Neuronal activity controls the development of interneurons in the somatosensory cortex

Abstract

BACKGROUND: Neuronal activity in cortical areas regulates neurodevelopment by interacting with defined genetic programs to shape the mature central nervous system. Electrical activity is conveyed to sensory cortical areas via intracortical and thalamocortical neurons, and includes oscillatory patterns that have been measured across cortical regions.

OBJECTIVE: In this work, we review the most recent findings about how electrical activity shapes the developmental assembly of functional circuitry in the somatosensory cortex, with an emphasis on interneuron maturation and integration. We include studies on the effect of various neurotransmitters and on the influence of thalamocortical afferent activity on circuit development. We additionally reviewed studies describing network activity patterns.

METHODS: We conducted an extensive literature search using both the PubMed and Google Scholar search engines. The following keywords were used in various iterations: “interneuron”, “somatosensory”, “development”, “activity”, “network patterns”, “thalamocortical”, “NMDA receptor”, “plasticity”. We additionally selected papers known to us from past reading, and those recommended to us by reviewers and members of our lab.

RESULTS: We reviewed a total of 132 articles that focused on the role of activity in interneuronal migration, maturation, and circuit development, as well as the source of electrical inputs and patterns of cortical activity in the somatosensory cortex. 79 of these papers included in this timely review were written between 2007 and 2016.

CONCLUSIONS: Neuronal activity shapes the developmental assembly of functional circuitry in the somatosensory cortical interneurons. This activity impacts nearly every aspect of development and acquisition of mature neuronal characteristics, and may contribute to changing phenotypes, altered transmitter expression, and plasticity in the adult. Progressively changing oscillatory network patterns contribute to this activity in the early postnatal period, although a direct requirement for specific patterns and origins of activity remains to be demonstrated.

Keywords

interneuron / neurodevelopment / neuroplasticity / thalamocortical / NMDA receptors / neuronal maturation

Introduction

Development of neocortical areas follows a defined sequence in which excitatory and inhibitory neurons, generated in the dorsal and ventral telencephalon respectively, migrate to their final locations ( Fishell and Rudy, 2011). As they mature, neurons participate in nascent electrical patterns, and ultimately extend dendritic and axonal branches to form functional connections. During these periods, proper development is dependent not only on genetic patterns and progression of intrinsic programs, but also on the activity of input connections ( Erzurumlu and Gaspar, 2012). In this review, we will focus on the activity-dependent processes within the mouse somatosensory cortex, highlighting some recent pertinent findings in other sensory cortices. The somatosensory cortex has been extensively studied in this context because of its well-characterized anatomy and ease of experimental manipulation (for reviews on the auditory and visual sensory systems see ( White and Fitzpatrick, 2007; Sanes and Kotak, 2011; Espinosa and Stryker, 2012; Kral, 2013; Arroyo and Feller, 2016; Chaudhury et al., 2016)). Although we focused our discussion on the developmental processes occurring within the somatosensory cortex of mouse, these processes are likely mirrored throughout the neocortex. In particular, similar cell types ( Wichterle et al., 1999; Wichterle et al., 2001; Zeisel et al., 2015; Tasic et al., 2016), dependence on sensory input for maturation ( Siegel et al., 2012; Ji et al., 2016), and network activity ( Colonnese et al., 2010; Siegel et al., 2012) have been identified throughout sensory cortices. Further, the human neocortex has been shown to display early network patterns similar to that of the mouse and rat ( Milh et al., 2007), and as such, findings in this area may be extended to the understanding of human developmental neurobiology.

