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Review article
Timing matters: A strategy for neurons to make diverse connections Tatsumi Hirata a,b,∗ , Lena Iwai a a b
Division of Brain Function, National Institute of Genetics, 1111 Yata, Mishima, 411-8540, Japan SOKENDAI (Graduate University for Advanced Studies), Japan
a r t i c l e
i n f o
Article history: Received 7 July 2018 Received in revised form 21 August 2018 Accepted 21 August 2018 Available online xxx Keywords: Development Neurogenesis Timing Neuronal birthdate Axon guidance
a b s t r a c t Neurogenesis proceeds like a continuous wave, in which each type of neurons is produced over a few days to several days. During this protracted time window, early-born and late-born neurons are sequentially produced with a considerable time lag. Even if they are identical in their genetic and molecular specifications, they could develop different characteristics under the influences of the timing of their birth. In this review, we discuss the potential influences of “timing” as a generic parameter affecting neuronal differentiation, particularly on axon guidance and connections. These ideas have rarely been tested experimentally, but may provide a new strategy by which phenotypic diversity is increased in neurons. © 2018 Elsevier B.V. and Japan Neuroscience Society. All rights reserved.
Contents 1. 2. 3. 4. 5. 6.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00 Significance of the birthdate in human society . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00 The earlier the start, the greater the reach . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00 Born together, wire together . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00 Different times, different ways . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00 Future projections . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00 Declarations of interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00 Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
1. Introduction It is generally agreed that the “neurogenetic timing” when neurons complete their final mitosis is a critical determinant for neurons. Examples in various nervous systems indicate that the neuronal birthdate determines location, morphology, physiology or connection patterns of neurons. Intensive research over the past few decades has successfully identified gene networks involved in these processes, confirming our current conceptual framework that neural progenitors keep track of time and assign specific gene expressions and a neuronal type identity to the daughter neurons depending on neurogenetic timing (Arlotta et al., 2005; Molyneaux et al., 2005; Shen et al., 2006; Suzuki et al., 2012). This neuronal
∗ Corresponding author at: Division of Brain Function, National Institute of Genetics, Yata 1111, Mishima, 411-8540, Japan. E-mail address: [email protected] (T. Hirata).
type specification based on the neuronal birthdate is well discussed in recent reviews including one in this issue (Fame et al., 2011; Leone et al., 2008; Suzuki and Hirata, 2013; Kawaguchi, 2018). In this review, we will focus on less-discussed aspects of the birthdate effect; specifically, how the relative timing of neurogenesis in identically specified neurons can create phenotypic diversities among them in terms of axon guidance and connections. One reason that we started to consider the contribution of relative timing in neurogenesis is that the post-genome era simply casted a doubt about whether diverse neuronal phenotypes are truly explainable by differential gene expressions alone. Particularly, we are concerned with axon wiring and connection patterns. After Sperry’s chemoaffinity hypothesis (Sperry, 1963), researchers looked for the specific chemical tags that mediate axon and target recognition. Specific pairs of axon guidance molecules and their receptors, in more recent terminology, were successfully
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Fig. 1. The earlier the start, the greater the reach. (A) An early-born sibling develops earlier compared to a later-born sibling. (B) In the developing nervous system, an early-born neuron starts to elongate its axon earlier, and therefore reach the target earlier, so that the axon can spend more time to grow farther and expand the territory by the “first come, first served” rule. On the other hand, the axon of a late-born neuron reaches its target later and settles for a limited territory.
Fig. 2. Born together wire together. (A) People of similar age are more likely to interact with each other in human society. (B) In the nervous system, pre- and post-synaptic neurons that are both in the appropriate timing for synaptogenesis selectively make connections, forming time-matched networks.
identified, but the numbers of these “tags” are too small to account for construction of the myriad of highly diversified neural connections (Polleux et al., 2007; Stoeckli, 2018; Yu and Bargmann, 2001). These guidance molecules can have greater functions than their numbers, because they are repetitively used in different places and times, and combine their forces to modify their individual functions. Yet, it appears that our knowledge regarding molecular axon guidance is vastly insufficient to explain the actual phenomena. If we turn our attention to classic articles from 1970s, many authors discuss the non-molecular force of axon guidance inspired by the temporal order of neurogenesis (Bayer and Altman, 1987). These mechanisms can possibly explain phenotypic diversification of neurons without any chemical tags. In this review, we would like to revisit the non-molecular form of axon guidance from the perspective of “timing”. We will also discuss other potential scenarios where the neurogenetic “timing” may have significant influence on neuronal connections. We propose three hypotheses: 1) the earlier the start, the greater the reach (Fig. 1), 2) born together, wire together (Fig. 2) and 3) different times, different ways (Fig. 3). Because this classification is new and far from complete, let us start with anecdotal examples to clarify the essence that we try to convey in each hypothesis.
