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NEUROSCIENCE |
1 Centre de recherche Université Laval Robert-Giffard, Department of Psychiatry, Laval University School of Medicine, Quebec, Canada
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Abstract |
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(Received 31 January 2006;
accepted after revision 24 March 2006;
first published online 31 March 2006)
Corresponding author Z-w Zhang: Centre de recherche Universite Laval Robert-Giffard, 2601, de la canardière, F-6500 Québec, QC, G1J 2G3 Canada. Email: zhongwei.zhang{at}crulrg.ulaval.ca
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Introduction |
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In the peripheral nervous system, the elimination of redundant synapses is activity dependent (Lichtman & Colman, 2000). Blocking all synaptic transmission prevents synapses from being eliminated, whereas enhancing the level of activity at the postsynaptic site accelerates the process. At the neuromuscular junction, the relative strength of individual synapses can determine the fate of a synapse, suggesting a critical role for activity-dependent competition (Buffelli et al. 2003). It still unclear, however, whether neuronal activity plays an instructive role in synapse elimination in the brain.
The regression of redundant climbing fibres at the climbing fibre–Purkinje cell synapse (CF synapse) in the cerebellum is also activity dependent. Chronic blockade of N-methyl-D-aspartate receptors (NMDARs) during a critical period in early life attenuates the refinement of CF innervation pattern (Rabacchi et al. 1992; Kakizawa et al. 2000). However, functional NMDARs are absent at the CF and the parallel fibre synapses during the critical period, suggesting an indirect effect of NMDAR-mediated signalling on the refinement of CF synapses. Furthermore, disruptions of the function and maturation of the parallel fibre–PC synapse also attenuate the regression of redundant CF synapses (Crepel et al. 1980; Mariani & Changeux, 1980; Kano et al. 1997). Thus, interactions among different populations of synapses in the same neuron may have an important role in synapse elimination. This raises the possibility that pruning mechanisms are cell and synapse specific.
The retinogeniculate connection undergoes extensive remodelling during postnatal development (Shatz, 1996; Wong, 1999). After eye-specific segregation of retinal ganglion axons in the lateral geniculate nucleus but just before eye opening, each geniculate neuron in the mouse receives synaptic inputs from as many as 20 retinal ganglion cells; 2 weeks after eye opening, only one to three inputs remain (Chen & Regehr, 2000). Although the time course strongly suggests a role for sensory experience in the elimination of redundant retinal inputs, direct evidence is still missing. Moreover, it is unclear whether similar developmental changes can be found in other sensory thalamic nuclei.
In this study, we examined developmental remodelling at the lemniscal synapse of the somatosensory system related to the mystacial vibrissae (whiskers) in the mouse. The whisker system in rodents, because of its topographic organization and accessibility for sensory manipulation, has been widely used in structure–function analyses and in developmental studies (Killackey et al. 1995; Fox & Wong, 2005). We know more about the anatomy, physiology and development of the whisker system than any other neural pathways in mice and rats. The primary thalamic relay for the whisker system is the ventral posteromedial nucleus (VPm), which receives inputs from the principal five nucleus (Pr5) of the trigeminal sensory complex in the brainstem, and projects to the primary somatosensory cortex. The synapse formed between a Pr5 axon and a VPm neuron is called the lemniscal synapse, since Pr5 axons travel in the medial lemniscus before reaching the VPm. In adult rats, each VPm neuron receives inputs from one to three Pr5 axons (Deschenes et al. 2003). Whether this selectivity is the result of a developmental refinement is unknown. Here we show that lemniscal synapses in the murine VPm undergo extensive synapse elimination and remodelling during the second week after birth. Surprisingly, whisker deprivation has little effect on the developmental refinement at the lemniscal synapse.