Somatosensory information from the periphery is relayed through the trigeminal nucleus of the brain stem and sensory nuclei of the thalamus, which conveys this information to the cortex. Topographic information from the whisker pad is represented in barrel formations of axons, dendrites, and somata in the barrel cortex ( Lorente de No, 1922; Woolsey and Van der Loos, 1970; Welker 1971; Killackey, 1973; Welke,r 1976). Remarkably, sensory inputs shape the formation of these barrels ( van der Loos and Woolsey, 1973; Petersen, 2007). The local cortical circuitry targeted by sensory afferents includes excitatory neurons and inhibitory neurons. We will limit the scope of the review to cover the activity-dependent development of interneurons (for a review on the role of activity on excitatory neurons see ( Erzurumlu and Gaspar, 2012). Although they comprise only about 20% of cortical neurons, interneurons exhibit extreme diversity and can be divided into two main groups: early-born neurons arising from the medial ganglionic eminence (MGE), and later-born neurons from the caudal ganglionic eminence (CGE) ( Van Eden et al., 1989; DeDiego et al., 1994; Butt et al., 2005). In addition, these groups can be further subdivided into at least 15 subtypes by biochemical markers and electrophysiological properties ( Miyoshi et al., 2007; Ascoli et al., 2008; Miyoshi et al., 2010; Rudy et al., 2011). The emergence of subtype-specific features is controlled by intrinsic genetic programs as well as activity-dependent mechanisms ( Kepecs and Fishell, 2014). Upon being generated ventrally, cortical interneurons undergo prolonged migration into the cortex, which is already populated with pyramidal neurons and other early-born neuronal types ( Sultan et al., 2013). Furthermore, the development of these neurons continues into the first postnatal month ( Okaty et al., 2009). This extended maturation renders interneurons particularly susceptible to the early influence of environmental factors such as electrical activity.

Activity-dependent neuronal migration

Activity, including calcium transients and neurotransmitter signaling, plays a role in neuronal migration ( Uhlén et al., 2015). In addition to its role in modulation of the migration of glutamatergic neurons ( Behar et al., 1999; Behar et al., 2000; Kihara et al., 2002; Heck et al., 2007; Liu et al., 2008; Liu et al., 2010; Bony et al., 2013; Luhmann et al., 2015; Bando et al., 2016), neuronal activity regulates gamma aminobutyric acid (GABA)-ergic interneuron migration in the cortex. In this section, we will discuss evidence for the role of activity in interneuron migration, as well as the specific roles that GABA and other neurotransmitters may play in this process.

In CGE-derived interneurons, a cell-autonomous decrease in excitability leads to aberrant interneuron allocation into deep cortical layers ( De Marco Garcia et al., 2011). Similarly, the migration of MGE-derived interneurons ( Close et al., 2012; Denaxa et al., 2012) relies on the expression of the activity-dependent gene special AT-rich binding protein 1(Satb1). This gene was initially identified in a microarray- based screen as a target of the homeobox transcription factor Lhx6 ( Liodis et al., 2007), which is fundamental for the normal migration and specification of cortical interneuron subtypes. Satb1 expression has been further characterized in developing interneurons ( Batista-Brito et al., 2008). Consistent with the role of these transcriptional cassettes in migration, interneuron-specific deletion of Satb1 causes abnormal laminar distribution of SST-expressing interneurons. Altogether these results indicate that neuronal excitability is required for the induction of activity-dependent programs, which enable the migration of cortical interneurons.

In vitro experimental evidence indicates that GABA modulates interneuron migration ( Soria and Valdeolmillos, 2002; Bortone and Polleux, 2009; de Lima et al., 2009). Pharmacological treatment of cortical slices with GABA-A receptor antagonists decreases the percent of interneurons tangentially migrating into the cortex whereas GABA-A receptor agonists have the opposite effect ( Cuzon et al., 2006; Cuzon Carlson and Yeh, 2011; Kilb et al., 2013). Further, in vivo experiments reveal that blockade of GABA-A receptor, blockade of sodium-potassium-chloride co-transporter (NKCC1), and chelation of intracellular calcium all significantly reduce the tangential motility rate, while diazepam increases motility ( Inada et al., 2011). In addition to its role in tangential migration, GABA both stimulates motion, and acts as a stop signal for radial migration. Although in vitro experiments suggest that this change in responsiveness, from increasing motility to halting, results from the upregulation of potassium chloride co-transporter 2 (KCC2) ( Bortone and Polleux, 2009), further in vivo experiments using spatiotemporally controlled elimination of this protein are necessary to demonstrate the requirement for KCC2.