when the neurons are born. Yet, there is probably more to the birthdate. Let us consider three additional situations where the birthdate affects people more indirectly. First, the birthdate automatically determines the birth order in siblings (Fig. 1A). Even though all siblings inherit stochastically equal genetic traits, by the so-called “birth order effect” each child is supposed to develop a personal character typical to the birth order. A rather inevitable consequence of the birth order is that the early-born ones start performing various activities earlier and are generally larger, thereby dominate some space in the family. The second scenario is a situation where the birth timing of both oneself and others are important (Fig. 2A). People tend to choose their partners and friends of a similar age over other generations, even if they are born in distant places. This tendency results in a strong demographic force to bundle similarly aged people in the same social network. Lastly, environmental transitions can affect people’s behavior depending on their birthdates (Fig. 3A). Consider the situation in Berlin. When the Berlin Wall was present, people could not move across this boundary. People born after its collapse in 1989, however, can behave in a completely different way. In the following sections, we extend the above three scenarios one by one and propose that similar effects of the birthdate may be applicable to neurons.
2. Significance of the birthdate in human society 3. The earlier the start, the greater the reach In astrology, the birthdate deterministically allocates intrinsic properties to individuals, who live out with their destined fates irrespective of the circumstances surrounding them. This is actually similar to the situation in neurogenesis, where neuronal fates are genetically and molecularly specified by the birthdate at the time
3 H-thymidine birthdate analyses conducted during 1960–1970 often noted that early-born neurons have large cell bodies with long axons and late-born neurons are small with short axons (Altman and Bayer, 1975; Altman and Das, 1965; Hinds, 1968). In those
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Fig. 3. Different times, different ways. (A) A transition of social historical environment creates peoples’ distinct behaviors in Berlin. (B) In this hypothetical situation of a nervous system, a repulsive guidance molecule begins to be expressed halfway through the process of axon projections. Suppose that all axons express the receptor for this guidance molecule. Early-growing axons pass through the domain, because they reach it before the expression of the guidance molecule. Later-growing axons are repelled by the guidance molecule and project into a different way.
days, the primary focus was the comparison of large projection neurons and small interneurons. Since our current knowledge indicates that these two populations originate from totally segregated neural progenitors with highly distinct gene expressions (Bandler et al., 2017; Hu et al., 2017), these remarks may not be directly applicable to the present discussion. There are still some examples that larger neurons differentiate earlier from the same progenitor pools (Hinds, 1968; Lawson et al., 1974), but also other cases that the generation of medium-sized neurons precedes that of largesized ones (Jones, 1984; Walsh et al., 1983). Thus, it appears that there is no general consensus about correlation between birthdate and neuron size. Meanwhile, a more important lesson gained from these arguments would be that a functional benefit may exist when the generation of long projection neurons precedes that of local interneurons (Hinds, 1968; Nishida and Ito, 2017); it is conceivable that the long projection neurons require time to extend their axon terminals to the distant target to make functional connections with local interneurons there. Conceivably, neurons can make use of differences of their birthdate timings. Suppose that a wave of neurogenesis for a single neuronal type typically continues around 2–4 days (Bayer and Altman, 1987). Since the speed of axon elongation is estimated as 20–100 m per hour (Godement et al., 1994; Halloran and Kalil, 1994; Sretavan and Reichardt, 1993), the last axons would lag behind the first ones by 1–10 mm, which readily covers the full dimension of a typical target (Fig. 1B). Indeed, time-different arrival of axons is readily observable as a chronological growth ring in some axon tracts (Inaki et al., 2004; Walsh, 1986; Walsh and Guillery, 1985; Yamatani et al., 2004). Furthermore, a long-delayed arrival of axons grown by late-born neurons has been directly shown in a visual target (Dallimore et al., 2002). Since early-born neurons reach their axons to the target earlier, they would have ample time to develop their terminals farther and occupy more of the limited target sites as compared with the later cohorts by the “first come, first served” rule (Fig. 1B). An observation that may support this scenario is that axon projections from the main olfactory bulb extend to around ten target areas that are spatially continuous in the brain. During development, the bulb axons first penetrate only proximal targets and then gradually expand over distant targets (Schwob and Price, 1978). Yet, even in the adult stage, the proximal targets that receive early innervation are more densely populated with the bulb axons
