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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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Related in: MedlinePlus

Chronic effects of the NMDAR inhibitor ketamine on the theta state power spectrum.(a) Experimental design and CA1 s.r. theta LFP recordings. After weaning at postnatal day 21, rats were reared in ENR for 3 days to learn to drink from water bottles. Thereafter, the water was supplemented with ketamine (0.1% w/v) until the day of the recording (upper panel). Typical recording of bilateral theta-associated gamma oscillations from the CA1 s.r. of an ENR+ketamine (ENR+ket) rat. Left (L) and right (R) paired traces are wideband and slow gamma-filtered recordings, respectively (lower panel). (b) PSDs of the left and right CA1 s.r. theta state LFPs in ENR and ENR+ket conditions. The averaged PSDs were plotted as in Fig. 2b. (c) Mean R/L power ratios of theta (left panel), slow gamma (middle panel) and fast gamma (right panel) in CA1 s.r. of ENR and ENR+ket rats. The slow and fast gamma power ratios of ENR+ket were significantly lower than 1 (*P<0.05 and **P<0.01, respectively, t-test, NENR=10, NENR+ket=8). The ENR and ENR+ket power ratios were significantly different (***P<0.001, t-test, NENR=10, NENR+ket=8). Acute effect (within 90 min) of intramuscular ketamine administration (3.0 mg kg−1, ENR+a-ket, NENR+a-ket=4) on slow and fast gamma power is also shown in black in the middle and the right panel. ENR+a-ket did not show the inhibitory effects seen in ENR+ket. Error bars represent s.e.m.
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f3: Chronic effects of the NMDAR inhibitor ketamine on the theta state power spectrum.(a) Experimental design and CA1 s.r. theta LFP recordings. After weaning at postnatal day 21, rats were reared in ENR for 3 days to learn to drink from water bottles. Thereafter, the water was supplemented with ketamine (0.1% w/v) until the day of the recording (upper panel). Typical recording of bilateral theta-associated gamma oscillations from the CA1 s.r. of an ENR+ketamine (ENR+ket) rat. Left (L) and right (R) paired traces are wideband and slow gamma-filtered recordings, respectively (lower panel). (b) PSDs of the left and right CA1 s.r. theta state LFPs in ENR and ENR+ket conditions. The averaged PSDs were plotted as in Fig. 2b. (c) Mean R/L power ratios of theta (left panel), slow gamma (middle panel) and fast gamma (right panel) in CA1 s.r. of ENR and ENR+ket rats. The slow and fast gamma power ratios of ENR+ket were significantly lower than 1 (*P<0.05 and **P<0.01, respectively, t-test, NENR=10, NENR+ket=8). The ENR and ENR+ket power ratios were significantly different (***P<0.001, t-test, NENR=10, NENR+ket=8). Acute effect (within 90 min) of intramuscular ketamine administration (3.0 mg kg−1, ENR+a-ket, NENR+a-ket=4) on slow and fast gamma power is also shown in black in the middle and the right panel. ENR+a-ket did not show the inhibitory effects seen in ENR+ket. Error bars represent s.e.m.

Mentions: As NMDAR activation is involved in many forms of CA3-CA1 synaptic plasticity both in vitro and in vivo, we addressed if NMDAR activation is involved in the experience-dependent enhancement of gamma oscillations by administering the NMDAR antagonist ketamine11. Rats were reared in ENR for 3–4 weeks, with ketamine included in the drinking water (0.1% w/v, supplemented with 0.5% w/v sucrose; ENR+ket). The ENR+ket rats did not show any apparent behavioural abnormalities (Supplementary Fig. S6). Ketamine administration and laterality showed a significant degree of interaction (two-way ANOVA, F(1, 16)=6.88, P=0.0185). Moreover, the slow gamma power of ENR+ket group was significantly smaller than that of ENR group in both sides (left: P=0.0425, right: P=0.0218, Shaffer’s method, NENR=10, NENR+ket=8; Fig. 3a). The fast gamma, too, showed a significant interaction of ketamine and laterality (F(1, 16)=11.8, P=0.0034). We observed no difference in the (R/L)θ between ENR+ket and ENR (P=0.734, t-test). In contrast, (R/L)γs in the ketamine-treated rats was significantly lower than ENR rats (P=0.000455, t-test), and surprisingly shifted below 1 (0.873±0.0528), indicating a left dominance of slow gamma oscillations (P=0.0472, t-test). Similarly, (R/L)γf for ENR+ket was 0.771±0.0428 (P=0.0011, t-test) and significantly different from ENR (P=0.000010, t-test; Fig. 3c). Acute administration of ketamine (intramuscular injection, 3.0 mg kg−1) just before recording in enriched environment-reared rats (ENR+a-ket) did not show the effects of chronic ketamine administration (R/Lγs=1.22±0.041, P=0.750, ENR versus ENR+a-ket; R/Lγf=1.05±0.044, P=0.137, ENR versus ENR+a-ket, t-test, NENR+a-ket=4; Fig. 3c).