Current experimental evidence indicates that glutamatergic signaling is not required for the migration of cortical CGE-derived interneurons. Genetic elimination of thalamic input as well as whisker plucking do not affect the migration of CGE-derived interneuron cell types ( De Marco García et al., 2015). Furthermore, application of kynurenic acid, a blocker of both NMDA- and AMPA-mediated signaling, resulted in no migratory defects of CGE-derived interneuron subtypes ( De Marco Garcia et al., 2011). In contrast, in vitro experiments suggest that pharmacological blockade of ionotropic receptors in cortical slices causes aberrant MGE interneuron migration ( Manent et al., 2006, Yozu et al., 2008; Bortone and Polleux, 2009). However, the lack of in vivo experiments in which glutamatergic inputs onto MGE-derived interneurons are genetically ablated precludes the analysis of the impact of glutamatergic signaling on the migration of MGE-derived interneurons.

In addition to GABA and glutamate, serotonin and glycine modulate interneuron migration ( Luhmann et al., 2015). Interference of serotonin signaling early in development leads to alterations in migration and the laminar position of interneurons ( Vitalis et al., 2007; Riccio et al., 2009; Murthy et al., 2014; Frazer et al., 2015). This manipulation selectively affects CGE-derived interneurons. In particular, serotonin acts via the 5HT3a receptor, which is selectively upregulated in these interneurons as they invade the developing cortex ( Murthy et al., 2014), suggesting a role for serotonin signaling in interneuron circuit assembly ( Vitalis et al., 2013). The role of serotonin in neuronal migration is further supported by the fact that increases in extracellular serotonin, in both serotonin transporter (SERT) knockout mice and in mice treated with SERT inhibitor fluoxetine, lead to increased migratory speed and altered laminar distribution ( Frazer et al., 2015). Furthermore, these manipulations also alter the expression-level of a host of genes, including some involved in neuronal migration ( Frazer et al., 2015). Altogether, these findings have potential clinical relevance, as selective-serotonin reuptake inhibitors (SSRIs) are currently used for the treatment of neuropsychiatric disorders in pregnant women, and may affect the migration, or more generally the genetic programs, of fetal developing cortical interneurons. In addition to the impact of GABA and serotonin on interneuron migration, genetic disruption of the alpha-2 subunit of the glycine receptor causes migratory defects ( Avila et al., 2013). In brief, interneuron migration is modulated by signaling from a diversity of neurotransmitter receptors whose relative contribution changes dynamically throughout development.

Activity-dependent maturation of cortical interneurons

Once interneurons reach their target laminae in the cortex, they begin to acquire mature properties including characteristic morphologies, intrinsic electrophysiological properties, and molecular features, such as the expression of neuropeptides and calcium binding proteins ( De Marco García et al., 2011; Miyoshi and Fishell, 2011; Karayannis et al., 2012). Subsequently, interneurons influenced by environmental cues form contacts with defined synaptic partners ( Batista-Brito and Fishell, 2009; Chu and Anderson, 2015). In this section, we will discuss the role of neuronal activity in interneuron maturation.

Both MGE- ( Close et al., 2012; Denaxa et al., 2012) and CGE-derived ( De Marco García et al., 2011) interneuron cell types undergo activity-dependent differentiation. In a subtype of MGE-derived interneurons, the somatostatin-positive (SST) neurons, Satb1 is necessary for synaptic integration and survival, as well as its previously discussed role in migration ( Close et al., 2012, Denaxa et al., 2012). In addition, neuronal excitability is required after postnatal day 3 (P3) for the morphological development of both reelin (Re) and calretinin (Cr)-expressing interneurons ( De Marco García et al., 2011). In these experiments, hyperpolarization induced after expression of an inward rectifying potassium channel, which leads to attenuation of neuronal excitability, caused defects in the maturation of neuronal processes ( De Marco García et al., 2011). Mechanistically, a reduction in neuronal excitability may impair the activation of NR2B-containing N-methyl-D-aspartate receptors (NMDARs) (see next section).