compared with the distal targets (Schwob and Price, 1984). Our preliminary observation also suggests that the last-born projection neurons in the main olfactory bulb, which are generated at the perinatal stage in mice, have only short axons that manage to reach only the proximal target in adulthood (Hirata, unpublished observation). Thus, the earlier neurons start, the greater their axons reach at least in the central olfactory system. 4. Born together, wire together Time-matched synaptogenesis has been extensively discussed previously (Bayer and Altman, 1987). This hypothesis postulates that both pre- and post-synaptic neurons have specific maturation stages appropriate for synaptogenesis, and that neurons which form good match in the stages selectively make synaptic connections (Fig. 2B). For example in rats, the projection neurons in the accessory olfactory bulbs are born two days earlier that those in the main olfactory bulbs (Bayer, 1983). Their axons make segregated projections onto their own specific targets, even though some of the accessory and main bulb targets are juxtaposed with no physical boundary. Interestingly, the postsynaptic neurons in the accessory bulb targets differentiate earlier than those in the main bulb targets (Bayer, 1980). Therefore, when the early-born accessory bulb neurons project their axons, the only available targets are the neurons in the accessory bulb targets, whereas the late-born main bulb neurons can selectively connect with the age-matched neurons in the main bulb targets, which are now ready for receiving innervation. Similar correlations in the neurogenetic timing of pre- and postsynaptic partners have been documented in many other nervous systems as well (Bayer and Altman, 1987). One of the most intensively studied regions describing timematched connections is the hippocampus; there is a strong spatiotemporal correlation of the arrival time of afferent axons, and the dendritic zones that receive the axons in the hippocampal pyramidal as well as dentate gyrus granule cells. Specifically, the first arriving afferents occupy the most distal zone of the dendrites, and later ones sequentially occupy a more proximal territory (Bayer and Altman, 1987). In the same dendritic zone, the axons from the ipsilateral and contralateral hippocampi compete for post-synaptic sites (O’Leary et al. 1979), and in this competition, time-matched synaptogenesis seems to take place (Gottlieb and Cowan, 1972). Specifically, early-born dentate granule cells receive more ipsi-
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lateral afferents that arrive earlier than the contralateral ones, whereas late-born granule cells receive ipsilateral and contralateral afferents almost equally, because both the afferents exist at comparable levels at that stage. More recently, an experimental test was conducted to verify time-matched hippocampus connections. Deguchi et al. (2011) found that early- and late-born subpopulations of dentate granule cells selectively connect with early- and late-born subpopulations of hippocampus CA3 pyramidal neurons, respectively. The time windows for synaptogenesis of these selective pairs are largely non-overlapped. By heterochronically co-culturing the preand post-tissues derived from different developmental stages, the authors showed that non-selective pairs make connections if, and only if, maturation stages are matched. Thus, matching of maturation stage can even overwrite the molecularly defined differences of neuronal subpopulations. This implies that temporal matching is the key mechanism for the selectivity of connections, i.e. neurons that born together wire together.
6. Future projections We have discussed potential scenarios where “timing” can increase diversity among neurons. Most examples described here show only correlations but have not tested experimentally. The reason is obvious; the hypotheses were not testable back in those days. However, the subsequent revolution of molecular biology techniques and developmental engineering has made it possible to directly test these hypotheses. For example, we recently developed a neuronal birthdate tag technique, by which neurons are genetically tagged with loxP recombination in a neuronal birthdate-dependent manner (Hirata, unpublished data). Using such a technique and combining it with the method to alter the timing of neurogenesis or axon projections (Mizutani and Saito, 2005; Olsson-Carter and Slack, 2010), we may be able to address the real significance of “neurogenetic timing” in the near future. Declarations of interest None.
