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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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Experimental design and recordings from bilateral hippocampi.(a) Experimental design. After weaning at 21 days, rats were reared either individually isolated in standard cages (ISO) or housed together in large enriched cages with wheels and toys (ENR). (b) Recording configuration. Simultaneous left and right CA1 in vivo recordings were performed using 16-channel linear silicon probes. (c) Typical recordings of theta-associated gamma oscillations from the entire CA1 area of ISO (upper panel) and ENR (lower panel) rats. Among 16 channels, recordings of 14 channels covering the entire CA1 area (from 200 μm above to 500 μm below pyramidal cell layer; from top traces to the bottom) are shown. Recordings from the pyramidal cell layer are indicated in black triangles. The spacing between channels is 50 μm.
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f1: Experimental design and recordings from bilateral hippocampi.(a) Experimental design. After weaning at 21 days, rats were reared either individually isolated in standard cages (ISO) or housed together in large enriched cages with wheels and toys (ENR). (b) Recording configuration. Simultaneous left and right CA1 in vivo recordings were performed using 16-channel linear silicon probes. (c) Typical recordings of theta-associated gamma oscillations from the entire CA1 area of ISO (upper panel) and ENR (lower panel) rats. Among 16 channels, recordings of 14 channels covering the entire CA1 area (from 200 μm above to 500 μm below pyramidal cell layer; from top traces to the bottom) are shown. Recordings from the pyramidal cell layer are indicated in black triangles. The spacing between channels is 50 μm.

Mentions: Exposing animals to enriched environments with various tactile, spatial and social experiences for 3–4 weeks is known to improve the animals’ ability to perform hippocampus-dependent behavioural tasks56. To study how experience sculpts hippocampal neuronal dynamics, we compared Long-Evans rats reared in isolation in standard cages (ISO) with those reared in groups in enriched environments (ENR) (Fig. 1a). 3.5–4.5 weeks after weaning, rats were anesthetized with urethane (1.6 g kg−1), and 16-channel linear silicon probes were used to record bilaterally in the CA1 region of the hippocampus (Fig. 1b, Supplementary Fig. S1). We employed a level of anesthesia in which theta and non-theta periods alternated spontaneously. We then used an algorithm that automatically extracted theta periods (see methods) and analyzed gamma oscillations during these times. The long-term gamma power was stable during theta episodes (Supplementary Fig. S2), and simply by eye, it was clear that the amplitude of gamma oscillations in the ENR group was larger than that of ISO (Fig. 2a). As slow and fast gamma oscillations in CA1 are generated, respectively, in s.r. and stratum lacunosum moleculare (s.l-m.)78, we analyzed the gamma oscillation changes in the two frequency bands separately (Fig. 2b). For slow gamma power (30–45 Hz), power spectral analysis revealed an average increase of 103% (ISO: 693.9±234.8 μV2, NISO=10; ENR: 1409±434.3 μV2, NENR=10) in the right hemisphere of the ENR rats, and there was a tendency for an increase on the left side as well (51.1% increase, ISO: 757.9±281.7 μV2, ENR 1151±241.4 μV2; Fig. 2c). Two-way analysis of variance (ANOVA) indicated a significant interaction between the environmental effects and the side of the hippocampus on the gamma power (F(1, 18)=8.2000, P=0.0103)). The main effect of the environment or the laterality was less influential than the combined effect (F(1, 18)=2.217, P=0.154; F(1, 18)=3.039, P=0.0984, respectively). For fast gamma (55–90 Hz), the increase in power was smaller (left, ISO: 150.6±29.86 μV2 versus ENR: 170.7±23.66 μV2, 15.4% increase; right, ISO: 138.5±26.26 μV2 versus ENR: 201.6±26.95 μV2, 45.6% increase; F(1,18)=1.327, P=0.264 for the environment; F(1,18)=1.954, P=0.179 for the side), however, once again the ANOVA showed a significant interaction of the environment and hemisphere (F(1, 18)=12.547, P=0.0023), suggesting that the environmental manipulation affects the power of the left and right gamma oscillations differentially.


Experience enhances gamma oscillations and interhemispheric asymmetry in the hippocampus.

