The impact of early environmental interventions on structural plasticity of the axon initial segment in neocortex

Nozari, Masoumeh; Suzuki, Toshimitsu; Rosa, Marcello G. P.; Yamakawa, Kazuhiro; Atapour, Nafiseh

doi:10.1002/dev.21453

Cited by 12 publications

(12 citation statements)

References 88 publications

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“…Our data adds to the literature by showing that brief exposure to MK-801 on the second week of life is enough to induce changes in GABAergic transmission as early as P21-28. This is consistent with increasing evidence supporting that postnatal NMDA antagonism during periods of rapid synaptogenesis significantly affects development of inhibitory transmission (Abekawa et al, 2007;Gu et al, 2016;Jones et al, 2014;Nozari et al, 2017;Roux et al, 2015).…”

Section: Discussionsupporting

confidence: 91%

Modifications of inhibitory transmission onto pyramidal neurons by postnatal exposure to MK‐801: Effects of enriched environment

Shojaei

Anaraki

Mirnajafi‐Zadeh

et al. 2017

Intl J of Devlp Neuroscience

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Early enriched environment (EE) prevents several deficits associated with postnatal MK-801 [N-Methyl-d-Aspartate (NMDA) receptor antagonist] treatment such as cognitive and locomotor deficits. We sought physiological correlates to such changes by looking at inhibitory synaptic inputs onto pyramidal cells in a prefrontal cortex slice preparation. Pharmacologically isolated γ-amino-butyric acid (GABA) receptor-mediated currents were measured using whole-cell patch clamp recordings. Wistar rats were raised in standard or EE from birth up to the time of experiments and were injected with saline or MK-801 (1mg/kg) on postnatal days (P) 6-10. We recorded miniature inhibitory post-synaptic currents (mIPSCs) of pyramidal cells in layer II/III of prefrontal cortex and measured their frequency, amplitude and kinetics. In control animals, the amplitude and frequency of mIPSCs increased strikingly during development from P21 to P28. MK-801 accelerated the development of mIPSCs frequency but caused a significant decrease in the amplitude of mIPSCs on P28 suggesting a significant reduction of inhibition onto pyramidal cells. EE per se led to a significant increase in both frequency and amplitude of mIPSCs, but its application to MK-801-treated rats resulted in moderate rescue of GABAergic transmission on P28. We conclude that postnatal MK-801 leads to reduced inhibitory transmission onto pyramidal cells of prefrontal cortex at adolescence which may underlie behavioural and morphological differences detected in vivo in rats. EE presentation from birth rather prevents GABAergic alterations associated with postnatal MK-801 treatment at adolescence.

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Section: Discussionsupporting

confidence: 91%

Modifications of inhibitory transmission onto pyramidal neurons by postnatal exposure to MK‐801: Effects of enriched environment

Shojaei

Anaraki

Mirnajafi‐Zadeh

et al. 2017

Intl J of Devlp Neuroscience

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“…Also, rapid dendritic growth is related with maturity of glutamatergic and GABA-ergic receptors (257, 258), making dendritic differentiation more prone to environmental influences. As such, for the development of early maturing neurons, as is the case for L3N, already during the perinatal and early postnatal period, the environment has an important role in regulating their morphological differentiation (259–263).…”

Section: Sequential Differentiation Of Principal Neurons In the Prefrmentioning

confidence: 99%

The Protracted Maturation of Associative Layer IIIC Pyramidal Neurons in the Human Prefrontal Cortex During Childhood: A Major Role in Cognitive Development and Selective Alteration in Autism