In addition to its contribution to the maturation of neuronal processes, neuronal activity influences emerging synaptic formation. A complete blockade of GABA signaling results in over proliferation of small synapses and overgrowth of axons, demonstrating a role for GABA in the pruning of synapses during a critical period of synaptic remodeling ( Wu et al., 2012). Similarly, a suppression of neurotransmitter release in single basket cells induces the formation of denser arbors and increases the number of smaller-sized boutons, without a change in the number of innervated somata ( Baho and Di Cristo, 2012). In contrast, GABA signaling via the GABA-A receptor and voltage gated calcium channels induces the formation of inhibitory synapses in layer II/III pyramidal cells during early development ( Oh et al., 2016). Thus, the role of GABA in circuit maturation is context dependent.

In sum, rather than being exclusively controlled by intrinsic genetic programs, interneuron differentiation and survival are under the strong influence of activity-dependent programs. However, it remains unclear whether a certain threshold of excitability or certain sources of inputs trigger activity-dependent development.

Thalamic inputs and the maturation of cortical microcircuits

After region-specific genetic programs pattern the cortex into basic functional subdivisions ( Miyashita-Lin et al., 1999), sensory inputs shape its connectivity and structure ( Sur and Leamey, 2001). Here we will discuss the specialization of sensory inputs, as well as the interaction between these inputs and circuit formation in the mouse neocortex (for a review of thalamocortical connectivity in the adult somatosensory cortex, see ( Feldmeyer, 2012) and ( Feldmeyer et al., 2013)). In addition, we summarize the evidence implicating the importance of N-methyl-D-aspartate (NMDA)-receptors as important in shaping this circuit.

Thalamocortical (TC) axons have distinct arborization patterns within the lamina of the somatosensory cortex depending on their anatomical origin. The main input from the ventroposteriormedial nucleus (VPM) to the somatosensory cortex is to layer IV with some axonal ramifications targeting layer VI. In contrast, projections from the rostral posterior nucleus (PO) target layers I and Va ( Feldmeyer, 2012). Therefore, somatic or dendritic location within cortical layers may be the sole determinant for TC innervation. Alternatively, input may be further restricted according to cell type identity within layers. In support of this notion, fast-spiking interneurons and excitatory cells receive TC input ( Agmon and Connors, 1992; Agmon and O’Dowd, 1992; Sun et al., 2006; Cruikshank et al., 2010), which evokes robust responses in both of these cell types in layer IV. In contrast, only weak responses are detected in SST interneurons within the same layer ( Cruikshank et al., 2010). Further, evoked action potentials can be recorded from 60% of inhibitory neurons, but less than 5% of excitatory neurons in layer IV and V ( Porter et al., 2001). The wiring of other sensory cortices also seems to support the concept that TC connectivity within cortical layers is cell type-restricted. Electrophysiological recordings in the auditory and visual cortices show that PV interneurons and excitatory cells throughout cortical layers are innervated by thalamic axons. However, only a fraction of SST and vasoactive intestinal peptide-expressing (VIP) interneurons in layer IV, and none of the SST and VIP cells elsewhere, receive thalamic innervation ( Ji et al., 2016). Taken together, this data supports the idea that TC connectivity may be specified by a combination of cell-type identity and laminar allocation. Importantly, these experiments were performed in adult animals, and as a result, it remains unclear whether similar patterns are present during development and whether dedicated molecular mechanisms restrict TC innervation to select cell types.

