Early brain wiring: activity-dependent processes

Penn, A. A.

doi:10.1093/oxfordjournals.schbul.a006880

Cited by 37Neuroscience and Neuropharmacology ResearchNeurogenesis and neuroplasticity mechanismsVisual perception and processing mechanisms

Early brain wiring: activity-dependent processes

Penn, A. A.·2001·Schizophrenia Bulletin

DOI 10.1093/oxfordjournals.schbul.a006880

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Abstract

One of the leading theories of the neuropathology of schizophrenia is that it is a developmental disorder of "neural connectivity." To assess this theory, it is first necessary to understand how precise neural connections normally are established. Sensory-driven neural activity has been widely recognized as crucial for this process. Recent studies have revealed a similar requirement for endogenous neural activity generated by the nervous system itself, long before there is any sensory input. These patterns of sensory-driven and endogenously generated neural activity sculpt the precise circuits that are crucial to the many complex functions of the adult brain. This article summarizes the principles of activity-dependent neural development as determined from basic neuroscience experiments, particularly those done using the mammalian visual system, to illustrate the role of patterned activity, neuronal competition, and critical periods in shaping neural circuitry. The potential molecular mechanisms involved in these features of activity-dependent neurodevelopment are discussed and possible links to the etiology of schizophrenia are briefly explored.

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PNNs mature gradually in an experience-dependent manner during late postnatal development, overlapping with the prodromal period and age of onset of schizophrenia.
“PNNs gradually mature in an experience-dependent manner during late stages of postnatal development, overlapping with the prodromal period/age of onset of schizophrenia.”
From Losing the sugar coating: Potential impact of perineuronal net abnormalities on interneurons in schizophrenia (2015) · cites this paper as Penn, 2001
In human and non-human primates, these ECM maturation events span adolescence and early adulthood, potentially coinciding with the prodromal period and onset of schizophrenia.
“Relevant to the pathophysiology of SZ, in human and non-human primates these events span across adolescence and early adulthood, potentially coinciding with the prodromal period and onset of SZ (Hensch, 2004; Penn, 2001; Sturman and Moghaddam, 2011).”
From Losing the sugar coating: Potential impact of perineuronal net abnormalities on interneurons in schizophrenia (2015) · cites this paper as Penn, 2001

