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.1996 Jul 15;16(14):4411-9.
doi: 10.1523/JNEUROSCI.16-14-04411.1996.

Upregulation of BDNF mRNA expression in the barrel cortex of adult mice after sensory stimulation

Affiliations

Upregulation of BDNF mRNA expression in the barrel cortex of adult mice after sensory stimulation

N Rocamora et al. J Neurosci..

Abstract

Upregulation of brain-derived neurotrophic factor (BDNF) mRNA expression by neuronal activity has been reported in cultured hippocampal cells and in different in vivo excitotoxic paradigms. The aim of the present study was to determine whether sensory stimulation of the whisker-to-barrel pathway alters BDNF mRNA expression in the cortex and, if so, to evaluate the specificity of this effect. To this end, a set of mystacial whiskers was unilaterally stimulated by mechanical deflection, and the expression of BDNF mRNA was analyzed in the barrel cortex by in situ hybridization (ISH) using a 35S-labeled antisense BDNF riboprobe and emulsion autoradiography. A clear-cut and specific upregulation of the BDNF mRNA expression was found at the level of the somatosensory cortex after the increased peripheral stimulation. In the barrel cortex of control mice, BDNF mRNA was present in a few cells in layers II/III and VI, whereas it was almost undetectable in layer IV. After 6 hr of whisker stimulation, increased levels of BDNF mRNA were found in layers II to VI of the contralateral barrel cortex. In layer IV, BDNF upregulation was confined to the barrels corresponding to the stimulated follicles. ISH combined with immunocytochemistry against the three calcium-binding proteins parvalbumin, calretinin, and calbindin-D28K revealed that BDNF mRNA-expressing cells do not belong to the GABAergic cell population of the barrel cortex. The present results support a role for BDNF in activity-dependent modifications of the adult cerebral cortex.

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Figures

Fig. 1.
Fig. 1.
BDNF mRNA expression in the barrel cortex after unilateral stimulation of the contralateral whiskerpad. Whiskers B1–3 and C1–3 were unilaterally stimulated for different time periods, and BDNF mRNA expression was analyzed on coronal sections through the contralateral barrel cortex.A,C, andD are dark-field photomicrographs of control (A) and stimulated barrel cortex for different time periods: 6 hr (C) and 24 hr (D).B is a bright-field photomicrograph of the Nissl-stained section shown inC. Roman numbers I, II/III, IV, and V/VI inB andDindicate layers in the barrel cortex. Note higher BDNF mRNA levels inC (6 hr stimulation) than inD (24 hr stimulation).E andF are higher-magnification bright-field photomicrographs showing BDNF mRNA hybridization signal (black silver grains) in layer IV of control (E) and 6 hr stimulated (F) barrel cortices.ArrowsinF indicate a wall of a barrel. Note the clear upregulation of BDNF mRNA expression in cells inF compared withE. Scale bar (shown inB) is 150 μm and pertains toA–D; scale bar (shown inE) is 25 μm and pertains also toF.
Fig. 2.
Fig. 2.
Quantification of the BDNF mRNA hybridization signal through the different layers of the barrel cortex. BDNF mRNA levels were measured in a cortical column 250 μm wide. Levels in contralateral (stimulated) and ipsilateral (control) barrel cortex are compared. InA, results are expressed as the mean of the medians of the number of cells expressing BDNF mRNA (with ≥10 silver grains over soma) in the different cortical layers (II/III, IV, and V/VI) of ipsilateral and contralateral barrel cortices ± the SD.Numbers represent the averaged levels of four different animals in which whiskers B1–3 and C1–3 were stimulated for a period of 6 hr.Asterisks denote statistically significant differences between contralateral and ipsilateral barrel cortex by the ANOVA test (*p ≤ 0.05, **p ≤ 0.001). InB, not only the number of labeled cells but also the levels of BDNF mRNA hybridization signal (BDNF mRNA-expressing cells were classified as cells with 10–19, 20–29, 30–39, and ≥40 grains/cell) were represented in the different cortical layers for a 6 hr stimulated animal.
Fig. 3.
Fig. 3.
One-to-one relationship between the stimulated whiskers and the corresponding contralateral, stimulated barrels.A andB are dark-field photomicrographs showing BDNF mRNA hybridization signal in tangential sections through stimulated barrel cortices of 6 hr stimulated animals. InA, several whiskers (C2, C3, and B3) were stimulated; inB, only one whisker (C2) was stimulated.C andDshow the Nissl-stained sections ofA andB, respectively.Arrowheads inA–D indicate blood vessels in the tissue to show correspondence between dark- and bright-field photomicrographs. Note that stimulation of whiskers results in BDNF mRNA upregulation that is restricted to the stimulated barrels. Scale bar (shown inD), 200 μm.
Fig. 4.
Fig. 4.
BDNF mRNA is not expressed in GABAergic cells of the barrel cortex. Bright-field photomicrographs of double-processed tissue: ISH for BDNF and immunocytochemistry (ICC) for each of the three different calcium-binding proteins parvalbumin (A), calretinin (B), and calbindin (C). InB, calretinin-immunoreacted section was also Nissl-stained. Note that the ISH result could not be seen inA–C because of the low magnification.D andE are higher-magnification views of coronal sections showing the combined ISH–ICC in the stimulated barrel cortex at layer IV level. InD, ICC was against CALB, and inE against PARV. Note that the BDNF mRNA hybridization signal is not present in PARV-immunoreactive cells (arrowheads inE), and that itis present in weak but not in heavy calbindin-immunoreactive neurons (D).F is a camera lucida drawing of a stimulated barrel C3 from a tangential section hybridized with BDNF and immunoreacted against PARV;bv is a blood vessel.Hatched area represents the wall of the barrel, where the density of cells made it difficult to individualize them; thus, only cells with a very high level of labeling were indicated as BDNF-expressing cells.Symbols inF indicate various classes of cells (see key to theleft) formed by those that are positive for BDNF mRNA, or not, in combination with being immunoreactive for parvalbumin, or not. Note that there are no PARV+/BDNF+ cells. Scale bar (shown inB) is 150 μm and pertains toA–C; scale bar (shown inD) is 25 μm and also pertains toE.
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