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Methods |
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Brain slices were prepared from C57BL/6 mice of either sex aged P7 to P24 (with the day of birth as P0) using methods similar to those previously described (Zhang, 2004). All procedures were performed according to the guidelines of the Canadian Council on Animal Care, and were approved by the Animal Care Committee at Laval University. Briefly, mice were deeply anaesthetized with ketamine (100 mg/kg, ip) and xylazine (10 mg/kg, ip), and decapitated. The brain was removed quickly (< 60 s) and placed in ice-cold solution containing (mM): 210 sucrose, 3.0 KCl, 1.0 CaCl2, 3.0 MgSO4, 1.0 NaH2PO4, 26 NaHCO3 and 10 glucose, saturated with 95% O2 and 5% CO2. Sagittal slices were cut at 300 µm on a vibrating tissue slicer (VT 1000s, Leica, Germany), and kept in artificial cerebral spinal fluid (ACSF) containing (mM): 124 NaCl, 3.0 KCl, 1.5 CaCl2, 1.3 MgCl2, 1.0 NaH2PO4, 26 NaHCO3 and 20 glucose, saturated with 95% O2 and 5% CO2 at room temperatures (21–23°C). Slices were allowed to recover for at least 1 h before any recording.
Patch-clamp recording
For recording, a slice was transferred to a submerge-type chamber where it was continuously exposed to ACSF heated to 30–32°C, saturated with 95% O2 and 5% CO2 and flowing at a rate of 2.0 ± 0.2 ml min–1. The slices were viewed first with a 4 x objective; and those sections containing both the medial lemniscus (ML) and the ventral basal nucleus of the thalamus were chosen for recording (Fig. 1A). In general, two slices with both ML and VPm can be obtained from each hemisphere. A concentric bipolar electrode (25 or 50 µm tip diameter, FHC, Bowdoinham, ME, USA) was placed in the ML to stimulate the leminscal pathway. Neurons in the VPm were then viewed under near-infrared illumination with a 40 x water-immersion objective (Fluor, 40 x, 0.80 W, Nikon, Mississauga, ON, USA) and a CCD camera (IR-1000, MTI, Michigan City, IN, USA).
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. Liquid junction potential, estimated to be +5 mV, was not corrected unless indicated otherwise. The seal resistance was greater than 5 G. Whole-cell recordings were made at the soma with a Multiclamp 700A amplifier (Axon Instruments). The series resistance (Rs), usually between 7 and 15 M, was not compensated. Stimuli (100 µs, 1–400 µA) were applied at 0.1 Hz (PG4000A and SIU90, Cygnus Technology, Delaware Water Gap, PA, USA). Experiments were conducted using the Axograph 4.9 program (Axon Instruments). Data were filtered at 2 or 4 kHz, and digitized at 8 or 16 kHz. In some experiments, neurons were labelled with biocytin (0.25% in pipette solution); after recording, slices were processed as previously described (Zhang, 2004). Drugs and drug delivery
All agents were applied by changing the bath perfusate from standard ACSF to modified ACSF to which various drugs were simply added. All solutions were continuously bubbled with 95% O2 and 5% CO2. D-(–)amino-5-phosphonopentanoic acid (d-APV), 2,3-dioxo-6-nitro-1,2,3,4-tetrahydrobenzo[f]quinoxaline-7-sulphonamide (NBQX), ifenprodil and picrotoxin were purchased from Tocris (Ellisville, MO, USA). All other chemicals were purchased from Sigma-Aldrich Canada (Oakville, ON, Canada).
Sensory deprivation
Mice aged P5 were anaesthetized with isoflurane (1–4%, inhalation). Large whiskers on both sides of the snout were pulled out gently with a pair of forceps. This process was repeated every other day until P19.
Data analysis
AxoGraph 4.9 and Origin 7 (OriginLab, Nothampton, MA, USA) were used for analysis. Throughout, means are given ± S.E.M. Means were compared using two-tailed Student's t test, or one-way ANOVA. Distributions were compared with Kolmogorov-Smirnov test (K-S test).
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Results |
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Elimination of functional inputs during development
We examined the input–output relationship at the lemniscal synapse from P7 to P24. Neurons were voltage-clamped at –70 mV, and synaptic responses were recorded over a range of stimulus intensity. This procedure was repeated for the same neuron at the holding potential of +40 mV to examine the NMDA component of the EPSC. Examples of the results are illustrated in Fig. 2. In mice aged P20–24, the majority of neurons showed an all-or-none response following ML stimulation (Fig. 2D). These results are similar to those obtained in VPm of adult rats, suggesting that each VPm neuron at this age generally receives input from a single lemniscal axon. In contrast, neurons at P7–9 showed incremental increases in the synaptic response with stronger stimulus intensities (Fig. 2A). In mice aged P11–13, synaptic responses also showed multiple steps in response to stronger stimulus intensities, but the increase was achieved with fewer steps (Fig. 2B). At P16–17, most neurons showed all-or-none response (Fig. 2C), similar to that observed at P20–24. These findings suggest that at 1 week old, each VPm neuron receives input from many lemniscal axons, and each axon contributes a small fraction of the total synaptic response; the number of axons contacting each VPm neuron decreases rapidly over the next few days to reach the adult level by P16–17.