5. Different times, different ways Acknowledgements Since neurogenesis is a protracted process, early-born and lateborn neurons could encounter drastically different landscapes in the rapidly changing developmental environment. For example, the attractive axon guidance molecule Netrin1 begins to be expressed in a small ventral domain within the central olfactory target area, shortly before the end of olfactory bulb projections (Kawasaki et al., 2006, unpublished observation). Its specific receptor DCC is expressed by virtually all olfactory bulb projection neurons during the time when the axons are in an active growing phase (Inaki et al., 2004). These observations suggest that the early growing axons from the olfactory bulb miss the chance to recognize Netrin1, whereas the late growing axons can respond to the delayed expression of Netrin1. Our observations indeed show that only the late-growing axons from the bulb selectively penetrate the small ventral domain (Yamatani et al., 2004) in which Netrin1 is expressed in the late developmental stage. This scenario may not be very uncommon, because many axon guidance molecules are expressed only transiently in a spatiotemporally restricted manner (Huber et al., 2005; Ito et al., 2008; Kawasaki et al., 2006). Furthermore, heterochronic culture assays have detected developmental transition of axon guidance environment in various nervous systems (Gotz et al., 1992; Hirata and Fujisawa, 1997, 1999; Pini, 1993; Tuttle et al., 1995). Yet, in these cases, it is not clear whether the environmental transition occurs during the time when the axons that are responsive to the same guidance signals are projecting, thereby phenotypically splitting neuron populations, which will otherwise have the same projection patterns. As far as we know, the only example with experimental support for this hypothesis is the ipsilateral projections of retinal axons in Xenopus (Nakagawa et al., 2000) (Fig. 3B). In tadpoles, the retinal axons solely project to the contralateral side through the optic chiasm. Only after metamorphosis, the late-born neurons, which are still generated in the ventro-temporal retina, begin to project axons ipsilaterally to accommodate the shift of visual fields caused by the metamorphic eye translocation. These ipsilateral projections are triggered by the late expression of Ephrin-B, a repulsive axon guidance molecule in the optic chiasm. This trigger is purely environmental, because if Ephrin-B is prematurely expressed in the optic chiasm in the tadpoles, the earlier-born retinal neurons that express the Ephrin-B receptor precociously project the axons ipsilaterally. Thus, in this system, the early-born and late-born neurons go different ways because they are born different times.
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Review article
Timing matters: A strategy for neurons to make diverse connections Tatsumi Hirata a,b,∗ , Lena Iwai a a b
Division of Brain Function, National Institute of Genetics, 1111 Yata, Mishima, 411-8540, Japan SOKENDAI (Graduate University for Advanced Studies), Japan
a r t i c l e
i n f o
Article history: Received 7 July 2018 Received in revised form 21 August 2018 Accepted 21 August 2018 Available online xxx Keywords: Development Neurogenesis Timing Neuronal birthdate Axon guidance
a b s t r a c t Neurogenesis proceeds like a continuous wave, in which each type of neurons is produced over a few days to several days. During this protracted time window, early-born and late-born neurons are sequentially produced with a considerable time lag. Even if they are identical in their genetic and molecular specifications, they could develop different characteristics under the influences of the timing of their birth. In this review, we discuss the potential influences of “timing” as a generic parameter affecting neuronal differentiation, particularly on axon guidance and connections. These ideas have rarely been tested experimentally, but may provide a new strategy by which phenotypic diversity is increased in neurons. © 2018 Elsevier B.V. and Japan Neuroscience Society. All rights reserved.
Contents 1. 2. 3. 4. 5. 6.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00 Significance of the birthdate in human society . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00 The earlier the start, the greater the reach . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00 Born together, wire together . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00 Different times, different ways . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00 Future projections . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00 Declarations of interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00 Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
1. Introduction It is generally agreed that the “neurogenetic timing” when neurons complete their final mitosis is a critical determinant for neurons. Examples in various nervous systems indicate that the neuronal birthdate determines location, morphology, physiology or connection patterns of neurons. Intensive research over the past few decades has successfully identified gene networks involved in these processes, confirming our current conceptual framework that neural progenitors keep track of time and assign specific gene expressions and a neuronal type identity to the daughter neurons depending on neurogenetic timing (Arlotta et al., 2005; Molyneaux et al., 2005; Shen et al., 2006; Suzuki et al., 2012). This neuronal
∗ Corresponding author at: Division of Brain Function, National Institute of Genetics, Yata 1111, Mishima, 411-8540, Japan. E-mail address: [email protected] (T. Hirata).