Increasing experimental evidence indicates that maturing sensory cortices possesses certain circuits in place at birth that exist only transiently to give way to adult circuitry ( Luhmann et al., 2003; Luhmann et al., 2014). Subplate neurons, a cohort of early born neurons that become dramatically reduced in number after the first postnatal week, are the initial recipients of TC axons and are fundamental in promoting synaptic scaling as well as the maturation of TC connections onto cortical excitatory cells ( Molnár et al., 1998; Hanganu et al., 2002; Kanold, 2004; Higashi et al., 2005). The importance of this transient population is highlighted in ablation experiments that result in absence of anatomical segregation of thalamic inputs and weakened TC synaptic transmission in adult ( Kanold et al., 2003). Another example of transient circuitry involves SST interneurons. In the first postnatal week, these neurons receive transient TC innervation and project from infra-granular layers to layer IV, a pattern of connectivity that is necessary for proper circuit assembly within the recipient layer ( Anastasiades et al., 2016; Marques-Smith et al., 2016; Tuncdemir et al., 2016). The progressive elimination of TC innervation to infra-granular SST interneurons ( Anastasiades et al., 2016; Tuncdemir et al., 2016) is in agreement with the observation that infra-granular SST interneurons are unresponsive to TC stimulation in adult ( Ji et al., 2016).

Although the mechanism that regulates the disappearance of transient circuitry is currently unknown, neurotransmitter receptors are attractive candidates. NMDARs are present in TC synapses at early stages of development ( LoTurco et al., 1991; Iwasato et al., 2000; Laaris et al., 2000). These receptors contain one obligatory NR1 subunit and two NR2 subunits, of which there are at least 4 isoforms ( Paoletti et al., 2013). NMDAR signaling to excitatory cells greatly affects the formation of barrel columns. After perturbation of this signaling pathway, TC axonal projections are more diffuse and the somata and dendritic orientation of excitatory cells within barrels does not develop ( Iwasato et al., 2000; Lee et al., 2005; Reiprich et al., 2005; Espinosa et al., 2009; Mizuno et al., 2014). Furthermore, elimination of TC glutamatergic inputs results in changes in cortical lamination ( Reiprich et al., 2005; Narboux-Nême et al., 2012; Li et al., 2013).

Given that NMDARs are one of the most highly regulated postsynaptic receptors during development, their dynamic expression, activation, or change in subunit composition could influence the developmental changes in TC signaling. A developmental decrease in the relative amount of NR2B-containing receptors compared with NR2A-containing receptors has been long appreciated. Specifically, there is a progressive increase in the contribution of NR2A-containing receptors, which parallels the increase in synaptic activity between P2 and P15 ( Crair and Malenka, 1995; Flint et al., 1997; Liu et al., 2004; Zhang and Sun 2011; Paoletti et al., 2013). Both MGE- and CGE-derived hippocampal interneurons possess high ratios of NR2B-containing NMDARs at birth. Whereas MGE-derived interneurons undergo the NR2B-to-NR2A developmental switch in subunit composition, CGE-derived interneurons retain high levels of the NR2B-containing receptors into adulthood, when compared with NR2A ( Matta et al., 2013). Taken together, these experiments suggest that cell type specific differences in NMDAR composition may be an important regulatory mechanism for circuit maturation.

Direct TC innervation to cortical interneurons is important for the development of somatosensory circuitry. Whisker trimming during the second postnatal week leads to a reduction in PV expression and a decrease in inhibitory currents onto spiny stellate cells ( Jiao et al., 2006). Furthermore, sensory inputs influence interneuron development at even earlier stages of maturation. Direct TC inputs are required for the axonal and dendritic development of CGE-derived Re-expressing interneurons during the first postnatal week ( De Marco García et al., 2015). Mechanistically, NR2B-containing NMDARs, which are enriched in TC synapses onto Re-expressing interneurons, regulate the maturation of cell morphology ( De Marco García et al., 2015). In addition, SST interneurons, which receive transient thalamic innervation, are necessary for the establishment of mature TC inputs to pyramidal and PV interneurons in deep cortical layers ( Tuncdemir et al., 2016). However, whether the role of SST interneurons in circuit development can be attributed to the presence of transient TC connectivity remains to be determined. Given existing data on the complexity and specialization of long- and short-range connections, and the presence of a clear critical period of plasticity ( Daw et al., 2007), it is tempting to hypothesize that transient connectivity and integration of inputs onto specific neuronal subtypes regulates the maturation of cortical circuitry.

