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International Journal of Neuroscience, 119:214–226, 2009 C 2009 Informa Healthcare USA, Inc. Copyright ISSN: 0020-7454 / 1543-5245 online DOI: 10.1080/00207450802330819 Downloaded By: [University of Tokyo/TOKYO DAIGAKU] At: 10:00 13 January 2009 REGIONAL DIFFERENCE IN STAINABILITY WITH CALCIUM-SENSITIVE ACETOXYMETHYL-ESTER PROBES IN MOUSE BRAIN SLICES SHIGEHIRO NAMIKI Graduate School of Life and Environmental Sciences University of Tsukuba Ibaraki, Japan and Laboratory of Chemical Pharmacology Graduate School of Pharmaceutical Sciences The University of Tokyo Tokyo, Japan TAKUYA SASAKI NORIO MATSUKI Laboratory of Chemical Pharmacology Graduate School of Pharmaceutical Sciences The University of Tokyo Tokyo, Japan YUJI IKEGAYA Laboratory of Chemical Pharmacology Graduate School of Pharmaceutical Sciences We are grateful to thank members of our laboratory for helpful discussion. This work was supported in part by a Grant-in-Aid for Science Research on Priority Areas (Elucidation of Neural Network Function in the Brain, numbers 18021008 and 17023015), Grants-in-Aid for Science Research 17650090 and 17689004 from the Ministry of Education, Culture, Sports, Science, and Technology of Japan, Sumitomo Foundation Grant 050038. Address correspondence to Yuji Ikegaya, Laboratory of Chemical Pharmacology, Graduate School of Pharmaceutical Sciences, The University of Tokyo, Tokyo, 113-0033, Japan. E-mail: [email protected] 214 AM-DYE LOADING OF ACUTE BRAIN SLICES 215 Downloaded By: [University of Tokyo/TOKYO DAIGAKU] At: 10:00 13 January 2009 The University of Tokyo Tokyo, Japan and Precursory Research for Embryonic Science and Technology (PRESTO) Japan Science and Technology Agency Tokyo, Japan Loading neurons with membrane permeable Ca2+ indicators is a core experimental procedure in functional multineuron Ca2+ imaging (fMCI), an optical technique for monitoring multiple neuronal activities. Although fMCI has been applied to several brain networks, including cerebral cortex, hippocampus, and cerebellum, no studies have systematically addressed the dye-loading efficiency in different brain regions. Here, we describe the stainability of Oregon Green 488 BAPTA-1AM in mouse acute brain slice preparations. The data are suggestive of the potential usability of fMCI in many brain regions, including olfactory bulb, thalamus, dentate gyrus, habenular nucleus, and pons. Keywords acetoxymethyl ester, calcium imaging, fMCI, mouse, neuron, slice INTRODUCTION Functional multineuron Ca2+ imaging (fMCI) is a method to optically record the spiking activity from a large number of cells by taking advantage of the fact that the intracellular Ca2+ concentration in the cell body of a neuron increases transiently in response to individual action potentials. Because the signal is evident so as to detect a single action potential and clearly distinguishable from that of neighboring neurons, fMCI can reconstruct large-scale spike trains at the single cell level from neuronal networks in situ (Takahashi, Sasaki, Usami, Matsuki, & Ikegaya, 2007). This spatial resolution is a great advantage over many other techniques such as electroencephalogram, functional magnetic resonance imaging, and voltage-sensitive dye imaging. Another advantage of fMCI is the signal source identification, that is, fMCI can precisely determine the locations of individual cells that fire spikes and even do not fire spikes. This identification cannot be achieved by electrophysiological single-unit and multiple-unit recording techniques. Moreover, fMCI is, currently, the only technique that can simultaneously monitor the activity of thousands of neurons, and hence it could serve as a new-generation tool for disclosing the hidden dynamics of huge neuronal networks (Cossart, Aronov, & Yuste, 2003; Ikegaya et al., 2004; Ohki, Chung, Ch’ng, Kara, & Reid, 2005). To monitor Ca2+ signals, one has to load cells with Ca2+ indicators. For large-scale recordings, there are mainly two options so far. One is to use Downloaded By: [University of Tokyo/TOKYO DAIGAKU] At: 10:00 13 January 2009 216 S. NAMIKI ET AL. genetically encoded fluorescent sensors, and the other is to use with membranepermeable chemical dyes, such as acetoxymethyl (AM) ester-conjugated reagents. Many types of genetically encoded probes are shown to work in in vitro and in vivo situations (Bozza, McGann, Mombaerts, & Wachowiak, 2004; Diez-Garcia et al., 2005; Hasan et al., 2004; Reiff et al., 2005), but they require multiple