type specification based on the neuronal birthdate is well discussed in recent reviews including one in this issue (Fame et al., 2011; Leone et al., 2008; Suzuki and Hirata, 2013; Kawaguchi, 2018). In this review, we will focus on less-discussed aspects of the birthdate effect; specifically, how the relative timing of neurogenesis in identically specified neurons can create phenotypic diversities among them in terms of axon guidance and connections. One reason that we started to consider the contribution of relative timing in neurogenesis is that the post-genome era simply casted a doubt about whether diverse neuronal phenotypes are truly explainable by differential gene expressions alone. Particularly, we are concerned with axon wiring and connection patterns. After Sperry’s chemoaffinity hypothesis (Sperry, 1963), researchers looked for the specific chemical tags that mediate axon and target recognition. Specific pairs of axon guidance molecules and their receptors, in more recent terminology, were successfully
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Fig. 1. The earlier the start, the greater the reach. (A) An early-born sibling develops earlier compared to a later-born sibling. (B) In the developing nervous system, an early-born neuron starts to elongate its axon earlier, and therefore reach the target earlier, so that the axon can spend more time to grow farther and expand the territory by the “first come, first served” rule. On the other hand, the axon of a late-born neuron reaches its target later and settles for a limited territory.
Fig. 2. Born together wire together. (A) People of similar age are more likely to interact with each other in human society. (B) In the nervous system, pre- and post-synaptic neurons that are both in the appropriate timing for synaptogenesis selectively make connections, forming time-matched networks.
identified, but the numbers of these “tags” are too small to account for construction of the myriad of highly diversified neural connections (Polleux et al., 2007; Stoeckli, 2018; Yu and Bargmann, 2001). These guidance molecules can have greater functions than their numbers, because they are repetitively used in different places and times, and combine their forces to modify their individual functions. Yet, it appears that our knowledge regarding molecular axon guidance is vastly insufficient to explain the actual phenomena. If we turn our attention to classic articles from 1970s, many authors discuss the non-molecular force of axon guidance inspired by the temporal order of neurogenesis (Bayer and Altman, 1987). These mechanisms can possibly explain phenotypic diversification of neurons without any chemical tags. In this review, we would like to revisit the non-molecular form of axon guidance from the perspective of “timing”. We will also discuss other potential scenarios where the neurogenetic “timing” may have significant influence on neuronal connections. We propose three hypotheses: 1) the earlier the start, the greater the reach (Fig. 1), 2) born together, wire together (Fig. 2) and 3) different times, different ways (Fig. 3). Because this classification is new and far from complete, let us start with anecdotal examples to clarify the essence that we try to convey in each hypothesis.
when the neurons are born. Yet, there is probably more to the birthdate. Let us consider three additional situations where the birthdate affects people more indirectly. First, the birthdate automatically determines the birth order in siblings (Fig. 1A). Even though all siblings inherit stochastically equal genetic traits, by the so-called “birth order effect” each child is supposed to develop a personal character typical to the birth order. A rather inevitable consequence of the birth order is that the early-born ones start performing various activities earlier and are generally larger, thereby dominate some space in the family. The second scenario is a situation where the birth timing of both oneself and others are important (Fig. 2A). People tend to choose their partners and friends of a similar age over other generations, even if they are born in distant places. This tendency results in a strong demographic force to bundle similarly aged people in the same social network. Lastly, environmental transitions can affect people’s behavior depending on their birthdates (Fig. 3A). Consider the situation in Berlin. When the Berlin Wall was present, people could not move across this boundary. People born after its collapse in 1989, however, can behave in a completely different way. In the following sections, we extend the above three scenarios one by one and propose that similar effects of the birthdate may be applicable to neurons.
2. Significance of the birthdate in human society 3. The earlier the start, the greater the reach In astrology, the birthdate deterministically allocates intrinsic properties to individuals, who live out with their destined fates irrespective of the circumstances surrounding them. This is actually similar to the situation in neurogenesis, where neuronal fates are genetically and molecularly specified by the birthdate at the time
3 H-thymidine birthdate analyses conducted during 1960–1970 often noted that early-born neurons have large cell bodies with long axons and late-born neurons are small with short axons (Altman and Bayer, 1975; Altman and Das, 1965; Hinds, 1968). In those
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Fig. 3. Different times, different ways. (A) A transition of social historical environment creates peoples’ distinct behaviors in Berlin. (B) In this hypothetical situation of a nervous system, a repulsive guidance molecule begins to be expressed halfway through the process of axon projections. Suppose that all axons express the receptor for this guidance molecule. Early-growing axons pass through the domain, because they reach it before the expression of the guidance molecule. Later-growing axons are repelled by the guidance molecule and project into a different way.