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Developmental changes in AMPA/NMDA ratio
We examined AMPA and NMDA components of the synaptic current from P7 to P24. As illustrated in Fig. 1C, the peak current recorded at –70 mV can be entirely attributed to AMPA receptor activation. At +40 mV, two distinct components were observed: a fast AMPA component, followed by a slowly rising and slowly decaying NMDA component (Fig. 1C). Since the AMPA component decays rapidly, the synaptic current after the initial 6 ms is mediated almost entirely by NMDA receptors. Accordingly, we estimated the ratio of AMPA to NMDA components by measuring, in the same cell, synaptic currents at –70 and +40 mV using the same stimulus intensity (Fig. 3A and B). The AMPA component was estimated by measuring the peak of EPSC at –70 mV, while the NMDA component was estimated at +40 mV by measuring the amplitude of EPSC at 7 ms after the beginning of EPSC. The results are summarized in Fig. 3C. The AMPA/NMDA ratio was 0.79 ± 0.08 at P7–9 (n = 22), but increased rapidly over the next few days to 2.44 ± 0.27 at P16–17 (n = 12), and was relatively stable thereafter.
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Developmental changes in the properties of the NMDA component
We examined the decay rate of the NMDA component of the synaptic current recorded at +40 mV. As illustrated in Fig. 5A–C, there was a significant reduction in the decay rate of EPSC recorded at +40 mV. The time constant of the decay was 99.1 ± 12.6 ms at P7–9 (n = 19), 44.5 ± 3.6 ms at P11–13 (n = 16), 36.6 ± 2.4 ms at P16–17 (n = 11), and 37.1 ± 1.9 ms at P20–24 (n = 23). Thus, the largest reduction in the decay time constant occurred during the second week.
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Previous studies have shown development changes in subunit composition of AMPA receptors at central synapses. Specifically, AMPA receptors in cortical pyramidal neurons lack the GluR2 subunit during early development, which results in an inward rectification and a high Ca2+ permeability (Kumar et al. 2002). An up-regulation and incorporation of GluR2 subunit lead to a linear I–V relationship and low Ca2+ permeability. To examine whether AMPA receptors at the lemniscal synapse undergo a similar change, we studied the I–V relationship of the AMPA component at P11–13 and P20–24 in the presence of the selective NMDA receptor antagonist D-APV (50 or 100 µM). At P12, the I–V curve of peak current showed a strong inward rectification (Fig. 7A). Surprisingly, a strong inward rectification was also present at P24 (Fig. 7B). We estimated the ratio of the peak current recorded at +35 mV to that at –35 mV, and used it as the rectification index (1 means no rectification, and 0 means complete inward rectification). The rectification index was 0.34 ± 0.04 at P11–13 (n = 7; Fig. 7C), not significantly different from that at P20–24 (0.36 ± 0.05, n = 5; P > 0.5, unpaired t test).
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Developmental changes in paired-pulse response
We studied paired-pulse responses at +40 and –70 mV from P7 to P24. As illustrated in Fig. 8A and B, paired-pulse stimulations at 50 ms interval consistently caused short-term depression of the synaptic response. We estimated the ratio of the second to the first response at both +40 mV (NMDA component) and –70 mV (AMPA component), and the results are summarized in Fig. 8C. The paired-pulse ratio of the NMDA component showed little change from P7 to P24, with 0.56 ± 0.04 at P7–9 (n = 14), 0.60 ± 0.02 at P11–13 (n = 13), 0.67 ± 0.04 at P16–17 (n = 10), and 0.57 ± 0.03 at P20–24 (n = 12). The paired-pulse ratio of the AMPA component was also stable from P7 to P24, with mean values of 0.63 ± 0.02 at P7–9, 0.58 ± 0.03 at P11–13, 0.58 ± 0.02 at P16–17, and 0.56 ± 0.03 at P20–24.