spike bursts to change their fluorescence intensity and cannot detect single action potentials. Nor are they kinetically fast enough to solve temporal accuracy of action potentials. Therefore, synthetic AM dyes are widely used at present. fMCI with AM dye has been applied in many regions of acute brain slices, including neocortex (Mao, Hamzei-Sichani, Aronov, Froemke, & Yuste, 2001; Yuste & Katz, 1991), hippocampus (Canepari, Mammano, Kachalsky, Rahamimoff, & Cherubini, 2000; Crepel et al., 2007; Sasaki, Kimura, Tsukamoto, Matsuki, & Ikegaya, 2006), striatum (Osanai, Yamada, & Yagi, 2006), olfactory bulb (Kapoor & Urban, 2006), and cerebellum (Ghozland, Aguado, Espinosa-Parrilla, Soriano, & Maldonado, 2002; Sullivan, Nimmerjahn, Sarkisov, Helmchen, & Wang, 2005). These authors, however, focused on only one or a few brain regions of interest, and no reports have described the difference in dye loading among brain regions. In our experience, we have vaguely noticed that there is a regional difference between superficial and deep layers of the frontal cortex and between granule cells and pyramidal cells in the hippocampus, as alluded earlier (Ikegaya, Le Bon-Jego, & Yuste, 2005). In the present study, therefore, we systematically examined the efficiency of loading with Oregon Green 488 BAPTA-1AM (OGB-1), one of the most frequently used Ca2+-sensitive dyes in fMCI, in various brain areas under the same loading protocol and the same experimental setup. MATERIALS AND METHODS Materials R NeuroTrace 530/615, OGB-1, and Pluronic F-127 were obtained from Invitrogen (Carlsbad, CA, USA). Cremophor EL was obtained from Sigma (St. Louis, MO, USA). The stock solutions were stored at −20◦ C and diluted immediately before use. Slice Preparations According to the Japanese Pharmacological Society guide for the care and use of laboratory animals, postnatal 14- or 15-day-old mice (SLC, Shizuoka, Japan) Downloaded By: [University of Tokyo/TOKYO DAIGAKU] At: 10:00 13 January 2009 AM-DYE LOADING OF ACUTE BRAIN SLICES 217 were deeply anesthetized with ether and immediately decapitated. The brain was quickly isolated and immersed in ice-cold modified artificial cerebrospinal fluid (ACSF) consisting of (in mM) 27 NaHCO3 , 1.4 NaH2 PO4 , 2.5 KCl, 0.5 Ascorbic acid, 7.0 MgSO4 , 1.0 CaCl2 , and 222.1 sucrose. ACSF was continuously bubbled with 95% O2 and 5% CO2 . Coronal or horizontal slices of 350 or 400 µm in thickness were prepared using a vibratome (Vibratome 3000; Vibratome Company, St. Louis, MO, USA). After dissection, slices were maintained for 30 min at room temperature in ACSF, consisting of (in mM): 127 NaCl, 26 NaHCO3 , 1.5 KCl, 1.24 KH2 PO4 , 1.4 MgSO4 , 2.4 CaCl2 , and 10 glucose. Bulk Loading of OGB-1 OGB-1 was used to visualize Ca2+ signal, because this dye displays relatively good neuron specificity and has a high signal-to-noise ratio (Ikegaya et al., 2005; Takahashi et al., 2007). For bulk loading of OGB-1, slices were transferred into a 35 mm dish filled with 4 ml of ACSF, and 5 µl of dye solution was directly applied to the surface of brain region of interest. The dye solution consisted of 0.07% OGB-1, 1.4% Pluronic F-127, and 0.7% Cremophor EL in DMSO. The slices were incubated for 40 min at 37◦ C in a custom-made incubation chamber (Ikegaya et al., 2005). After being washed, they were maintained in dye-free ACSF at room temperature for at least 30 min. Functional Multineuron Ca2+ Imaging (fMCI) Slices were perfused with physiological ACSF consisting of (in mM): 127 NaCl, 26 NaHCO3 , 3.3 KCl, 1.24 KH2 PO4 , 1.0 MgSO4 , 1.0 CaCl2 , and 10 glucose. This ionic composition is designed to mimic that of in vivo cerebrospinal fluid and known to increase the level of spontaneous network activity (Sanchez-Vives & McCormick, 2000; McNay et al., 2004). After >15 min of perfusion, we began to image spontaneous or evoked Ca2+ signals. Stimulation (50 µs at 100 µA) was given with bipolar tungsten electrodes. Images were captured at 10 or 20 frames/s with Nipkow disk confocal microscope (CSU22; Yokogawa Electric, Tokyo, Japan), cooled CCD camera (iXon DV887DCS-BV; Andor Technology, Belfast, UK), upright microscope (Eclipse FN1; Nikon, Tokyo, Japan), water-immersion objective (16×, 0.80 numerical aperture, CFI75 LWD 16XW; Nikon, Tokyo, Japan), and image acquisition software (SOLIS; Andor Technology, Belfast, UK). Fluorophores were excited at 488 nm with an argon–krypton laser (10–20 mW, 641-YB-A01; Melles Griot, Carlsbad, CA, 218 S. NAMIKI ET AL. Downloaded By: [University of Tokyo/TOKYO