days, the primary focus was the comparison of large projection neurons and small interneurons. Since our current knowledge indicates that these two populations originate from totally segregated neural progenitors with highly distinct gene expressions (Bandler et al., 2017; Hu et al., 2017), these remarks may not be directly applicable to the present discussion. There are still some examples that larger neurons differentiate earlier from the same progenitor pools (Hinds, 1968; Lawson et al., 1974), but also other cases that the generation of medium-sized neurons precedes that of largesized ones (Jones, 1984; Walsh et al., 1983). Thus, it appears that there is no general consensus about correlation between birthdate and neuron size. Meanwhile, a more important lesson gained from these arguments would be that a functional benefit may exist when the generation of long projection neurons precedes that of local interneurons (Hinds, 1968; Nishida and Ito, 2017); it is conceivable that the long projection neurons require time to extend their axon terminals to the distant target to make functional connections with local interneurons there. Conceivably, neurons can make use of differences of their birthdate timings. Suppose that a wave of neurogenesis for a single neuronal type typically continues around 2–4 days (Bayer and Altman, 1987). Since the speed of axon elongation is estimated as 20–100 m per hour (Godement et al., 1994; Halloran and Kalil, 1994; Sretavan and Reichardt, 1993), the last axons would lag behind the first ones by 1–10 mm, which readily covers the full dimension of a typical target (Fig. 1B). Indeed, time-different arrival of axons is readily observable as a chronological growth ring in some axon tracts (Inaki et al., 2004; Walsh, 1986; Walsh and Guillery, 1985; Yamatani et al., 2004). Furthermore, a long-delayed arrival of axons grown by late-born neurons has been directly shown in a visual target (Dallimore et al., 2002). Since early-born neurons reach their axons to the target earlier, they would have ample time to develop their terminals farther and occupy more of the limited target sites as compared with the later cohorts by the “first come, first served” rule (Fig. 1B). An observation that may support this scenario is that axon projections from the main olfactory bulb extend to around ten target areas that are spatially continuous in the brain. During development, the bulb axons first penetrate only proximal targets and then gradually expand over distant targets (Schwob and Price, 1978). Yet, even in the adult stage, the proximal targets that receive early innervation are more densely populated with the bulb axons
compared with the distal targets (Schwob and Price, 1984). Our preliminary observation also suggests that the last-born projection neurons in the main olfactory bulb, which are generated at the perinatal stage in mice, have only short axons that manage to reach only the proximal target in adulthood (Hirata, unpublished observation). Thus, the earlier neurons start, the greater their axons reach at least in the central olfactory system. 4. Born together, wire together Time-matched synaptogenesis has been extensively discussed previously (Bayer and Altman, 1987). This hypothesis postulates that both pre- and post-synaptic neurons have specific maturation stages appropriate for synaptogenesis, and that neurons which form good match in the stages selectively make synaptic connections (Fig. 2B). For example in rats, the projection neurons in the accessory olfactory bulbs are born two days earlier that those in the main olfactory bulbs (Bayer, 1983). Their axons make segregated projections onto their own specific targets, even though some of the accessory and main bulb targets are juxtaposed with no physical boundary. Interestingly, the postsynaptic neurons in the accessory bulb targets differentiate earlier than those in the main bulb targets (Bayer, 1980). Therefore, when the early-born accessory bulb neurons project their axons, the only available targets are the neurons in the accessory bulb targets, whereas the late-born main bulb neurons can selectively connect with the age-matched neurons in the main bulb targets, which are now ready for receiving innervation. Similar correlations in the neurogenetic timing of pre- and postsynaptic partners have been documented in many other nervous systems as well (Bayer and Altman, 1987). One of the most intensively studied regions describing timematched connections is the hippocampus; there is a strong spatiotemporal correlation of the arrival time of afferent axons, and the dendritic zones that receive the axons in the hippocampal pyramidal as well as dentate gyrus granule cells. Specifically, the first arriving afferents occupy the most distal zone of the dendrites, and later ones sequentially occupy a more proximal territory (Bayer and Altman, 1987). In the same dendritic zone, the axons from the ipsilateral and contralateral hippocampi compete for post-synaptic sites (O’Leary et al. 1979), and in this competition, time-matched synaptogenesis seems to take place (Gottlieb and Cowan, 1972). Specifically, early-born dentate granule cells receive more ipsi-
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lateral afferents that arrive earlier than the contralateral ones, whereas late-born granule cells receive ipsilateral and contralateral afferents almost equally, because both the afferents exist at comparable levels at that stage. More recently, an experimental test was conducted to verify time-matched hippocampus connections. Deguchi et al. (2011) found that early- and late-born subpopulations of dentate granule cells selectively connect with early- and late-born subpopulations of hippocampus CA3 pyramidal neurons, respectively. The time windows for synaptogenesis of these selective pairs are largely non-overlapped. By heterochronically co-culturing the preand post-tissues derived from different developmental stages, the authors showed that non-selective pairs make connections if, and only if, maturation stages are matched. Thus, matching of maturation stage can even overwrite the molecularly defined differences of neuronal subpopulations. This implies that temporal matching is the key mechanism for the selectivity of connections, i.e. neurons that born together wire together.
