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Department of Physiology, Tokyo Medical and Dental University, Graduate School and Faculty of Medicine, Tokyo 113-8519, Japan
Submitted 12 April 2004; accepted in final form 26 May 2004
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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; Saper 1995; Spyer 1982). Therefore the investigation of the NTS function is of great importance; not only to reveal how visceral information is integrated in the brain stem, but also to elucidate, as one of the fundamental models, how the CNS processes sensory information from the peripheries.
Although many anatomical and physiological studies have been done in adult animals, the ontogenetic approach to the physiological functions of the NTS has been hampered because of the small size and fragility of embryonic NTS neurons. We employed an optical recording technique with voltage-sensitive dyes (for reviews, see Cohen and Salzberg 1978; Grinvald et al. 1988; Salzberg 1983; Wu et al. 1998) and proved that the optical technique is a useful tool for analyzing the embryogenetic expression of neural functions in the CNS (for reviews, see Kamino 1990; Momose-Sato et al. 2001, 2002).
In our previous investigations, we examined the spatio-temporal patterns of neural activity evoked by glossopharyngeal/vagal stimulation in embryonic brainstems. We showed three-dimensional profiles of the glossopharyngeal/vagal response areas corresponding to the NTS (sensory nucleus), the dorsal motor nucleus of the vagus nerve (DMNV: motor nucleus), and the nucleus of the glossopharyngeal nerve (Nucl IX: motor nucleus) in chick and rat embryos (Komuro et al. 1991; Momose-Sato et al. 1991, 1994, 1999; Sato et al. 1995, 1998, 2002a, b, 2004). In these studies, we proved the following characteristics of the embryonic chick NTS. 1) In both the N. IX- and N. X-related NTS, optical signals were composed of fast and slow signals, and the fast signal corresponded mainly to the presynaptic action potential and the slow signal to the glutamatergic excitatory postsynaptic potential (EPSP) (Komuro et al. 1991; Momose-Sato 1994; Sato et al. 1995). 2) In both the N. IX- and N. X-related NTS, the glutamatergic EPSPs consisted of non–N-methyl-D-aspartate (NMDA) and NMDA receptor components (Komuro et al. 1991; Momose-Sato et al. 1994). 3) In the N. X-related NTS, the glutamertagic EPSP was expressed at day 7 of incubation in normal Ringer solution. However, synaptic function mediated by NMDA receptors was already generated latently at the 6-day-old embryonic stage, and the onset of synaptic function was regulated by a Mg2+ block on the NMDA receptors (Momose-Sato et al. 1994). 4) In the N. X-related NTS, the DL-2-amino-5-phosphonovaleric acid (APV) and Mg2+ sensitivity of the vagal glutamatergic EPSPs changed during development (Momose-Sato et al. 1994).
In the ontogenetic approaches to elucidate a manner of sensory information processing in the NTS, it is important to clarify whether there are any differences in developmental organization of synaptic functions between the N. IX and N. X. In this study, we addressed two questions: 1) whether the dynamic changes in the APV/Mg2+ sensitivity of the glutamertagic EPSPs are also observed in the N. IX-related NTS and 2) whether the synaptic function in the N. IX-related NTS emerges at the same time in the N. X-related NTS. From the results obtained, we extracted principles of the developmental expression of the NTS function.
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METHODS |
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Brain stem slice preparations dissected from 5- to 9-day-old embryonic (E5–E9) chicks were used (n = 36). Experiments were carried out in accordance with the Tokyo Medical and Dental University guidelines for the care and use of laboratory animals. All efforts were made to minimize the number of animals used and their suffering. Fertilized eggs of White Leghorn chickens (Saitama Experimental Animals Supply, Saitama, Japan) were incubated for 5–9 days in a forced-draft incubator (type P-008, Showa Incubator Laboratories, Urawa, Japan) at a temperature of 37°C and 60% humidity, and were turned once each hour. In the present experiment, E5 corresponded to the Hamburger-Hamilton stage (H-H stages: Hamburger and Hamilton 1951) 26–27, E6 to stages 28–29, E7 to stages 30–32, E8 to stages 33–34, and E9 to stage 35. The embryos were decapitated, and brainstems, with the glossopharyngeal nerve fiber attached, were dissected from the embryos. Slice preparations of about 1,500 µm thickness were made from the isolated brain stem at the level of the glossopharyngeal nerve root. The pia mater was carefully removed in the bathing solution. After staining with the dye, the preparation was attached to the silicone (KE 106LTV, Shin-etsu Chemical, Tokyo, Japan) bottom of a simple chamber with the spinal cord side up. The bathing solution contained (in mM) 138 NaCl, 5.4 KCl, 1.8 CaCl2, 0.5 MgCl2, and 10 glucose (10 Tris-HCl buffer; pH 7.3). The solution was equilibrated with oxygen.