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The whisker sensory system is already functional in mice by the end of the first week. Whisking, a key feature of exploratory behaviour in mice, begins typically around P9. The lemniscal synapse, as the primary relay for whisker sensory information, is likely to be highly active during these early explorations. To examine whether sensory experience plays a role in synapse elimination and refinement at the lemniscal synapse, whisker deprivations were performed between P5 and P19 by removing all whiskers on both sides of the snout. Synaptic responses were examined at P20–23. Whisker deprivation had no effect on synapse elimination: the majority of VPm neurons received a single fibre in deprived mice with a distribution very similar to that of normal mice at the same age (Fig. 9A). Synaptic properties also did not differ significantly from normal mice. These include paired-pulse ratios (Fig. 9B), EPSC amplitudes (Fig. 9C), the AMPA/NMDA ratio, and decay constant of NMDAR-mediated EPSC. The paired-pulse ratio was 0.65 ± 0.04 (n = 16) at –70 mV, and 0.63 ± 0.02 at +40 mV, values not different from those obtained in normal mice (P > 0.01, unpaired t test). The maximum EPSC amplitude was 891 ± 123 pA (n = 16) at –70 mV and 667 ± 110 pA at +40 mV, also not different from those measured for normal mice (P > 0.5, unpaired t test). The AMPA/NMDA ratio was 2.37 ± 0.24 (n = 16), not different from that of normal mice (2.41 ± 0.31, n = 18; P > 0.5, unpaired t test). Finally, the decay constant for NMDAR currents was 35.6 ± 1.7 ms (n = 22) for whisker-deprived mice, a value not different from that of normal mice (37.1 ± 1.9 ms, n = 23; P > 0.5, unpaired t test).
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Discussion |
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Synapse elimination in the VPm during development
Tactile information from large whiskers on the rodent snout is relayed to the neocortex through two distinct pathways. The first involves the Pr5 in the brainstem and the VPm in the thalamus, and is called the lemniscal pathway (Williams et al. 1994; Veinante & Deschenes, 1999). The second, called the paralemniscal pathway, involves the spinal trigeminal subnucleus (Sp5) that projects to the posterior thalamic nucleus (Veinante et al. 2000). The lemniscal pathway is topographically organized; information from each whisker is relayed by discrete cluster of neurons in the Pr5 and the VPm.
The whisker-specific pattern emerges early during development. Whisker-specific segregation is already established by P4 in the VPm of rats (Belford & Killackey, 1979) and mice (Munoz et al. 1999). Our results showed that at P7–9, well after whisker-specific innervation pattern is formed, each VPm neuron is innervated by an average of eight lemniscal axons, but by P16–17, the majority of VPm neurons receive one or two lemniscal afferents. These findings suggest that initial connections from Pr5 to VPm neurons lack precision, and a much higher degree of specificity is achieved through synapse elimination during the second week, presumably involving local pruning of subsets of axonal branches.
The developmental refinement of innervation pattern in the VPm is similar to that observed in the lateral geniculate nucleus (LGN) in the mouse. Before eye opening but well after the formation of eye-specific zones, each LGN neuron receives a large number of ascending afferents from the retina – all but one to three are eliminated over the 3 weeks after eye opening (Chen & Regehr, 2000). However, the time course of refinement differs significantly between these two structures. In the VPm, an adult-like pattern is reached by P16–17, whereas in the LGN, the refinement lasts until P28. These findings suggest that although extensive synapse elimination may be a general phenomenon at relay synapses in thalamic nuclei, the critical period of refinement is synapse specific.
Developmental changes in synaptic properties in the VPm
Our results showed that the refinement of innervation pattern in the VPm is associated with dramatic changes in synaptic properties. While some of the changes are similar to those observed at other central glutamatergic synapses, others are clearly different.
