ReviewNeuronal Activity Patterns in the Developing Barrel Cortex
Graphical abstract
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.).
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