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

Experimental design and recordings from bilateral hippocampi.(a) Experimental design. After weaning at 21 days, rats were reared either individually isolated in standard cages (ISO) or housed together in large enriched cages with wheels and toys (ENR). (b) Recording configuration. Simultaneous left and right CA1 in vivo recordings were performed using 16-channel linear silicon probes. (c) Typical recordings of theta-associated gamma oscillations from the entire CA1 area of ISO (upper panel) and ENR (lower panel) rats. Among 16 channels, recordings of 14 channels covering the entire CA1 area (from 200 μm above to 500 μm below pyramidal cell layer; from top traces to the bottom) are shown. Recordings from the pyramidal cell layer are indicated in black triangles. The spacing between channels is 50 μm.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3644069&req=5

f1: Experimental design and recordings from bilateral hippocampi.(a) Experimental design. After weaning at 21 days, rats were reared either individually isolated in standard cages (ISO) or housed together in large enriched cages with wheels and toys (ENR). (b) Recording configuration. Simultaneous left and right CA1 in vivo recordings were performed using 16-channel linear silicon probes. (c) Typical recordings of theta-associated gamma oscillations from the entire CA1 area of ISO (upper panel) and ENR (lower panel) rats. Among 16 channels, recordings of 14 channels covering the entire CA1 area (from 200 μm above to 500 μm below pyramidal cell layer; from top traces to the bottom) are shown. Recordings from the pyramidal cell layer are indicated in black triangles. The spacing between channels is 50 μm.
Mentions: Exposing animals to enriched environments with various tactile, spatial and social experiences for 3–4 weeks is known to improve the animals’ ability to perform hippocampus-dependent behavioural tasks56. To study how experience sculpts hippocampal neuronal dynamics, we compared Long-Evans rats reared in isolation in standard cages (ISO) with those reared in groups in enriched environments (ENR) (Fig. 1a). 3.5–4.5 weeks after weaning, rats were anesthetized with urethane (1.6 g kg−1), and 16-channel linear silicon probes were used to record bilaterally in the CA1 region of the hippocampus (Fig. 1b, Supplementary Fig. S1). We employed a level of anesthesia in which theta and non-theta periods alternated spontaneously. We then used an algorithm that automatically extracted theta periods (see methods) and analyzed gamma oscillations during these times. The long-term gamma power was stable during theta episodes (Supplementary Fig. S2), and simply by eye, it was clear that the amplitude of gamma oscillations in the ENR group was larger than that of ISO (Fig. 2a). As slow and fast gamma oscillations in CA1 are generated, respectively, in s.r. and stratum lacunosum moleculare (s.l-m.)78, we analyzed the gamma oscillation changes in the two frequency bands separately (Fig. 2b). For slow gamma power (30–45 Hz), power spectral analysis revealed an average increase of 103% (ISO: 693.9±234.8 μV2, NISO=10; ENR: 1409±434.3 μV2, NENR=10) in the right hemisphere of the ENR rats, and there was a tendency for an increase on the left side as well (51.1% increase, ISO: 757.9±281.7 μV2, ENR 1151±241.4 μV2; Fig. 2c). Two-way analysis of variance (ANOVA) indicated a significant interaction between the environmental effects and the side of the hippocampus on the gamma power (F(1, 18)=8.2000, P=0.0103)). The main effect of the environment or the laterality was less influential than the combined effect (F(1, 18)=2.217, P=0.154; F(1, 18)=3.039, P=0.0984, respectively). For fast gamma (55–90 Hz), the increase in power was smaller (left, ISO: 150.6±29.86 μV2 versus ENR: 170.7±23.66 μV2, 15.4% increase; right, ISO: 138.5±26.26 μV2 versus ENR: 201.6±26.95 μV2, 45.6% increase; F(1,18)=1.327, P=0.264 for the environment; F(1,18)=1.954, P=0.179 for the side), however, once again the ANOVA showed a significant interaction of the environment and hemisphere (F(1, 18)=12.547, P=0.0023), suggesting that the environmental manipulation affects the power of the left and right gamma oscillations differentially.

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