Voltage-sensitive dye staining
Each preparation was stained by incubating it for 20 min in Ringer solution containing 0.2 mg/ml of a voltage-sensitive merocyanine-rhodanine dye, NK2761 (Hayashibara Biochemical Laboratories/Kankoh-Shikiso Kenkyusho, Okayama, Japan) (Kamino et al. 1981; Momose-Sato et al. 1995), and the excess (unbound) dye was washed away with dye-free Ringer solution before recording. This merocyanine-rhodanine dye has been shown to be particularly useful in embryonic nervous and cardiac tissues (Kamino 1991; Momose-Sato et al. 1995).
Electrical stimulation
The cut end of the glossopharyngeal nerve was drawn into a micro-suction electrode fabricated from a hematocrit tube (VC-HO75P, TERUMO, Tokyo, Japan), which had been hand-pulled to a fine tip (about 100 µm internal diam) over a low-temperature flame. Positive (depolarizing) square current pulses (8 µA/5 ms), which evoked maximum responses, were applied to the glossopharyngeal nerve at intervals of 10–15 min.
Optical recording
Light from a 300-W tungsten-halogen lamp (type JC-24V/300W, Kondo Philips, Tokyo, Japan) was collimated, rendered quasi-monochromatic with a heat filter and an interference filter with a transmission maximum at 703 ± 15 nm (Asahi Spectra, Tokyo, Japan), and focused on the preparation. An objective [S Plan Apo, 10x, 0.4 numerical aperture (NA)] and a photographic eyepiece projected a real image of the preparation (magnification, 25x) onto a multi-element silicon photodiode matrix array mounted on an Olympus Vanox microscope (type AHB-L-1, Olympus Optical, Tokyo, Japan). The focal plane was set on different depths with moving a microscope stage. To detect the largest optical responses from the N. IX-related NTS, we set the focal plane at the level of the glossopharyngeal nerve root (Fig. 1; also see Sato et al. 1995). In the present experiments, we used the 128ch optical recording system using a 12 x 12-element silicon photodiode array (MD-144-4PV, Centronic, Croydon, UK), which was constructed in our laboratory (for reviews, see Kamino 1991; Momose-Sato et al. 2001). Each pixel (element) of the array detected light transmitted by a square region (56 x 56 µm2 using 25x magnification) of the preparation. The output of each detector in the diode array was passed to an amplifier (time constant of AC-coupling 
3 s) via a current-to-voltage converter. The amplified outputs from 127 elements of the detector were first recorded simultaneously on a 128-channel recording system (RP-890 series, NF Electronic Instruments, Yokohama, Japan) and were passed to a computer. The time resolution of this system was 1 ms. The time interval between each recording was 10–15 min, and incident light was turned off except during the measuring period. In this condition, little or no signal fatigue was observed, and the degree of variability between successive recordings in terms of amplitude and duration of the signals was small. The recordings were made in a single sweep. The optical measurement was carried out in a still chamber without continuous perfusion with Ringer solution at room temperature (26–30°C). The recorded signals were presented as the fractional change 
I/I (the change in the light intensity divided by DC background intensity).
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RESULTS |
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To show a typical response pattern of neural activity in the N. IX-related brain stem nuclei, we show color-coded representations of multiple-site optical sectioning recordings of neural activity induced by N. IX stimulation in an 8-day-old preparation (Fig. 1), which was recorded in a similar way as described previously (Sato et al. 2002a). The focus was set to two different depths: focus 1 corresponding to 500 µm cephalic to the level of the glossopharyngeal nerve root and focus 2 corresponding to the level of the glossopharyngeal nerve root. With a stimulating current applied to the right glossopharyngeal nerve, action potentials (fast signals) were most clearly recorded from the dorso-medial region in focus 1, whereas glutamate-mediated EPSPs (slow signals) were detected mainly from the dorso-lateral region in focus 2. These regions correspond to the nucleus of the glossopharyngeal nerve (Nucl IX; motor nucleus) and the nucleus of the tractus solitarius (NTS; sensory nucleus), respectively (Breazile 1979; Sato et al. 1995).
