). “The Song circuit as a model of basal ganglia function” in The neuroethology of birdsong springer handbook of auditory research. eds. Sakata J. T. Woolley S. C. Fay R. R. Popper A. N. (Cham: Springer International Publishing), 93–125.
Lensjø K. K. Lepperød M. E. Dick G. Hafting T. Fyhn M. (2017). Removal of perineuronal nets unlocks juvenile plasticity through network mechanisms of decreased inhibition and increased gamma activity. J. Neurosci. 37, 1269–1283. do i: 10.1523/JNEUROSCI.2504-16.2016. doi: 10.1523/JNEUROSCI.2504-16.2016, PMID: 28039374
Liu H. Gao P.-F. Xu H.-W. Liu M.-M. Yu T. Yao J.-P. et al. (2013). Perineuronal nets increase inhibitory GABAergic currents during the critical period in rats. Int. J. Ophthalmol. 6, 120–125. doi: 10.3980/j.issn.2222-3959.2013.02.02, PMID: 23638408
Lupori L. Totaro V. Cornuti S. Ciampi L. Carrara F. Grilli E. et al. (2023). A comprehensive atlas of perineuronal net distribution and colocalization with parvalbumin in the adult mouse brain. Cell Rep. 42:112788. doi: 10.1016/j.celrep.2023.112788, PMID: 37436896
Miranda J. M. Cruz E. Bessières B. Alberini C. M. (2022). Hippocampal parvalbumin interneurons play a critical role in memory development. Cell Rep. 41:111643. doi: 10.1016/j.celrep.2022.111643, PMID: 36384113
Murphy K. Lawley K. S. Smith P. Prather J. F. (2020). “New insights into the avian song system and neuronal control of learned vocalizations” in The neuroethology of birdsong, springer handbook of auditory research. eds. Sakata J. T. Woolley S. C. Fay R. R. Popper A. N., vol. 71 (Cham: Springer International Publishing), 65–92.
Murray A. J. Woloszynowska-Fraser M. U. Ansel-Bollepalli L. Cole K. L. H. Foggetti A. Crouch B. et al. (2015). Parvalbumin-positive interneurons of the prefrontal cortex support working memory and cognitive flexibility. Sci. Rep. 5:16778. doi: 10.1038/srep16778, PMID: 26608841
Olson C. R. Hodges L. K. Mello C. V. (2015). Dynamic gene expression in the song system of zebra finches during the song learning period: ontogeny of Song system gene expression. Devel Neurobio 75, 1315–1338. doi: 10.1002/dneu.22286, PMID: 25787707
Pfenning A. R. Hara E. Whitney O. Rivas M. V. Wang R. Roulhac P. L. et al. (2014). Convergent transcriptional specializations in the brains of humans and song-learning birds. Science 346:1256846. doi: 10.1126/science.125684, PMID: 25504733
Pizzorusso T. Medini P. Berardi N. Chierzi S. Fawcett J. W. Maffei L. (2002). Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298, 1248–1251. doi: 10.1126/science.1072699
Pyka M. Wetzel C. Aguado A. Geissler M. Hatt H. Faissner A. (2011). Chondroitin sulfate proteoglycans regulate astrocyte-dependent synaptogenesis and modulate synaptic activity in primary embryonic hippocampal neurons. Eur. J. Neurosci. 33, 2187–2202. doi: 10.1111/j.1460-9568.2011.07690.x, PMID: 21615557
Reiner A. Laverghetta A. V. Meade C. A. Cuthbertson S. L. Bottjer S. W. (2004). An immunohistochemical and pathway tracing study of the striatopallidal organization of area X in the male zebra finch. J. Comp. Neurol. 469, 239–261. doi: 10.1002/cne.11012, PMID: 14694537
Rowlands D. Lensjø K. K. Dinh T. Yang S. Andrews M. R. Hafting T. et al. (2018). Aggrecan directs extracellular matrix-mediated neuronal plasticity. J. Neurosci. 38, 10102–10113. doi: 10.1523/JNEUROSCI.1122-18.2018, PMID: 30282728
Sakata J. T. Woolley S. C. (2020). “Scaling the levels of birdsong analysis” in The neuroethology of birdsong springer handbook of auditory research. eds. Sakata J. T. Woolley S. C. Fay R. R. Popper A. N. (Cham: Springer International Publishing), 1–27.
Sakata J. T. Woolley S. C. (2022). The role of parvalbumin neurons in the evolution of skilled behaviours. PLoS Biol. 20:e3001795. doi: 10.1371/journal.pbio.3001795, PMID: 36129902
Sakata J. T. Yazaki-Sugiyama Y. (2020). “Neural circuits underlying vocal learning in songbirds” in The neuroethology of birdsong springer handbook of auditory research. eds. Sakata J. T. Woolley S. C. Fay R. R. Popper A. N., vol. 71 (Cham: Springer International Publishing), 29–63.
