Elsevier

Neuroscience

Volume 368, 1 January 2018, Pages 256-267
Neuroscience

Review
Neuronal Activity Patterns in the Developing Barrel Cortex

https://doi.org/10.1016/j.neuroscience.2017.05.025Get rights and content

Highlights

  • Electrical activity plays an important role in neonatal barrel cortex.

  • Spindle bursts and early gamma oscillations synchronize local columnar networks.

  • Disturbances in early activity cause cortical disorganization.

Abstract

The developing barrel cortex reveals a rich repertoire of neuronal activity patterns, which have been also found in other sensory neocortical areas and in other species including the somatosensory cortex of preterm human infants. The earliest stage is characterized by asynchronous, sparse single-cell firing at low frequencies. During the second stage neurons show correlated firing, which is initially mediated by electrical synapses and subsequently transforms into network bursts depending on chemical synapses. Activity patterns during this second stage are synchronous plateau assemblies, delta waves, spindle bursts and early gamma oscillations (EGOs). In newborn rodents spindle bursts and EGOs occur spontaneously or can be elicited by sensory stimulation and synchronize the activity in a barrel-related columnar network with topographic organization at the day of birth. Interfering with this early activity causes a disturbance in the development of the cortical architecture, indicating that spindle bursts and EGOs influence the formation of cortical columns. Early neuronal activity also controls the rate of programed cell death in the developing barrel cortex, suggesting that spindle bursts and EGOs are physiological activity patterns particularly suited to suppress apoptosis. It remains to be studied in more detail how these different neocortical activity patterns control early developmental processes such as formation of synapses, microcircuits, topographic maps and large-scale networks.

Introduction

It is well accepted that electrical activity plays a very important role in the developing brain. During so-called critical periods brain regions processing sensory information (specific brainstem and thalamic nuclei, sensory neocortical areas) undergo substantial structural and functional modifications based on the electrical activity arising from the sensory periphery (for review Erzurumlu and Gaspar, 2012, Espinosa and Stryker, 2012, Kral, 2013). These experience-dependent modifications occur at the synaptic as well as at the large-scale network level. It is often ignored that the brain reveals complex electrical activity patterns during prenatal and early postnatal development, clearly before sensory experience gained through the exploration modifies neuronal circuits during the critical periods. Although the concept for the existence of a precritical period has emerged over the last decade (for review Feller and Scanziani, 2005, Khazipov and Luhmann, 2006, Blankenship and Feller, 2010), the complexity and the role of spontaneous and evoked activity patterns during earliest stages of brain development has been addressed in detail only more recently. In the spinal cord and in supraspinal circuits electrical activity is evident from the beginning of development and controls cell generation versus cell death, differentiation, axonal guidance, synapse formation, neurotransmitter specification, and the development of early circuits (for review Sanes and Lichtman, 1999, Schouenborg, 2004, Borodinsky et al., 2012, Blumberg et al., 2013, Spitzer, 2015). In the visual system, spontaneous retinal activity (“retinal waves”) triggers cortical activity and controls the formation of retinotopic maps before eye opening (Hanganu et al., 2006, Colonnese and Khazipov, 2010, Colonnese et al., 2010, Ackman et al., 2012, Xu et al., 2015). In the auditory system, spontaneous activity is present in the cochlea at early stages before hearing onset (Tritsch et al., 2007, Johnson et al., 2011, Wang et al., 2015) and controls the development of central auditory pathways. An important role of early spontaneous and evoked activity patterns has been also demonstrated in the developing somatosensory thalamocortical system and it becomes more and more evident that synchronized electrical activity is an important regulator of various ontogenetic processes during earliest stages of sensory system development (for review Hanganu-Opatz, 2010, Kilb et al., 2011, Sieben et al., 2013, Luhmann et al., 2016).

Since spontaneous and evoked activity patterns can be also observed in the cerebral cortex of preterm human babies even before the cortex has gained its characteristic six-layered organization (Vanhatalo et al., 2002, Milh et al., 2007, Tolonen et al., 2007, Chipaux et al., 2013, Omidvarnia et al., 2014) (for review Colonnese and Khazipov, 2012), it is also of pivotal clinical interest to understand the mechanisms underlying the generation of early activity patterns and their functional role during early development. The relevance of these questions becomes even more obvious with recent clinical reports demonstrating that fetal antiepileptic drug exposure or exposure to drugs, which are routinely used in neonatal intensive care, have a prominent impact on spontaneous activity (Malk et al., 2014, Videman et al., 2014). Furthermore, increased neuronal activity in preterms correlates with a faster growth of brain structures during subsequent months (Benders et al., 2015) and changes in the pattern of spontaneous activity can be used to predict the clinical outcome of extremely preterm infants (Iyer et al., 2015).