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Prieto‐Lloret, J., Caceres, A. I., Obeso, A., Rocher, A., Rigual, R. J., Agapito, M. T., Bustamante, R., Castañeda, J., Pérez-García, M. T., López‐López, J. R., et al. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.049445 · Cited by 42 · see citing works
“It is well known that the presence of normal neural activity is essential for the formation and maintenance of a mature system of neural connections (Kaas 1995; Katz & Shatz 1996; Crair 1999; Personius & Balice-Gordon 2000; Penn 2001).”
Background
Early Visual Development: Implications for the Neonatal Intensive Care Unit and Care
Graven, S. N. (2011) · Clinics in Perinatology · doi:10.1016/j.clp.2011.08.006 · Cited by 41 · see citing works
MiR-223 regulates the differentiation of immature neurons
Harraz, M. M., Xu, J., Guiberson, N. G. L., Dawson, T. M., & Dawson, V. L. (2014) · Molecular and Cellular Therapies · doi:10.1186/2052-8426-2-18 · Cited by 32 · see citing works
“Post-transcriptional gene expression regulation is required for neuronal network formation including dendrite growth, branching and neuronal activity [33].”
Phosphenes, retinal discrete dark noise, negative afterimages and retinogeniculate projections: A new explanatory framework based on endogenous ocular luminescence
Salari, V., Scholkmann, F., Vimal, R. L. P., Császár, N., Aslani, M., & Bókkon, I. (2017) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2017.07.001 · Cited by 28 · see citing works
“It has been suggested that this shapes appropriately patterned circuits (Penn, 2001).”
Developmental biomarkers in schizophrenia and other psychiatric disorders: common origins, different trajectories?
Keshavan, M. S., Diwadkar, V. A., & Rosenberg, D. (2005) · Epidemiology and Psychiatric Sciences · doi:10.1017/s1121189x00007934 · Cited by 28 · see citing works
“Developmental changes in neurobiology also depend on patterns of gene- (Lesch, 2004) and behavior-environment interactions (Penn, 2001; Ramakers, 2005).”
Background
Altered brain gene expression but not steroid biochemistry in a genetic mouse model of neurodevelopmental disorder
Trent, S., Fry, J. P., Ojarikre, O. A., & Davies, W. (2014) · Molecular Autism · doi:10.1186/2040-2392-5-21 · Cited by 26 · see citing works
“As sulphated and non-sulphated steroid hormones can act as modulators at key neurotransmitter receptors, including N-methyl-D-aspartic acid (NMDA) and γ-aminobutyric acid type A (GABAA) receptors [9], lack of STS developmentally could potentially elicit important effects on neuronal organisation processes mediated by…”
Background
The Placenta: The Lost Neuroendocrine Organ
Pașca, A. M., & Penn, A. A. (2010) · NeoReviews · doi:10.1542/neo.11-2-e64 · Cited by 24 · see citing works
“(9) Despite major efforts, these prevalent, debilitating, lifelong disorders remain biologically unexplained.”
Background
Building a circuit through correlated spontaneous neuronal activity in the developing vertebrate and invertebrate visual systemsPreprint
Choi, B. J., Chen, Y., & Desplan, C. (2021) · Genes & Development · doi:10.1101/gad.348241.121 · Cited by 24 · see citing works
“During synaptogenesis, neuronal activity across neuronal networks shapes and refines the circuit to a more mature form that is optimized for various external sensory stimuli (Penn 2001; Ganguly and Poo 2013).”
Background
Genetic background mutations drive neural circuit hyperconnectivity in a fragile X syndrome model
Kennedy, T., Rinker, D. C., & Broadie, K. S. (2020) · BMC Biology · doi:10.1186/s12915-020-00817-0 · Cited by 19 · see citing works
Dysregulation of auditory neuroplasticity in schizophrenia
Voss, P., Thomas, M. E., Guercio, G. D., & de Villers‐Sidani, E. (2018) · Schizophrenia Research · doi:10.1016/j.schres.2018.04.025 · Cited by 21 · see citing works
Delayed onset of prepulse inhibition deficits following kainic acid treatment on postnatal day 7 in rats
Howland, J. G., Hannesson, D. K., & Phillips, A. G. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03731.x · Cited by 19 · see citing works
“…is rarely observed in the brains of patients with schizophrenia (but see Stevens, 1994), therefore alterations in normal patterns of connectivity between affected brain areas may underlie the expression of some symptoms of schizophrenia (Friston, 1999; Harrison, 1999; Benes, 2000; Penn, 2001).”
Background
Behavioral and stereological characterization of Hdc KO mice: Relation to Tourette syndrome
Abdurakhmanova, S., Chary, K., Kettunen, M. I., Sierra, A., & Panula, P. (2017) · The Journal of Comparative Neurology · doi:10.1002/cne.24279 · Cited by 17 · see citing works
“Current research on brain development and wiring has revealed an important role of activity-dependent plasticity and neural differentiation by endogenous or sensory input induced neural activity (Murphy, 2003; Penn, 2001).”
Background
The impact of extrauterine life on visual maturation in extremely preterm born infants
Schwindt, E. M., Giordano, V., Róna, Z., Czaba, C., Olischar, M., Waldhoer, T., Werther, T., Fuiko, R., Berger, A., & Klebermaß-Schrehof, K. (2018) · Pediatric Research · doi:10.1038/s41390-018-0084-y · Cited by 18 · see citing works
Temperature regulates synaptic subcellular specificity mediated by inhibitory glutamate signaling
Wang, M., Witvliet, D. K., Wu, M., Kang, L., & Shao, Z. (2021) · PLoS Genetics · doi:10.1371/journal.pgen.1009295 · Cited by 14 · see citing works
“Neuronal activity plays critical roles in neural circuitry development [18,19].”
Background
Epigenetics and Allostasis
Walsh, A., & Yun, I. (2014) · Criminal Justice Review · doi:10.1177/0734016814530148 · Cited by 13 · see citing works
“This process is encapsulated in neuroscience’s pithy saying: ‘‘The neurons that fire together, wire together; those that don’t, won’t’’ (Penn, 2001, p. 339).”
Background
Dynamic regulation of excitatory and inhibitory synaptic transmission by growth hormone in the developing mouse brain
Li, G., Wu, Q.-Z., Song, T.-J., Zhen, X.-C., & Yu, X. (2022) · Acta Pharmacologica Sinica · doi:10.1038/s41401-022-01027-w · Cited by 11 · see citing works
Principles of endogenous and sensory activity-dependent brain development: the visual system
Penn, A. A., & Shatz, C. J. (2010) · Cambridge University Press eBooks · doi:10.1017/cbo9780511711848.012 · Cited by 11 · see citing works
In vivo methylmercury exposure induced long-lasting epileptiform activity in layer II/III neurons in cortical slices from the rat
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“…specific formation and elimination of certain synapses between neurons located in the same or different cortical layers (for review, see Katz and Shatz, 1996; Hohnke and Sur, 1999; Sur et al., 1999; Penn, 2001; Grubb, 2004; Sur and Rubenstein, 2005; Majewska and Sur, 2006; Marsh et al., 2008).”
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Wiring of the brain
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Cellular and Molecular Mechanisms Underlying Synaptic Subcellular Specificity
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Investigating Techniques to Help Early English Language Learners Prepare for Kindergarten
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Authors: Penn, A. A.
Affiliations: Lucile Packard Children's Hospital (US)
Corresponding author: Penn, A. A.
ORCID: Penn, A. A.
Venue: Schizophrenia Bulletin
Publisher: Oxford University Press (OUP)
Published: 2001-01-01
Volume: 27
Issue: 3
Pages: 337-347
ISSN: 0586-7614 (ISSN-L)
1745-1701
DOI: 10.1093/oxfordjournals.schbul.a006880
OpenAlex: W2151702145
Cited by: 37
References: 88
Citations by year: 2024: 2 · 2022: 1 · 2021: 3 · 2020: 1 · 2019: 1 · 2018: 3 · 2017: 2 · 2015: 1 · 2014: 3 · 2013: 1 · 2012: 2
FWCI: 0.17
Type: journal article
Language: en
Open access: closed
Locations: Schizophrenia Bulletin (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
Keywords: etiology of schizophrenia
MeSH terms: Cyclic AMP, Axons, Brain, gamma-Aminobutyric Acid, Geniculate Bodies, Humans, Nerve Growth Factors, Nerve Net, Retinal Ganglion Cells, Schizophrenia, Synapses, Visual Cortex, N-Methylaspartate

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