In our previous studies, we did similar experiments in other focal planes and in every developmental stage tested (5- to 9-day-old embryos). Although the signals were not completely separated in the two focal planes, the response in the Nucl IX was most clearly detected from focus 1, whereas that in the NTS was largest at the level of focus 2 (Sato et al. 1995, 2002a). In this study, we recorded slow signals on focus 2 and examined dynamic changes in the N. IX-related synaptic function in the NTS.
Developmental changes in APV sensitivity of the slow optical signal
Figure 2 shows optical signals induced by glossopharyngeal nerve stimulation and the suppressive effects of APV on the optical signals. In Fig. 2A, the left recording shows control signals recorded in normal Ringer solution and the right one shows signals recorded in an APV-containing solution in an 8-day-old preparation. The later phase of the slow signals was markedly reduced when APV (200 µM) was added to the bathing solution (also see Fig. 2B), while the initial phase of the slow signals was reduced by an application of 6-cyano-7-nitroquinoxaline-2, 3-dione (CNQX; 5 µM; Fig. 2C). These results imply that the later phase of postsynaptic potentials in the NTS is mediated by NMDA receptors, while the initial phase is mediated by non-NMDA receptors. In Fig. 2B, we show enlarged traces of optical signals detected from 7- to 9-day-old preparations. The amplitude of the slow signal gradually increased with development. In the presence of APV, the later phase of the slow signal was reduced in every developmental stage.
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). It has also been assumed that the fractional signal size is proportional to the magnitude of the membrane potential changes in each cell and process and to the number and membrane area of activated neural elements within the field detected optically by one photodiode under conditions where the amount of dye bound to the membrane is uniform (Kamino et al. 1989; Obaid et al. 1985; Orbach et al. 1985). To reveal the spatial distribution pattern of the glossopharyngeal responses and the APV sensitivity, we measured the areas under the slow signal curves (signal area) obtained in normal and APV-containing solutions and constructed maps of the contour lines of the signal areas. The maps shown in Fig. 3A were constructed using the recordings from 7- to 9-day-old preparations. The top row shows the maps of the control signals in each preparation, the second row was made with data obtained from the APV-containing solution, and the third row was made with the differences [S = (the slow signal area in normal solution) – (the area estimated in the APV-containing solution)]. The value of S reached a saturation level with the APV concentration used in this study.
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S (third row) was also very similar to that of the control signal area, with the relative position of the peak area site of S corresponding to that of the control signal area. The size of S gradually increased with development, suggesting that the NMDA receptor–mediated component of the glutamatergic excitatory postsynaptic function gradually increases in the NTS during development (also see Table 1).
To examine the relative sensitivity to APV, we estimated the ratios of the APV-induced reduction area (S) to the control area (S) and made distribution maps of the ratios (S/S). Figure 3B shows the distribution of the ratio for the signal component reduced by APV. The data were obtained from the maps shown in Fig. 3A. In these maps, the values of the ratio (S/S) are indicated by the relative size of the solid circles: the ratios were divided into five sizes. There were differences in the regional distribution pattern of the ratio (S/S) between these preparations. In the 7-day-old preparation, the ratio was almost homogenous in the NTS; in the 8-day-old preparation, the ratio was larger in the medial region; and in the 9-day-old preparation, the ratio increased over the whole response area with the distribution pattern being similar to that in the 8-day-old preparation (see Table 1). These features are considered to represent the regional distribution of APV sensitivity and of the ratio of functionally expressed NMDA receptors to total glutamatergic receptor function.