The aim of this paper is to provide an overview on our current understanding of the development, the generation and the functional role of early neocortical activity patterns in rodents. Although we will focus on a structurally and functionally well defined subregion of the somatosensory cortex, the barrel cortex (for review Petersen, 2007, Feldmeyer et al., 2013), we will also emphasize the role of subcortical structures and the motor system in the generation of activity patterns in the barrel cortex. Specifically we will address the following questions: (1) What types of spontaneous and evoked activity patterns can be observed in the developing rodent barrel cortex? What do we know about the molecular, cellular and network mechanisms underlying the generation of these different patterns? (2) What is the role of these activity patterns in the formation of early networks and topographic maps? (3) How does electrical activity control programed cell death during early neocortical development?

Section snippets

Developmental sequence of different activity patterns in early neocortical development

Many brain structures in different species, in vertebrates as well as in invertebrates, show a similar temporal sequence in the early development of spontaneous and evoked electrical activity patterns. In rodent barrel cortex, four distinct developmental stages can be differentiated depending on the temporal and spatial organization of activity, including its local/large scale and vertical/horizontal synchronization, generative mechanisms, involvement of subcortical and intracortical

Role of early activity in network function and formation

A compelling amount of experimental data indicates that early activity plays an important role in the development of functional connectivity, topographic maps and higher-order associative circuits (for review Kirkby et al., 2013, Ackman and Crair, 2014, Okawa et al., 2014). In the developing visual system it has been documented that early neuronal activity interacts with transcriptional gene regulation to control network formation (for review Cang and Feldheim, 2013). The activity-dependent

Role of early activity in controlling apoptosis

Programed cell death (apoptosis) is an important process during early brain development (for review Fuchs and Steller, 2011). In the cerebral cortex of rodents, about 70% of the neurons die by apoptosis around E14 (Blaschke et al., 1996). A second wave of apoptosis can be observed during the first postnatal week (for review Nikolic et al., 2013), exactly during a developmental period when the cerebral cortex reveals a rich repertoire of spontaneous and evoked synchronized activity patterns. It

Perspectives

Although distinct neuronal activity patterns have been demonstrated in newborn rodent barrel cortex with various techniques under in vitro and in vivo conditions, neither their underlying mechanisms nor their functional role during early neocortical development are fully understood. It became clear that subcortical structures, other cortical areas and motor systems play a central role in the generation of certain activity patterns. It became also evident that early cortical activity patterns

Acknowledgments

The authors are most thankful to their co-workers who contributed over the last years to the results discussed in this review. Financial support for our work came from the Deutsche Forschungsgemeinschaft (H.J.L.), INSERM and the program of competitive growth of KFU (R.K.).

References (165)

  • L.A. Elias et al.

    Gap junctions: multifaceted regulators of embryonic cortical development

    Trends Neurosci

    (2008)
  • J.S. Espinosa et al.

    Uncoupling dendrite growth and patterning: single-cell knockout analysis of NMDA receptor 2B

    Neuron

    (2009)
  • J.S. Espinosa et al.

    Development and plasticity of the primary visual cortex

    Neuron

    (2012)
  • D. Feldmeyer et al.

    Barrel cortex function

    Prog Neurobiol

    (2013)
  • M.B. Feller et al.

    A precritical period for plasticity in visual cortex

    Curr Opin Neurobiol

    (2005)
  • Y. Fuchs et al.

    Programmed cell death in animal development and disease

    Cell

    (2011)
  • I.L. Hanganu-Opatz

    Between molecules and experience: role of early patterns of coordinated activity for the development of cortical maps and sensory abilities

    Brain Res Rev

    (2010)
  • S. Higashi et al.

    Prenatal development of neural excitation in rat thalamocortical projections studied by optical recording

    Neuroscience

    (2002)
  • S. Hirsch et al.

    Pathway-specificity in N-methyl-d-aspartate receptor-mediated synaptic inputs onto subplate neurons

    Neuroscience

    (2008)
  • M. Hübener et al.

    Neuronal plasticity: beyond the critical period

    Cell

    (2014)
  • C. Ikonomidou et al.

