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Experience enhances gamma oscillations and interhemispheric asymmetry in the hippocampus.

Shinohara Y, Hosoya A, Hirase H - Nat Commun (2013)

Bottom Line: This experience-dependent gamma enhancement is consistently larger in the right hippocampus across subjects, coinciding with a lateralized increase of synaptic density in the right hippocampus.Moreover, interhemispheric coherence in the enriched environment group is significantly elevated at the gamma frequency.These results suggest that enriched rearing sculpts the functional left-right asymmetry of hippocampal circuits by reorganization of synapses.

View Article: PubMed Central - PubMed

Affiliation: Laboratory for Neuron Glia Circuit, RIKEN Brain Science Institute, Wako, Japan. shinohara@brain.riken.jp

ABSTRACT
Gamma oscillations are implicated in higher-order brain functions such as cognition and memory, but how an animal's experience organizes these gamma activities remains elusive. Here we show that the power of hippocampal theta-associated gamma oscillations recorded during urethane anesthesia tends to be greater in rats reared in an enriched environment than those reared in an isolated condition. This experience-dependent gamma enhancement is consistently larger in the right hippocampus across subjects, coinciding with a lateralized increase of synaptic density in the right hippocampus. Moreover, interhemispheric coherence in the enriched environment group is significantly elevated at the gamma frequency. These results suggest that enriched rearing sculpts the functional left-right asymmetry of hippocampal circuits by reorganization of synapses.

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Asymmetrical increase of synapse numbers in CA1 s.r. in ENR.(a) Immunostaining of glutamatergic presynaptic terminals by VGLUT1. Typical images of VGLUT1 immunostaining (upper panel). VGLUT1 was used to label excitatory presynaptic terminals. Each image is a maximum intensity projection of seven consecutive depth images (150 μm interval). Note that VGLUT1 immunoreactivity is more intense in the s.r. of the ENR rat. Scale bar, 10 μm. (b) Bar graphs of the left versus right fluorescence intensity balance for VGLUT1. The mean VGLUT1 fluorescence intensity was more intense in the CA1 s.r. of the ENR rat (*P<0.05, Tukey’s honestly significant difference test, NISO=4, NENR=6 (s.o.); NISO=5, NENR=9 (s.r.); NISO=5, NENR=5 (s.l-m.)). (c) Representative EM images of the left and right CA1 s.r. prepared from ISO and ENR rats. Scale bar, 1.0 μm. Arrowheads indicate the locations of postsynaptic density thickening. (d) Pairwise comparisons of left versus right spine density in CA1 s.r. Three rats were investigated for each rearing condition (**P<0.01, paired t-test, NISO=3, NENR=3). Error bars represent s.e.m.
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f6: Asymmetrical increase of synapse numbers in CA1 s.r. in ENR.(a) Immunostaining of glutamatergic presynaptic terminals by VGLUT1. Typical images of VGLUT1 immunostaining (upper panel). VGLUT1 was used to label excitatory presynaptic terminals. Each image is a maximum intensity projection of seven consecutive depth images (150 μm interval). Note that VGLUT1 immunoreactivity is more intense in the s.r. of the ENR rat. Scale bar, 10 μm. (b) Bar graphs of the left versus right fluorescence intensity balance for VGLUT1. The mean VGLUT1 fluorescence intensity was more intense in the CA1 s.r. of the ENR rat (*P<0.05, Tukey’s honestly significant difference test, NISO=4, NENR=6 (s.o.); NISO=5, NENR=9 (s.r.); NISO=5, NENR=5 (s.l-m.)). (c) Representative EM images of the left and right CA1 s.r. prepared from ISO and ENR rats. Scale bar, 1.0 μm. Arrowheads indicate the locations of postsynaptic density thickening. (d) Pairwise comparisons of left versus right spine density in CA1 s.r. Three rats were investigated for each rearing condition (**P<0.01, paired t-test, NISO=3, NENR=3). Error bars represent s.e.m.