The developmental increases in synaptic AMPA currents and in the ratio of AMPAR/NMDAR at the lemniscal synapse are similar to those observed at the retinogeniculate synapse in ferrets and mice (Ramoa & McCormick, 1994; Chen & Regehr, 2000), at thalamocortical synapses in rats and mice (Crair & Malenka, 1995; Lu et al. 2001), and at auditory relay synapses in the brain stem in rats and mice (Bellingham et al. 1998; Joshi & Wang, 2002; Youssoufian et al. 2005). Likewise, the developmental decreases in the amplitude and the duration of synaptic NMDAR current at the VPm relay synapse are comparable with those observed in the LGN (Ramoa & McCormick, 1994; Chen & Regehr, 2000), in auditory brain stem (Bellingham et al. 1998; Joshi & Wang, 2002; Youssoufian et al. 2005), in the optical tectum (Wu et al. 1996), the superior colliculus (Shi et al. 1997), and in the neocortex (Carmignoto & Vicini, 1992; Crair & Malenka, 1995; Lu et al. 2001). Furthermore, developmental decreases in the sensitivity to ifenprodil, the selective antagonist of NR2B-containing NMDARs, have been described at synapses in the LGN and the neocortex (Ramoa & Prusky, 1997; Lu et al. 2001). Thus, the maturation of the lemniscal synapse follows a general trend that involves acquisition of AMPA receptors and changes in subunit composition of NMDA receptors.
Inward rectification of synaptic AMPAR currents has been described in GABAergic interneurons throughout the brain, and has been attributed to a polyamine block of GluR2-lacking AMPA receptors (Burnashev et al. 1992; McBain & Dingledine, 1993; Kamboj et al. 1995; Koh et al. 1995). In pyramidal neurons of the neocortex, inward rectification of AMPAR currents is only present before P16, and the developmental change is associated with an increase in GluR2 expression in these neurons (Kumar et al. 2002). Our results showed that at the lemniscal synapse, there was little change in the inward rectification of AMPAR currents between P11 and P24. This finding is consistent with previous studies showing low levels of GluR2 in the VPm of young and adult rats (Spreafico et al. 1994; Liu, 1997; Mineff & Weinberg, 2000). The presence of GluR2-lacking AMPARs at the leminiscal synapse may have implications for the transmission of sensory information through the thalamus.
Our results showed paired-pulse depression at the lemniscal synapse for the period of P7 to P24. This is comparable with the results obtained at the retinogeniculate synapse (Chen & Regehr, 2000), but is different from the results obtained at corticothalamic synapses where paired-pulse facilitation has been observed in both young and adult thalamic neurons (Turner & Salt, 1998; Castro-Alamancos & Calcagnotto, 1999; Reichova & Sherman, 2004). Our results are also different from those in the striatum, the cerebellum and the neocortex, where a developmental shift from paired-pulse depression to facilitation has been observed (Choi & Lovinger, 1997; Pouzat & Hestrin, 1997; Reyes & Sakmann, 1999; Kumar & Huguenard, 2001; Zhang, 2004). The lack of change in paired-pulse ratios indicates that the release probability reaches maturity before P7 at the lemniscal synapse, suggesting that an increase in the number or the size of the release site is associated with the maturation of the lemniscal synapse after P7.
Role of sensory experience in synaptic remodelling in the VPm
Previous studies have demonstrated a critical role for activity in the refinement and maturation of synapses in many parts of the nervous system (Katz & Shatz, 1996; Lichtman & Colman, 2000). Our results show that the lemniscal synapse in mice undergoes extensive remodelling during the second week when the animal starts to explore the environment. It comes as a surprise therefore that whisker deprivation had little effect on the development of the synapse. Neither the innervation pattern nor the properties of the synapse appeared to be affected by whisker deprivation. A recent study has shown that whisker deprivation reduces the elimination of dendritic spines in the somatosensory cortex of young mice (Zuo et al. 2005). In this case, however, whisker deprivation was performed between 4 and 6 weeks after birth, and it is unclear how sensory deprivation affects the early phase of synapse elimination in the neocortex. Our results are in line with those obtained at the calyx of Held in congenitally deaf mice, where the development of synaptic properties appears to be normal in the absence of auditory nerve activity (Youssoufian et al. 2005).
Our results do not exclude the possibility that spontaneous activities play important roles in the remodelling of the lemniscal synapse. Neurons in the trigeminal ganglion or the Pr5 could be spontaneously active in young mice, which would lead to activity at the lemniscal synapse. Similarly, spontaneous activities in the neocortex, via the corticothalamic pathway, may promote the remodelling of lemniscal synapses through heterosynaptic mechanisms.
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