Developmental changes in Mg2+ sensitivity of the slow optical signal
It is well known that the NMDA receptor function is blocked by extracellular Mg2+ 
(Mayer et al. 1984; for a review, see Collingridge and Lester 1989). Figure 4 shows the effects of 
removal on the optical signals evoked by glossopharyngeal nerve stimulation. In Fig. 4A, the left recording shows control signals recorded in normal Ringer solution and the right one shows signals recorded in a Mg2+-free solution in an 8-day-old preparation. Enlarged traces of the optical signals detected from 7- to 9-day-old preparations are shown in Fig. 4B. The slow signal was markedly enhanced in the Mg2+-free solution in every developmental stage. This effect was blocked by APV (200 µM; data not shown), suggesting that the enhancive effect of removal is mediated by the NMDA receptor.
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S = (the slow signal area estimated in the Mg2+-free solution) – (the area in normal solution)]. In Fig. 5A, the patterns of the three contour line maps (control, Mg2+-free, and difference) were similar in each developmental stage. At E7 and E8, the peak area sites were positioned in the lateral region, whereas at E9, they were located in the medial region.
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S to the control area (S). In Fig. 5B, the values of the ratio (S/S) are represented by the relative sizes of solid circles: the size was divided into five grades. The data were obtained from the three preparations shown in Fig. 5A. In these maps, it was shown that the relative sensitivity to external Mg2+ was greatest in the 8-day-old preparation (see Table 2) and that the signals in the ventral region of the response area were relatively more affected by external Mg2+ than in the dorsal region. These results show that the relative sensitivity to does not increase in a simple fashion but dynamically changes during development.
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At the 6-day-old embryonic stage, glossopharyngeal nerve stimulation evoked no or very small postsynaptic responses in the NTS (n = 4). We examined whether the removal of induced expression of postsynaptic responses that were not significant in normal Ringer solution.
Figure 6A shows two examples of optical recordings obtained with glossopharyngeal nerve stimulation in 6-day-old preparations. In these preparations, glossopharyngeal nerve stimulation evoked only fast spike-like signals in normal Ringer solution: the slow signal was not significant (<1 x 10–4; Fig. 6A, left). However, when Mg2+ was removed from the extracellular solution, significant slow signals were elicited (Fig. 6A, right) in the region corresponding to the NTS (indicated by yellow in the top panels). The slow signals induced in the Mg2+-free solution were blocked by APV (200 µM), suggesting that they are attributable to NMDA receptors.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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) and consider a principle of the developmental expression of the NTS function. Developmental changes in APV/Mg2+ sensitivity of the glutamatergic EPSPs in the NTS
The glutamate receptor is conventionally divided into the NMDA receptor and the non-NMDA receptor, and APV is considered to be a specific antagonist to the NMDA receptor (Davies et al. 1981; for reviews, see Collingridge and Lester 1989; MacDonald and Nowak 1990; Watkins and Evans 1981). In this study, we used APV as a pharmacological tool to separate the NMDA and non-NMDA receptor components of the EPSP-related slow optical signal. In Fig. 3, it seems reasonable to consider that the signal area diminished at the saturation level of APV [difference (S); Fig. 3A, bottom] corresponds to the NMDA receptor component and that the signal area unaffected by APV (Fig 3A, middle) corresponds to the non-NMDA receptor component. As shown in Fig. 4, the slow signal induced by N. IX stimulation was enhanced by removal, and this effect was blocked by APV. Therefore in Fig. 5, it is considered that the signal area enhanced by removal [difference (S); Fig. 5A, bottom) reflects the distribution pattern of Mg2+ sensitivity of the NMDA receptor.
In Figs. 3 and 5, we extracted the following characteristics of the N. IX-related synaptic function in the embryonic chick NTS. 1) The total areas of the glutamatergic EPSP gradually expanded, and the NMDA and non-NMDA receptor components also increased as development proceeded from the 7- to 9-day embryonic stage (Fig. 3A; Table 1). 2) The ratio of the NMDA receptor function to total glutamatergic receptor function slightly increased with development, and the distribution patterns of the ratio changed from a homogenous pattern to a medially shifted pattern (Fig. 3B; Table 1). 3) The peak-area site of Mg2+ sensitivity (Fig. 5A) moved medially with development, and this was consistent with the developmental changes in the NMDA-receptor component (Fig. 3A). 4) The ratio of the Mg2+ sensitivity increased at the 8-day embryonic stage and decreased again at the 9-day embryonic stage (Fig. 5B; Table 2).