6. Future projections We have discussed potential scenarios where “timing” can increase diversity among neurons. Most examples described here show only correlations but have not tested experimentally. The reason is obvious; the hypotheses were not testable back in those days. However, the subsequent revolution of molecular biology techniques and developmental engineering has made it possible to directly test these hypotheses. For example, we recently developed a neuronal birthdate tag technique, by which neurons are genetically tagged with loxP recombination in a neuronal birthdate-dependent manner (Hirata, unpublished data). Using such a technique and combining it with the method to alter the timing of neurogenesis or axon projections (Mizutani and Saito, 2005; Olsson-Carter and Slack, 2010), we may be able to address the real significance of “neurogenetic timing” in the near future. Declarations of interest None.
5. Different times, different ways Acknowledgements Since neurogenesis is a protracted process, early-born and lateborn neurons could encounter drastically different landscapes in the rapidly changing developmental environment. For example, the attractive axon guidance molecule Netrin1 begins to be expressed in a small ventral domain within the central olfactory target area, shortly before the end of olfactory bulb projections (Kawasaki et al., 2006, unpublished observation). Its specific receptor DCC is expressed by virtually all olfactory bulb projection neurons during the time when the axons are in an active growing phase (Inaki et al., 2004). These observations suggest that the early growing axons from the olfactory bulb miss the chance to recognize Netrin1, whereas the late growing axons can respond to the delayed expression of Netrin1. Our observations indeed show that only the late-growing axons from the bulb selectively penetrate the small ventral domain (Yamatani et al., 2004) in which Netrin1 is expressed in the late developmental stage. This scenario may not be very uncommon, because many axon guidance molecules are expressed only transiently in a spatiotemporally restricted manner (Huber et al., 2005; Ito et al., 2008; Kawasaki et al., 2006). Furthermore, heterochronic culture assays have detected developmental transition of axon guidance environment in various nervous systems (Gotz et al., 1992; Hirata and Fujisawa, 1997, 1999; Pini, 1993; Tuttle et al., 1995). Yet, in these cases, it is not clear whether the environmental transition occurs during the time when the axons that are responsive to the same guidance signals are projecting, thereby phenotypically splitting neuron populations, which will otherwise have the same projection patterns. As far as we know, the only example with experimental support for this hypothesis is the ipsilateral projections of retinal axons in Xenopus (Nakagawa et al., 2000) (Fig. 3B). In tadpoles, the retinal axons solely project to the contralateral side through the optic chiasm. Only after metamorphosis, the late-born neurons, which are still generated in the ventro-temporal retina, begin to project axons ipsilaterally to accommodate the shift of visual fields caused by the metamorphic eye translocation. These ipsilateral projections are triggered by the late expression of Ephrin-B, a repulsive axon guidance molecule in the optic chiasm. This trigger is purely environmental, because if Ephrin-B is prematurely expressed in the optic chiasm in the tadpoles, the earlier-born retinal neurons that express the Ephrin-B receptor precociously project the axons ipsilaterally. Thus, in this system, the early-born and late-born neurons go different ways because they are born different times.
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Please cite this article in press as: Hirata, T., Iwai, L., Timing matters: A strategy for neurons to make diverse connections. Neurosci. Res. (2018), https://doi.org/10.1016/j.neures.2018.09.006