    Antiepileptic drugs and brain development

    Epilepsy Res

    (2010)
  • R. Khazipov et al.

    Early patterns of electrical activity in the developing cerebral cortex of human and rodents

    Trends Neurosci

    (2006)
  • R. Khazipov et al.

    Early gamma oscillations

    Neuroscience

    (2013)
  • S. Kirischuk et al.

    Cajal-Retzius cells: update on structural and functional properties of these mystic neurons that bridged the 20th century

    Neuroscience

    (2014)
  • L.A. Kirkby et al.

    A role for correlated spontaneous activity in the assembly of neural circuits

    Neuron

    (2013)
  • N. Koolen et al.

    Early development of synchrony in cortical activations in the human

    Neuroscience

    (2016)
  • A. Kral

    Auditory critical periods: A review from system's perspective

    Neuroscience

    (2013)
  • D.M. Kullmann et al.

    Extrasynaptic glutamate spillover in the hippocampus: evidence and implications

    Trends Neurosci

    (1998)
  • M. Kummer et al.

    Column-like Ca(2+) clusters in the mouse neonatal neocortex revealed by three-dimensional two-photon Ca(2+) imaging in vivo

    Neuroimage

    (2016)
  • J.H. Lee et al.

    Neurodevelopmental implications of the general anesthesia in neonate and infants

    Exp Neurol

    (2015)
  • V. Lessmann et al.

    Neurotrophin secretion: current facts and future prospects

    Prog Neurobiol

    (2003)
  • H.J. Luhmann

    Cajal-Retzius and subplate cells - transient cortical neurons and circuits

  • H.J. Luhmann et al.

    Early GABAergic circuitry in the cerebral cortex

    Curr Opin Neurobiol

    (2014)
  • K. Malk et al.

    Drug effects on endogenous brain activity in preterm babies

    Brain Dev

    (2014)
  • J.B. Ackman et al.

    Retinal waves coordinate patterned activity throughout the developing visual system

    Nature

    (2012)
  • A. Agmon et al.

    Topological precision in the thalamic projection to neonatal mouse barrel cortex

    J Neurosci

    (1995)
  • D. Akhmetshina et al.

    The Nature of the Sensory Input to the Neonatal Rat Barrel Cortex

    J Neurosci

    (2016)
  • C. Allène et al.

    Sequential generation of two distinct synapse-driven network patterns in developing neocortex

    J Neurosci

    (2008)
  • S. An et al.

    Sensory-evoked and spontaneous gamma and spindle bursts in neonatal rat motor cortex

    J Neuroscience

    (2014)
  • A. Balkowiec et al.

    Activity-dependent release of endogenous brain-derived neurotrophic factor from primary sensory neurons detected by ELISA in situ

    J Neurosci

    (2000)
  • Y. Bando et al.

    Control of spontaneous Ca2+ transients is critical for neuronal maturation in the developing neocortex

    Cereb Cortex

    (2016)
  • M.J. Benders et al.

    Early brain activity relates to subsequent brain growth in premature infants

    Cereb Cortex

    (2015)
  • R. Bermejo et al.

    Topography of rodent whisking - I. Two-dimensional monitoring of whisker movements

    Somatosens Mot Res

    (2002)
  • A.G. Blankenship et al.

    Mechanisms underlying spontaneous patterned activity in developing neural circuits

    Nat Rev Neurosci

    (2010)
  • A.J. Blaschke et al.

    Widespread programmed cell death in proliferative and postmitotic regions of the fetal cerebral cortex

    Development

    (1996)
  • M.E. Blue et al.

    A comparison of pattern formation by thalamocortical and serotonergic afferents in the rat barrel field cortex

    Cereb Cortex

    (1991)
  • J. Cang et al.

    Developmental mechanisms of topographic map formation and alignment

    Annu Rev Neurosci

    (2013)
  • M. Chipaux et al.

    Auditory stimuli mimicking ambient sounds drive temporal “delta-brushes” in premature infants

    PLoS One

    (2013)
  • M.T. Colonnese

    Rapid developmental emergence of stable depolarization during wakefulness by inhibitory balancing of cortical network excitability

    J Neurosci

    (2014)
  • M.T. Colonnese et al.

    “Slow activity transients” in infant rat visual cortex: a spreading synchronous oscillation patterned by retinal waves

    J Neurosci

    (2010)
  • Cited by (0)

    View full text