Download regional difference in stainability with calcium

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
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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]
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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
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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)
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AM-DYE LOADING OF ACUTE BRAIN SLICES
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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,
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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
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AM-DYE LOADING OF ACUTE BRAIN SLICES
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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.
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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
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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
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Table 2. OGB-1-staining efficacy in cerebral cortex
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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.
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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.
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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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