Mentions: To investigate the anatomical correlates of this experience-dependent induction of LFP enhancement, the organization of glutamatergic and GABAergic synapses in CA1 was examined by immunofluorescent labelling in a separate set of rats (Fig. 6a, Supplementary Fig. S7). We used immunofluorescence labelling for vesicular glutamate transporter type 1 (VGLUT1) and vesicular GABA (γ-aminobutyric acid) transporter (VGAT) to label axon terminals of glutamatergic and GABAergic synapses, respectively. Confocal imaging of immunolabelled CA1 s.o. (VGLUT1: NISO=4, NENR=6; VGAT: NISO=3, NENR=4), s.r. (N=5, 9; 6, 8) and s.l-m. (N=5, 5; 6, 6) revealed punctate distributions of VGLUT1 and VGAT. Two-way ANOVA analysis indicated that the R/L balance of mean VGLUT1 fluorescence intensity is higher in ENR (F(1, 28)=7.24, P=0.0119; Fig. 6b) and is dependent on the anatomical location (F(2, 28)=4.51, P=0.02). Moreover, a significant degree of interaction between rearing condition and anatomical location was revealed (F(2, 28)=3.55, P=0.0423). The R/L balance of fluorescence intensity was also examined for VGAT signals and housing environment, and a weaker but significant interaction was detected (F(1, 27)=4.51, P=0.0429; Supplementary Fig. S7b). The two-way ANOVA analysis suggests that rearing condition is a significant factor that influences the R/L balance of VGAT-positive terminals (F(1, 27)=4.51, P=0.0249). Furthermore, using confocal microscopy, we counted the fluorescent puncta in respective images. The R/L balances of puncta were similar to those of fluorescence intensity for VGLUT1 and VGAT (Supplementary Fig. S7c). Next, we examined the CA1 s.r. spine synapse density by electron microscopy (Fig. 6c). In ISO rats, the average spine densities of the left and the right s.r. were 1.30±0.07 and 1.31±0.07 spines per μm3, respectively (Fig. 6d). However, in ENR rats, the spine density of the right was approximately twice of the left (0.831±0.0824 versus 1.96±0.0959, spines per μm3; paired t-test, P=0.00998). Despite these differences in spine density, the distribution of postsynaptic density areas could not be distinguished by either laterality or rearing condition (Supplementary Fig. S8).


Experience enhances gamma oscillations and interhemispheric asymmetry in the hippocampus.

Shinohara Y, Hosoya A, Hirase H - Nat Commun (2013)