DAIGAKU] At: 10:00 13 January 2009 USA) and visualized through a 507 nm long-pass emission filter. For each cell, the fluorescence change was calculated as (Ft –F 0 )/F 0 , where Ft is the fluorescence intensity at any time point, and F 0 is the average baseline across 10 s before and after time t. Spike-triggered Ca2+ signals were semiautomatically detected with custom-written software in Microsoft Visual Basic (Microsoft, Seattle, WA, USA) (Ikegaya et al., 2004). Non-neuronal cells in OGB-1 stained slices were discarded here (Sasaki, Matsuki, & Ikegaya, 2007). Histochemistry To confirm that neurons were labeled with OGB-1, OGB-1-loaded slices were stained with red fluorescent Nissl. After Ca2+ imaging, the slices were fixed with 4% paraformaldehyde in 0.1 M phosphate buffer (pH = 7.3) with 10 mM sucrose for 0.5–1 hr at room temperature and permeabilized with 0.1% Triton X-100 for 30 min. They were incubated with 2% Nissl in 0.1 M phosphate buffer for 30 min. They were imaged with a confocal system (Bio-Rad MRC-1024; Richmond, CA, USA) with a Nikon objective (20×, 0.75 numerical aperture, CFI Plan Apo; Nikon, Tokyo, Japan). Serial optical sections were acquired at 2-µm z-axis intervals to reconstruct three-dimensional images with ImageJ software (NIH, Bethesda, MD, USA). The classification and nomenclature of brain region accords to the atlas of Franklin and Paxinos (1997). Comparing the number of dye-positive cells in OGB-1 and Nissl-labeled slices, we scored the relative staining efficiency, which was rated with the following criteria: (−) if less than 25% of the neurons were stained, (+) if 25%–50% of the neurons were stained, (++) if 50%–75% of the neurons were stained, and (+++) if more than 75% of the neurons were stained. RESULTS We analyzed acute slices prepared from 12 mice. Although neurons labeled with OGB-1 were found in most of brain regions, the staining efficiency varied widely from brain region to brain region. In this paper, we report the average stainability in all slices tested. OGB-1 Staining in Acute Brain Slice Typical examples of OGB-1 staining and posthoc Nissl labeling are shown for six different brain regions, i.e., the dentate gyrus, the thalamus, superficial Downloaded By: [University of Tokyo/TOKYO DAIGAKU] At: 10:00 13 January 2009 AM-DYE LOADING OF ACUTE BRAIN SLICES 219 layers of the perirhinal cortex and entorhinal cortex, and superficial and deep layers of the somatosensory cortex (Figure 1). In these regions, many neurons, which were labeled with the neuron-specific marker Nissl, were stained with OGB-1. Table 1 summarizes the OGB-1-staining efficiency of various brain areas. This regional difference in the staining efficiency was almost consistent across experiments. Brain regions with high staining scores include the dentate gyrus granule cell layer, olfactory bulb granule cell layer, cerebellar granule cell layer, and habenular nucleus. Nondifferentiated neural stem cells in the subventricular zone near the olfactory bulb were also stained. Regions with low staining scores include Ammon’s horn CA1–CA3 pyramidal cell layer, the basolateral amygdala, and the caudate putamen. The CA1–CA3 pyramidal cell layer, except for CA3c, exhibited the worst stainability, and often, no cells were stained. We further examined the subregional difference in the cerebral cortex (Table 2). The same anterior–posterior level in coronal slices was chosen across animals with reference to the anatomical cross sections of the hippocampus, the basolateral amygdala, and the lateral and third ventricles. This position corresponds to figure 44 or 45 in Franklin and Paxinos (1997). The alignment of subcortical regions in a slice was shown in order from the dorsal to ventral axis in Table 2. Almost all layer 1 neurons were stained with OGB-1. This stainability was common across cortical regions. As for other layers, the staining efficiency was moderate. In general, layer 2/3 (superficial layers) neurons were slightly more stained as compared to layer 5/6 (deep layers) neurons, but the absolute stainability differed across subregions. Dorsal parts, such as the retrosplenial granular cortex and the retrosplenial agranular cortex, scored higher than ventral parts, especially the piriform cortex. Functional Multineuron Ca2+ Imaging Is fMCI applicable to various areas in brain slices? Figure 2 shows representative Ca2+ fluorescence traces and raster plots of the onset timings of Ca2+ transients in networks of the olfactory bulb glomerular layer, hippocampal CA3 