In our previous study (Momose-Sato et al. 1994), we examined developmental changes in the slow signals evoked by vagus nerve stimulation and reported similar characteristics of the APV and Mg2+ sensitivity of the glutamertagic EPSPs in the N. X-related NTS. These results indicate that the developmental sequence of the glutamatergic receptor function in the NTS is the same for the N. IX- and N. X-related NTS.
Concerning Mg2+ sensitivity of the glutamatergic EPSPs, there seem to be some causes in its developmental change: one is that the total fraction of the NMDA receptor decreases at the 9-day-old embryonic stage and another is that the Mg2+ sensitivity of the NMDA receptor changes with development. Considering that the inhibitory effect of Mg2+ on the NMDA receptor is voltage-dependent (Mayer et al. 1984; Nowak et al. 1984), it is also possible that changes in resting membrane potential may play a role in the developmental changes in the Mg2+ sensitivity of the NMDA receptor. During early development, it is known that changes in excitatory amino acid receptors, particularly NMDA receptors, occur in the CNS, and a transient increase in the expression of glutamate, NMDA, and AMPA receptors has been shown in different brain areas (Baudry et al. 1981; Insel et al. 1990; Miller et al. 1990; Tremblay et al. 1988). In addition, it has been reported that the Mg2+ sensitivity of NMDA receptors changes during development, and it has been suggested that changes in Mg2+ regulation of the NMDA receptor may play a role in its development in the CNS (Bowe and Nadler 1990; Morrisett et al. 1990). The developmental change in the expression and the sensitivity to Mg2+ of the NMDA receptor may be related to the early development of synaptic transfer efficacy within the NTS.
Initial expression of synaptic function in the NTS
As shown in Fig. 6, in normal Ringer solution containing 0.5 mM Mg2+, only fast spike-like signals were usually observed in the 6-day-old preparations, whereas small slow signals were elicited by removal. In the embryonic chick N. X-related NTS, it has been shown that synaptic function mediated by NMDA receptors is latently generated at the 6-day-old stage and that the onset of synaptic function is regulated by a Mg2+ block on the NMDA receptors (Momose-Sato et al. 1994). These data indicate that, irrespective of projecting nerves, N. IX and N. X, synaptic function mediated by the NMDA receptor is generated in the NTS as early as the 6-day-old embryonic stage and is suppressed by external Mg2+.
In an anatomical investigation (Hiscock and Straznicky 1986), it has been reported that neurons in the distal glossopharyngeal and vagal ganglia are generated between the second and fifth days of incubation, and those in the proximal ganglia are produced between the fourth and seventh days. The results obtained with optical recording suggest that functional synapses of the glossopharyngeal and vagal nerves have already been generated by the 6-day-old embryonic stage, at which the neuronal generation in the proximal ganglia has not yet been completed.
The NTS has a number of unique anatomical and phenotypical features that contribute to its pivotal role in neuronal regulation and integration of autonomic functions. In adults, it is considered that the NTS is not a simple "relay" nucleus, but rather that it performs complex integration of information from multiple synaptic inputs from the periphery and central origins (Paton and Kasparov 2000). In this study, we showed that the initial expression and principal characteristics of synaptic function are similar between the N. IX- and N. X-related NTS. These results suggest that the peripheral information conducted by the N. IX and N. X may be simultaneously processed and integrated in the NTS from the beginning of nuclear organization.
One question in ontogenetic investigations of sensory information processing is whether there is any common feature in developmental organization of synaptic functions between different nerves that project to the same nucleus. This study showed that this was the case with the N. IX and N. X responses in the embryonic chick NTS. In Fig. 7, we summarize the sequence of the postsynaptic function in the chick NTS, which was common irrespective of the projecting nerves, the N. IX and N. X.
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ACKNOWLEDGMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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FOOTNOTES |
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Address for reprint requests and other correspondence: K. Sato, Dept. of Physiology, Tokyo Medical and Dental Univ., Graduate School and Faculty of Medicine, 1-5-45 Yushima, Bunkyo-ku, Tokyo 113-8519, Japan (E-mail: katsushige.phy2{at}tmd.ac.jp).
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REFERENCES |
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