Asymmetrical increase of synapse numbers in CA1 s.r. in ENR.(a) Immunostaining of glutamatergic presynaptic terminals by VGLUT1. Typical images of VGLUT1 immunostaining (upper panel). VGLUT1 was used to label excitatory presynaptic terminals. Each image is a maximum intensity projection of seven consecutive depth images (150 μm interval). Note that VGLUT1 immunoreactivity is more intense in the s.r. of the ENR rat. Scale bar, 10 μm. (b) Bar graphs of the left versus right fluorescence intensity balance for VGLUT1. The mean VGLUT1 fluorescence intensity was more intense in the CA1 s.r. of the ENR rat (*P<0.05, Tukey’s honestly significant difference test, NISO=4, NENR=6 (s.o.); NISO=5, NENR=9 (s.r.); NISO=5, NENR=5 (s.l-m.)). (c) Representative EM images of the left and right CA1 s.r. prepared from ISO and ENR rats. Scale bar, 1.0 μm. Arrowheads indicate the locations of postsynaptic density thickening. (d) Pairwise comparisons of left versus right spine density in CA1 s.r. Three rats were investigated for each rearing condition (**P<0.01, paired t-test, NISO=3, NENR=3). Error bars represent s.e.m.
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f6: Asymmetrical increase of synapse numbers in CA1 s.r. in ENR.(a) Immunostaining of glutamatergic presynaptic terminals by VGLUT1. Typical images of VGLUT1 immunostaining (upper panel). VGLUT1 was used to label excitatory presynaptic terminals. Each image is a maximum intensity projection of seven consecutive depth images (150 μm interval). Note that VGLUT1 immunoreactivity is more intense in the s.r. of the ENR rat. Scale bar, 10 μm. (b) Bar graphs of the left versus right fluorescence intensity balance for VGLUT1. The mean VGLUT1 fluorescence intensity was more intense in the CA1 s.r. of the ENR rat (*P<0.05, Tukey’s honestly significant difference test, NISO=4, NENR=6 (s.o.); NISO=5, NENR=9 (s.r.); NISO=5, NENR=5 (s.l-m.)). (c) Representative EM images of the left and right CA1 s.r. prepared from ISO and ENR rats. Scale bar, 1.0 μm. Arrowheads indicate the locations of postsynaptic density thickening. (d) Pairwise comparisons of left versus right spine density in CA1 s.r. Three rats were investigated for each rearing condition (**P<0.01, paired t-test, NISO=3, NENR=3). Error bars represent s.e.m.
Mentions: To investigate the anatomical correlates of this experience-dependent induction of LFP enhancement, the organization of glutamatergic and GABAergic synapses in CA1 was examined by immunofluorescent labelling in a separate set of rats (Fig. 6a, Supplementary Fig. S7). We used immunofluorescence labelling for vesicular glutamate transporter type 1 (VGLUT1) and vesicular GABA (γ-aminobutyric acid) transporter (VGAT) to label axon terminals of glutamatergic and GABAergic synapses, respectively. Confocal imaging of immunolabelled CA1 s.o. (VGLUT1: NISO=4, NENR=6; VGAT: NISO=3, NENR=4), s.r. (N=5, 9; 6, 8) and s.l-m. (N=5, 5; 6, 6) revealed punctate distributions of VGLUT1 and VGAT. Two-way ANOVA analysis indicated that the R/L balance of mean VGLUT1 fluorescence intensity is higher in ENR (F(1, 28)=7.24, P=0.0119; Fig. 6b) and is dependent on the anatomical location (F(2, 28)=4.51, P=0.02). Moreover, a significant degree of interaction between rearing condition and anatomical location was revealed (F(2, 28)=3.55, P=0.0423). The R/L balance of fluorescence intensity was also examined for VGAT signals and housing environment, and a weaker but significant interaction was detected (F(1, 27)=4.51, P=0.0429; Supplementary Fig. S7b). The two-way ANOVA analysis suggests that rearing condition is a significant factor that influences the R/L balance of VGAT-positive terminals (F(1, 27)=4.51, P=0.0249). Furthermore, using confocal microscopy, we counted the fluorescent puncta in respective images. The R/L balances of puncta were similar to those of fluorescence intensity for VGLUT1 and VGAT (Supplementary Fig. S7c). Next, we examined the CA1 s.r. spine synapse density by electron microscopy (Fig. 6c). In ISO rats, the average spine densities of the left and the right s.r. were 1.30±0.07 and 1.31±0.07 spines per μm3, respectively (Fig. 6d). However, in ENR rats, the spine density of the right was approximately twice of the left (0.831±0.0824 versus 1.96±0.0959, spines per μm3; paired t-test, P=0.00998). Despite these differences in spine density, the distribution of postsynaptic density areas could not be distinguished by either laterality or rearing condition (Supplementary Fig. S8).

Bottom Line: This experience-dependent gamma enhancement is consistently larger in the right hippocampus across subjects, coinciding with a lateralized increase of synaptic density in the right hippocampus.Moreover, interhemispheric coherence in the enriched environment group is significantly elevated at the gamma frequency.These results suggest that enriched rearing sculpts the functional left-right asymmetry of hippocampal circuits by reorganization of synapses.

View Article: PubMed Central - PubMed

Affiliation: Laboratory for Neuron Glia Circuit, RIKEN Brain Science Institute, Wako, Japan. shinohara@brain.riken.jp

ABSTRACT
Gamma oscillations are implicated in higher-order brain functions such as cognition and memory, but how an animal's experience organizes these gamma activities remains elusive. Here we show that the power of hippocampal theta-associated gamma oscillations recorded during urethane anesthesia tends to be greater in rats reared in an enriched environment than those reared in an isolated condition. This experience-dependent gamma enhancement is consistently larger in the right hippocampus across subjects, coinciding with a lateralized increase of synaptic density in the right hippocampus. Moreover, interhemispheric coherence in the enriched environment group is significantly elevated at the gamma frequency. These results suggest that enriched rearing sculpts the functional left-right asymmetry of hippocampal circuits by reorganization of synapses.

Show MeSH
Related in: MedlinePlus