pyramidal cell layer, deep layers of the entorhinal cortex, and cerebellar granule cell layer. Because many neurons were active even without external stimulation, we mainly monitored the spontaneous activity (supplemental movie 1). The olfactory bulb glomerular layer, which contains three types of juxtaglomerular cells, showed stereotyped synchronization of spontaneous activity (Figure 2(a)). Specifically, the areas that participated in synchronization S. NAMIKI ET AL. Downloaded By: [University of Tokyo/TOKYO DAIGAKU] At: 10:00 13 January 2009 220 Figure 1. Bolus loading of neurons in various brain regions with OGB-1. Confocal images of dentate gyrus (a), thalamus (b), perirhinal cortex (c), entorhinal cortex (d), and somatosensory cortex (e), (f). Left and middle columns show bulk-loaded OGB-1 and posthoc Nissl-Red, respectively, which are merged in right column. Scale bars are 50 µm. AM-DYE LOADING OF ACUTE BRAIN SLICES 221 Table 1. OGB-1-staining efficacy in brain slices from P14-P15 mice Downloaded By: [University of Tokyo/TOKYO DAIGAKU] At: 10:00 13 January 2009 Region Neocortex Superficial layers Deep layers Allocortex Superficial layers Deep layers Olfactory bulb Glomerular layer Mitral cell layer Granule cell layer Hippocampus CA1 CA3 CA3c Dentate gyrus Subiculum Amygdala Basolateral nucleus Centromedial nucleus Cortical nucleus Caudate putamen Thalamus Hypothalamus Habenular nucleus Colliculus Pons Cerebrum Purkinje cell Granule cell layer Stainability ++ ++ ++ + ++ + +++ − − + +++ + − + ++ − ++ ++ +++ ++ ++ + +++ Stainability is—for 0%–25%, + for 25%–50%, ++ for 50%–75%, and +++ for 75%–100%. were segmented and spatially restricted, corresponding to single glomeruli. The hippocampal CA3c pyramidal cell layer was also spontaneously active (Figure 2(b)). They showed roughly synchronized activity, but the synchronization was not spatially segregated or localized, that is, neighboring neurons did not necessarily belong to the same synchronous cell group. The deep layers of the entorhinal cortex, which receive the major afferents from the hippocampus and its related subicular complex, did not show prominent synchronization (Figure 2(c)). In the cerebellar granule cell layer, spontaneously active neurons were 222 S. NAMIKI ET AL. Table 2. OGB-1-staining efficacy in cerebral cortex Downloaded By: [University of Tokyo/TOKYO DAIGAKU] At: 10:00 13 January 2009 Cerebral cortex Retrosplenial granular cortex Retrosplenial agranular cortex Primary motor cortex Secondary motor cortex Primary somatosensory cortex, barrel field Primary somatosensory cortex, trunk reg Secondary somatosensory cortex Ectorhinal cortex Perirhinal cortex Lateral entorhinal cortex Piriform cortex Superficial Deep +++ +++ ++ ++ ++ ++ + ++ ++ ++ + ++ ++ ++ ++ ++ ++ + + + + + Stainability is—for 0%–25%, + for 25%–50%, ++ for 50%–75%, and +++ for 75%–100%. Figure 2. Time-lapse imaging of network activity in various brain regions. Representative somatic Ca2+ signal (top) and raster plots of Ca2+ transient onsets (bottom) of olfactory bulb (a), hippocampus (b), entorhinal cortex (c), and cerebellum (d). Each row in the graph represents a single neuron, and each mark indicates the onset of a single Ca2+ transient. Data indicate spontaneously occurring events, except for (d), in which the molecular layer was extracellularly stimulated at times 15, 30, 42, and 59 s. AM-DYE LOADING OF ACUTE BRAIN SLICES 223 rare (Figure 2(d)). We thus applied extracellular stimuli to the granule cell layer with bipolar electrodes. Several cells responded faithfully to the stimulation. Downloaded By: [University of Tokyo/TOKYO DAIGAKU] At: 10:00 13 January 2009 DISCUSSION In the present study, we provided information about the staining efficiency with OGB-1 in various brain regions. The systematic description is important for the following two reasons. First, if researchers who try to start experiments with fMCI can find the stainability of the network they are interested in, the information could be useful to determine whether or not their research project is feasible. Importantly, although the present study used only OGB-1, the trend of stainability seems to be similar between other Ca2+ indicators, such as fura-2AM and fluo-4AM. With fura-2AM and fluo-4AM as well, the superficial layers in the cerebral cortex score higher stainability than the deep layers, and the dentate gyrus is more stainable than the Ammon’s horn (Ikegaya et al., 2005). Thus, our information can roughly predict the relative staining efficiency with