The emergence of early network patterns

Neurons exhibit changing patterns of electrical activity throughout development. This activity is asynchronous at early embryonic stages ( Allène et al., 2008), but becomes synchronized around birth ( McCabe et al., 2006; Allène et al., 2008; Golshani et al., 2009; Allene and Cossart, 2010). The synchronous patterns of activity, which parallel neurodevelopmental maturation of physiological and morphological properties ( Allene and Cossart 2010), are conserved in humans ( Milh et al., 2007; Tolonen et al., 2007; Koolen et al., 2016). Though much work has been performed to describe these patterns, it is currently unknown whether they play an instructive role in the development of the somatosensory cortex. Complicating the analysis of activity patterns, the spatiotemporal characteristics of these oscillations vary depending on the methodology used to record them ( Allene and Cossart, 2010). In this section, we focus on reconciling the oscillatory patterns as seen in different experimental conditions, first discussing in vitro studies, and then examining data from two types of in vivo experiments – field recordings and calcium imaging. We then review possible pacemakers of oscillatory activity.

Three main types of activity have been recorded in vitro in cortical slices: synchronous plateau assemblies (SPAs), cortical early network oscillations (cENOs), and cortical giant depolarizing potentials (cGDPs). The earliest postnatal forms of correlated activity recorded in rat cortical slices are SPAs, which rely on gap junction coupling to activate small groups of neurons ( Allène et al., 2008; Allene and Cossart, 2010). Studies have revealed that SPAs occur primarily between P0 and P3 and co-exist with cENOs ( Corlew et al., 2004; Allène et al., 2008). Unlike SPAs, cENOs are tetrodotoxin (TTX)-sensitive ( Rheims et al., 2008) and require NMDAR activity ( Garaschuk et al., 2000; Allène et al., 2008). These oscillations occur at low frequency (~0.01 Hz), involve large cortical areas ( Allène et al., 2008), and are observed between embryonic day 17 (E17) and P3 in the developing mouse ( Corlew et al., 2004; McCabe et al., 2006). In contrast, cGDPs predominate in the cortex in the latter half of the first postnatal week through most of the second week. cGDPs are synaptically-driven recurrent oscillations (~0.1 Hz) that synchronize localized neuronal assemblies ( Allène et al., 2008) and are dependent upon GABA ( Rheims et al., 2008). In short, in in vitro experiments show that developing neurons follow a temporal sequence of network activity patterns, starting with gap junction-mediated SPAs and NMDA-mediated cENOs followed by GABA-A receptor mediated cGDPs.

In addition to network patterns recorded in cortical slices, oscillatory activity can be observed in vivo using field recordings. Synchronous activity has been described in the form of spindle bursts, gamma oscillations, and long oscillations in rat pups age P0 through P7 ( Yang et al., 2009, 2016). Spindle bursts appear every 10 s for 1-2 s, exhibit a frequency of 8-25 Hz rhythmic activity ( Yang et al., 2009) and are often associated with overt movement, including muscle twitches, limb/body jerks, crawling and suckling, but can occur either preceding or following movement ( Khazipov et al., 2004; Milh et al., 2007; An et al., 2014). Superimposed on this activity is a 30-40 Hz gamma wave pattern, lasting 150 to 300 ms and occurring every 10 to 30 s ( Khazipov and Luhmann 2006; Yang et al., 2009). In addition, 10-20 Hz long oscillations occur concurrently with the spindle bursting and gamma oscillations ( Yang et al., 2009), but differ from other activity types in their long-range propagation and their sparse occurrence ( Sun and Luhmann, 2007). Thus, oscillations are observed in field recordings in vivo, and synchronized activity can be broken down into three main waveforms—spindle, gamma, and long oscillations. However, as these activities show overlapping time courses in vivo, a parallel progression of the activity types like that seen in vitro, is not apparent in the living animal.