Schuppe E. R. Cantin L. Chakraborty M. Biegler M. T. Jarvis E. R. Chen C.-C. et al. (2022). Forebrain nuclei linked to woodpecker territorial drum displays mirror those that enable vocal learning in songbirds. PLoS Biol. 20:e3001751. doi: 10.1371/journal.pbio.3001751, PMID: 36125990
Shi W. Wei X. Wang X. Du S. Liu W. Song J. et al. (2019). Perineuronal nets protect long-term memory by limiting activity-dependent inhibition from parvalbumin interneurons. Proc. Natl. Acad. Sci. U. S. A. 116, 27063–27073. doi: 10.1073/pnas.1902680116
Slaker M. L. Jorgensen E. T. Hegarty D. M. Liu X. Kong Y. Zhang F. et al. (2018). Cocaine exposure modulates perineuronal nets and synaptic excitability of fast-spiking interneurons in the medial prefrontal cortex. eNeuro 5:ENEURO.0221-18.2018. doi: 10.1523/ENEURO.0221-18.2018, PMID: 30294670
Sohal V. S. Zhang F. Yizhar O. Deisseroth K. (2009). Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459, 698–702. doi: 10.1038/nature07991, PMID: 19396159
Spatazza J. Lee H. H. C. Di Nardo A. A. Tibaldi L. Joliot A. Hensch T. K. et al. (2013). Choroid-plexus-derived Otx2 homeoprotein constrains adult cortical plasticity. Cell Rep. 3, 1815–1823. doi: 10.1016/j.celrep.2013.05.014, PMID: 23770240
Spiro J. E. Dalva M. B. Mooney R. (1999). Long-range inhibition within the zebra finch song nucleus RA can coordinate the firing of multiple projection neurons. J. Neurophysiol. 81, 3007–3020. doi: 10.1152/jn.1999.81.6.3007, PMID: 10368416
Sugiyama S. Di Nardo A. A. Aizawa S. Matsuo I. Volovitch M. Prochiantz A. et al. (2008). Experience-dependent transfer of Otx2 homeoprotein into the visual cortex activates postnatal plasticity. Cells 134, 508–520. doi: 10.1016/j.cell.2008.05.054, PMID: 18692473
Takesian A. E. Hensch T. K. (2013). Balancing plasticity/stability across brain development. Prog Brain Res 207, 3–34. doi: 10.1016/B978-0-444-63327-9.00001-1, PMID: 24309249
Tewari B. P. Chaunsali L. Campbell S. L. Patel D. C. Goode A. E. Sontheimer H. (2018). Perineuronal nets decrease membrane capacitance of peritumoral fast spiking interneurons in a model of epilepsy. Nat. Commun. 9:4724. doi: 10.1038/s41467-018-07113-0, PMID: 30413686
Wang D. Fawcett J. (2012). The perineuronal net and the control of CNS plasticity. Cell Tissue Res. 349, 147–160. doi: 10.1007/s00441-012-1375-y, PMID: 22437874
Wild J. M. Williams M. N. Howie G. J. Mooney R. (2005). Calcium-binding proteins define interneurons in HVC of the zebra finch (Taeniopygia guttata). J. Comp. Neurol. 483, 76–90. doi: 10.1002/cne.20403, PMID: 15672397
Wild J. M. Williams M. N. Suthers R. A. (2001). Parvalbumin-positive projection neurons characterise the vocal premotor pathway in male, but not female, zebra finches. Brain Res. 917, 235–252. doi: 10.1016/S0006-8993(01)02938-9 PMID: 11640910
Wöhr M. Orduz D. Gregory P. Moreno H. Khan U. Vörckel K. J. et al. (2015). Lack of parvalbumin in mice leads to behavioral deficits relevant to all human autism core symptoms and related neural morphofunctional abnormalities. Transl. Psychiatry 5:e525. doi: 10.1038/tp.2015.19, PMID: 25756808
Woolley S. C. (2016). Social context differentially modulates activity of two interneuron populations in an avian basal ganglia nucleus. J. Neurophysiol. 116, 2831–2840. doi: 10.1152/jn.00622.2016, PMID: 27628208
Woolley S. C. Woolley S. M. N. (2020). “Integrating form and function in the songbird auditory forebrain” in The neuroethology of birdsong springer handbook of auditory research. eds. Sakata J. T. Woolley S. C. Fay R. R. Popper A. N. (Cham: Springer International Publishing), 127–155.
Xia F. Richards B. A. Tran M. M. Josselyn S. A. Takehara-Nishiuchi K. Frankland P. W. (2017). Parvalbumin-positive interneurons mediate neocortical-hippocampal interactions that are necessary for memory consolidation. elife 6:e27868. doi: 10.7554/eLife.27868
Xiang L. Wu Q. Sun H. Miao X. Lv Z. Liu H. et al. (2022). SARM1 deletion in parvalbumin neurons is associated with autism-like behaviors in mice. Cell Death Dis. 13, 638–611. doi: 10.1038/s41419-022-05083-2, PMID: 35869039
Xue M. Atallah B. V. Scanziani M. (2014). Equalizing excitation–inhibition ratios across visual cortical neurons. Nature 511, 596–600. doi: 10.1038/nature13321, PMID: 25043046
Yamada J. Jinno S. (2013). Spatio-temporal differences in perineuronal net expression in the mouse hippocampus, with reference to parvalbumin. Neuroscience 253, 368–379. doi: 10.1016/j.neuroscience.2013.08.061, PMID: 24016683
Yamada J. Ohgomori T. Jinno S. (2015). Perineuronal nets affect parvalbumin expression in GABAergic neurons of the mouse hippocampus. Eur. J. Neurosci. 41, 368–378. doi: 10.1111/ejn.12792, PMID: 25411016
Zengin-Toktas Y. Woolley S. C. (2017). Singing modulates parvalbumin interneurons throughout songbird forebrain vocal control circuitry. PLoS One 12:e0172944. doi: 10.1371/journal.pone.0172944