other AM dyes. Second, if the brain region of interest has not been addressed by prior studies, our data are useful to judge whether the fMCI technique is applicable to the network. Several brain regions have already been imaged with fMCI, including the neocortex (Mao et al., 2001; Yuste & Katz, 1991), hippocampus (Canepari et al., 2000; Crepel et al., 2007; Sasaki et al., 2006), olfactory bulb (Kapoor & Urban, 2006), and cerebellum (Ghozland et al., 2002), but our data extend the possibility for the application of fMCI to other regions, including the thalamus, hypothalamus, colliculus, pons, habenular nucleus, and paleocortex. The exact reason for the regional difference in stainability is unclear. We speculate that the staining efficacy changes with the maturity of neurons, with a trend of higher loading probability in younger neurons. During development, dorsomedially located cortices are relatively newly formed, as compared with ventrolaterally located cortices, showing higher staining scores with OGB-1 (Bayer & Altman, 1991). Within the same cortical region, superficial layers contain more recently postmigratory neurons than deeper layers (Bayer & Altman, 1991; Kriegstein, Noctor, & Martinez-Cerdeno, 2006), showing a higher labeling efficiency. The dentate granule cells are developed later than hippocampal pyramidal cells (Altman & Bayer, 1990b), being more easily labeled with OGB-1. This trend, however, does not hold true in all cases. For example, Ammon’s horn is developed later than the paleocortex (Altman & Bayer, 1990a), but hippocampal pyramidal cells are less stained than entorhinal neurons. Downloaded By: [University of Tokyo/TOKYO DAIGAKU] At: 10:00 13 January 2009 224 S. NAMIKI ET AL. Some developmental process, for example, progressive myelination and extracellular matrix formation, may determine the accessibility or permeability of AM probes, resulting in the regional difference in stainability. With this respect, it is suggestive that expression of proteins relevant to the composition of cell membrane such as mannosidase is inversely related to the pattern of OGB-1 staining in the hippocampus (Lein, Zhao, & Gage, 2004). On the other hand, it is intriguing to compare the stainability between AM dyes and voltage-sensitive dyes. The voltage-sensitive dye di-4-ANNEPS easily stains CA1 pyramidal cells (Airan et al., 2007), which are hardly stained with OGB-1AM. Voltage-sensitive dyes are incorporated into the plasma membrane, whereas AM dyes penetrate the membrane. The staining efficiency with Ca2+-sensitive dyes may be explained by their transmembrane permeability or AM-hydrolyzability, rather than accessibility to the membrane surface. We have presented raster plots recorded from four different networks. Although we did not further analyze the structures of the network activity because it is beyond the scope of this paper, it should be noted that fMCI revealed different activity structures in different networks, suggesting that neuronal circuits are designed to display intrinsically defined patterns of spontaneous activity, which may hence be related to specific functions. To our knowledge, there are no reports for large-scale imaging from the olfactory bulb glomerular layer and the deep layers of the entorhinal cortex with single-cell resolution. Specifically, even under in vitro conditions that did not receive any external sensory input, the glomerular layer exhibited nonrandomly organized ongoing activity, that is, a population of juxtaglomerular cells in a single glomerulus constituted a single synchronized cell group. This is consistent with studies with low-resolution recordings, which suggest that the glomeruli display spontaneous activity, the pattern of which is independent of that of adjacent glomeruli (Galan, Weidert, Menzel, Herz, & Galizia, 2006; Karnup, Hayar, Shipley, & Kurnikova, 2006). Single olfactory bulb glomeruli are, therefore, likely to work by themselves as functional units in intrinsic activity as well as odorant-evoked responses. fMCI will provide a powerful tool for investigating the spatiotemporal organization of these networks with single-cell resolution. Supplemental Movie 1. This movie was obtained with the fMCI technique from the olfactory bulb glomerular layer, hippocampal CA3c pyramidal cell layer, and medial entorhinal cortex layer 5/6. Images are trimmed in space and time, and time is compressed 10 times. Spike trains in Figure 2 were reconstructed from this movie. 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