Two-photon imaging coupled with voltage-sensitive dyes or genetic calcium indicators ( Stosiek et al., 2003) is often used as an alternative method for visualizing neuronal activity. However, limited studies with this methodology have been performed in the developing somatosensory cortex. Calcium oscillations are evident in the somatosensory cortex of resting pups at a cortical depth of 300-400 μm in the early postnatal time period (P0 to P3) ( Adelsberger et al., 2005). Given their developmental time course, the number of events, and the rate at which they occur and decay, it is possible that these waves are the in vivo correlate to cENOs ( Adelsberger et al., 2005). In the first postnatal week, oscillations also occur in layer I, a layer populated predominantly by Re-CGE interneurons and Cajal-Retzius neurons. Calcium transients in Re-interneurons, but not Cajal-Retzius cells, are synchronized, and this synchrony depends on a range of neurotransmitters and neuromodulators, but not on gap junctions or glycine ( Schwartz et al., 1998). From P5 to P12, layer II/III is synchronized across large areas—with oscillations extending beyond the boundaries of the barrel—and this activity becomes asynchronous after the second postnatal week ( Golshani et al., 2009). While in vivo imaging demonstrates a de-synchronization of the somatosensory cortical neurons in general, imaging of specific subtypes of neurons using genetically encoded calcium indicators shows that even in mature networks, there is cooperative firing of specific interneuronal subtypes ( Sippy and Yuste, 2013; Karnani et al., 2016), though it is unknown whether this cooperation emerges early in development.

Both GABAergic and glutamatergic transmission modulate early patterns of cortical activity ( Kilb et al., 2011). Excitatory post-synaptic potentials and inhibitory post-synaptic potentials are associated with spindle bursts in the first postnatal week ( Khazipov et al., 2004). Spindle-bursts and delta waves are NMDAR-dependent ( Minlebaev et al., 2009) whereas alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) blockade suppresses spindle bursts ( Minlebaev et al., 2007). In the second half of the first postnatal week, NMDAR antagonists suppress cortical rhythms ( Dupont et al., 2006). In addition, GABA antagonists decrease the compartmentalization of spontaneously generated rhythms ( Voigt et al., 2001; Kirmse et al., 2015), suggesting a role for this neurotransmitter in confining the spread of oscillations ( Minlebaev et al., 2007). All together these experiments suggest that glutamate is necessary to drive cortical oscillations, while GABA regulates their propagation.

One possible origin for synchronous cortical activity is the thalamus. Spindle-bursts are evoked by thalamic inputs ( Khazipov et al., 2004; Minlebaev et al., 2009), and early gamma oscillations are driven by these inputs ( Minlebaev et al., 2011). Moreover, the subplate has been hypothesized to play a role in the generation and maintenance of these oscillations ( Kanold and Luhmann, 2010). Removal of the subplate abolishes spontaneous and sensory evoked spindles in the somatosensory cortex ( Tolner et al., 2012) suggesting that both of these activity patterns are modulated by inputs relayed via the thalamus and amplified by the subplate ( Dupont et al., 2006; Kilb et al., 2011). Since correlated activity in developing ( Golshani et al., 2009) and mature pyramidal cells ( Cohen-Kashi Malina et al., 2016) is independent of thalamic inputs, cortical interneurons are attractive candidates as mediators of thalamic-induced cortical oscillations. GABAergic neurons outside of the cortex may also play a role in the generation, maintenance, or dampening of network oscillations ( Cossart et al., 2005). The piriform cortex and septal nucleus are pacemaker locations, and the wave initiation sites are highly correlated to the position of GABAergic neurons ( Conhaim et al., 2011). There are both GABAergic and glutamatergic fractions of waves that propagate from ventral structures; although, the glutamatergic fraction seems to preferentially propagate to the neocortex, particularly as postnatal development proceeds ( Easton et al., 2014). It is possible that both thalamic and other subcortical patterns interact to produce the oscillatory patterns observed in the developing somatosensory cortex.