et al. 2019

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The human specific cognitive shift starts around the age of 2 years with the onset of self-awareness, and continues with extraordinary increase in cognitive capacities during early childhood. Diffuse changes in functional connectivity in children aged 2–6 years indicate an increase in the capacity of cortical network. Interestingly, structural network complexity does not increase during this time and, thus, it is likely to be induced by selective maturation of a specific neuronal subclass. Here, we provide an overview of a subclass of cortico-cortical neurons, the associative layer IIIC pyramids of the human prefrontal cortex. Their local axonal collaterals are in control of the prefrontal cortico-cortical output, while their long projections modulate inter-areal processing. In this way, layer IIIC pyramids are the major integrative element of cortical processing, and changes in their connectivity patterns will affect global cortical functioning. Layer IIIC neurons have a unique pattern of dendritic maturation. In contrast to other classes of principal neurons, they undergo an additional phase of extensive dendritic growth during early childhood, and show characteristic molecular changes. Taken together, circuits associated with layer IIIC neurons have the most protracted period of developmental plasticity. This unique feature is advanced but also provides a window of opportunity for pathological events to disrupt normal formation of cognitive circuits involving layer IIIC neurons. In this manuscript, we discuss how disrupted dendritic and axonal maturation of layer IIIC neurons may lead into global cortical disconnectivity, affecting development of complex communication and social abilities. We also propose a model that developmentally dictated incorporation of layer IIIC neurons into maturing cortico-cortical circuits between 2 to 6 years will reveal a previous (perinatal) lesion affecting other classes of principal neurons. This “disclosure” of pre-existing functionally silent lesions of other neuronal classes induced by development of layer IIIC associative neurons, or their direct alteration, could be found in different forms of autism spectrum disorders. Understanding the gene-environment interaction in shaping cognitive microcircuitries may be fundamental for developing rehabilitation and prevention strategies in autism spectrum and other cognitive disorders.

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“…To explain the results in the hippocampus, it was suggested that the increase of the AIS length of Ube3a model mice might reflect a homeostatic response to a reduction in neuronal excitability, driven by the increase of α1-NaKA expression ( Kaphzan et al, 2011 , 2013 ). It has been well established that the AIS is a dynamic structure, and that the expression of sodium channels can depend on input activity ( Grubb and Burrone, 2010 ; Kuba et al, 2010 , 2014 , 2015 ; Gutzmann et al, 2014 ; Nozari et al, 2017 ). It is remarkable that the increase in AIS length was associated with a more negative membrane potential, both at hippocampal CA1 pyramidal neurons ( Kaphzan et al, 2011 ) and in the present study, since a chronic depolarization induces a rapid change in AIS length in cultured neurons ( Evans et al, 2015 ).…”

Section: Discussionmentioning

confidence: 99%

Enhanced Transmission at the Calyx of Held Synapse in a Mouse Model for Angelman Syndrome

Wang

Woerden

Elgersma

et al. 2018

Front. Cell. Neurosci.

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The neurodevelopmental disorder Angelman syndrome (AS) is characterized by intellectual disability, motor dysfunction, distinct behavioral aspects, and epilepsy. AS is caused by a loss of the maternally expressed UBE3A gene, and many of the symptoms are recapitulated in a Ube3a mouse model of this syndrome. At the cellular level, changes in the axon initial segment (AIS) have been reported, and changes in vesicle cycling have indicated the presence of presynaptic deficits. Here we studied the role of UBE3A in the auditory system by recording synaptic transmission at the calyx of Held synapse in the medial nucleus of the trapezoid body (MNTB) through in vivo whole cell and juxtacellular recordings. We show that MNTB principal neurons in Ube3a mice exhibit a hyperpolarized resting membrane potential, an increased action potential (AP) amplitude and a decreased AP half width. Moreover, both the pre- and postsynaptic AP in the calyx of Held synapse of Ube3a mice showed significantly faster recovery from spike depression. An increase in AIS length was observed in the principal MNTB neurons of Ube3a mice, providing a possible substrate for these gain-of-function changes. Apart from the effect on APs, we also observed that EPSPs showed decreased short-term synaptic depression (STD) during long sound stimulations in AS mice, and faster recovery from STD following these tones, which is suggestive of a presynaptic gain-of-function. Our findings thus provide in vivo evidence that UBE3A plays a critical role in controlling synaptic transmission and excitability at excitatory synapses.

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The impact of early environmental interventions on structural plasticity of the axon initial segment in neocortex

Cited by 12 publications

References 88 publications

Modifications of inhibitory transmission onto pyramidal neurons by postnatal exposure to MK‐801: Effects of enriched environment

Modifications of inhibitory transmission onto pyramidal neurons by postnatal exposure to MK‐801: Effects of enriched environment

The Protracted Maturation of Associative Layer IIIC Pyramidal Neurons in the Human Prefrontal Cortex During Childhood: A Major Role in Cognitive Development and Selective Alteration in Autism

Enhanced Transmission at the Calyx of Held Synapse in a Mouse Model for Angelman Syndrome

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