In sum, the neonatal somatosensory cortex undergoes different patterns of oscillatory activity, though the descriptions of this activity can vary with method of recording. These oscillations provide the electric drive necessary for the processes discussed in this review. However, it remains to be determined whether specific patterns are required for the proper assembly of cortical circuits. Due to limitations in existing knowledge and experimental tools, it has not yet been possible to replay rhythms of distinct origin and sequence to directly implicate cortical oscillations as instructive for neuronal connectivity. Furthermore, the distinct contribution of different cell types to these oscillations is not yet known, but the increasing availability of tools to dissect cell populations should enable specific analyses in the future. Regardless of their cellular origin and spatiotemporal features, these rhythms are conserved in the human neonatal cortex ( Milh et al., 2007) strongly suggesting that they subserve an important role during cortical development.

Plasticity of adult neuronal identity and connectivity

Neuronal intrinsic properties have been considered to be set early during differentiation and maintained through adulthood ( Kepecs and Fishell, 2014). In fact, these properties are currently used for the classification of interneuron subtypes ( Butt et al., 2005; Miyoshi et al., 2007; Miyoshi et al., 2010). However, recent experimental evidence revealed that cortical activity can trigger changes in intrinsic properties in the adult animal.

It has been shown that Er81, a member of the ETS family of transcription factors that delineates PV interneurons in layers II/III, is required for the modulation of their intrinsic properties in mature animals. Specifically, cell-autonomous elimination of Er81 results in reduced spiking latency, a hallmark of inhibitory gating mediated by Kv1.1 potassium channels. Kv1.1 expression is also reduced in Er81-ablated cells. Furthermore, motor learning regulates Er81 expression in PV interneurons ( Dehorter et al., 2015). Adult plasticity has also been demonstrated in the hippocampus, where repeated high-frequency stimulation of PV basket cells in CA1 results in potentiation of intrinsic neuronal excitability through the downregulation of potassium channels ( Campanac et al., 2013). These examples provide mechanistic evidence for activity-dependent plasticity of interneuron properties in adult through transcriptional regulation. With the new advent of single-cell RNA-sequencing technology, it has been possible to classify interneuronal subtypes into increasingly defined categories ( Zeisel et al., 2015; Tasic et al., 2016). It would be interesting to assess whether the expression of genes that confer interneurons with subtype identity are also subject changes in neuronal excitability.

In addition to regulating mature neuronal excitability, neuronal activity is required for the proper regulation of GABA expression in mature interneurons. Sensory deprivation leads to a decrease of GABA expression ( Rutherford et al., 1997; Huang et al., 2007). Furthermore, the expression of GABA-synthesizing enzymes, glutamic acid decarboxylase (GAD) -65 and 67, is also activity dependent ( Liang et al., 1996; Gierdalski et al., 2001; Mix et al., 2015), and can be specifically induced after sensory learning ( Gierdalski et al., 2001), suggesting that activity can influence interneuron output even after these neurons become integrated into the mature circuit.

Concluding remarks

It is clear that neuronal activity impacts the development and integration of cortical interneurons, by influencing their migration and maturation (Fig. 1). In addition, activity-dependent transcription programs control the electrophysiological properties and output of mature interneurons. Thus, a complex, dynamic interplay between intrinsic genetic programs and environmental influences shape cortical circuits from early developmental stages into adulthood. Because defects in interneurons and GABAergic signaling have been implicated in neurodevelopmental and neuropsychiatric diseases, including autism ( Marín, 2012; Takano, 2015), schizophrenia ( Marín, 2012; Lewis, 2014), and epilepsy ( Coulter, 2001; Trevelyan et al., 2015), it is of high importance to determine the factors regulating interneuron maturation, as further research in this area will illuminate possible treatments for these clinical problems.

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