Experience enhances gamma oscillations and interhemispheric asymmetry in the hippocampus.

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

Chronic effects of the NMDAR inhibitor ketamine on the theta state power spectrum.(a) Experimental design and CA1 s.r. theta LFP recordings. After weaning at postnatal day 21, rats were reared in ENR for 3 days to learn to drink from water bottles. Thereafter, the water was supplemented with ketamine (0.1% w/v) until the day of the recording (upper panel). Typical recording of bilateral theta-associated gamma oscillations from the CA1 s.r. of an ENR+ketamine (ENR+ket) rat. Left (L) and right (R) paired traces are wideband and slow gamma-filtered recordings, respectively (lower panel). (b) PSDs of the left and right CA1 s.r. theta state LFPs in ENR and ENR+ket conditions. The averaged PSDs were plotted as in Fig. 2b. (c) Mean R/L power ratios of theta (left panel), slow gamma (middle panel) and fast gamma (right panel) in CA1 s.r. of ENR and ENR+ket rats. The slow and fast gamma power ratios of ENR+ket were significantly lower than 1 (*P<0.05 and **P<0.01, respectively, t-test, NENR=10, NENR+ket=8). The ENR and ENR+ket power ratios were significantly different (***P<0.001, t-test, NENR=10, NENR+ket=8). Acute effect (within 90 min) of intramuscular ketamine administration (3.0 mg kg−1, ENR+a-ket, NENR+a-ket=4) on slow and fast gamma power is also shown in black in the middle and the right panel. ENR+a-ket did not show the inhibitory effects seen in ENR+ket. Error bars represent s.e.m.
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Related In: Results  -  Collection

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

f3: Chronic effects of the NMDAR inhibitor ketamine on the theta state power spectrum.(a) Experimental design and CA1 s.r. theta LFP recordings. After weaning at postnatal day 21, rats were reared in ENR for 3 days to learn to drink from water bottles. Thereafter, the water was supplemented with ketamine (0.1% w/v) until the day of the recording (upper panel). Typical recording of bilateral theta-associated gamma oscillations from the CA1 s.r. of an ENR+ketamine (ENR+ket) rat. Left (L) and right (R) paired traces are wideband and slow gamma-filtered recordings, respectively (lower panel). (b) PSDs of the left and right CA1 s.r. theta state LFPs in ENR and ENR+ket conditions. The averaged PSDs were plotted as in Fig. 2b. (c) Mean R/L power ratios of theta (left panel), slow gamma (middle panel) and fast gamma (right panel) in CA1 s.r. of ENR and ENR+ket rats. The slow and fast gamma power ratios of ENR+ket were significantly lower than 1 (*P<0.05 and **P<0.01, respectively, t-test, NENR=10, NENR+ket=8). The ENR and ENR+ket power ratios were significantly different (***P<0.001, t-test, NENR=10, NENR+ket=8). Acute effect (within 90 min) of intramuscular ketamine administration (3.0 mg kg−1, ENR+a-ket, NENR+a-ket=4) on slow and fast gamma power is also shown in black in the middle and the right panel. ENR+a-ket did not show the inhibitory effects seen in ENR+ket. Error bars represent s.e.m.
Mentions: As NMDAR activation is involved in many forms of CA3-CA1 synaptic plasticity both in vitro and in vivo, we addressed if NMDAR activation is involved in the experience-dependent enhancement of gamma oscillations by administering the NMDAR antagonist ketamine11. Rats were reared in ENR for 3–4 weeks, with ketamine included in the drinking water (0.1% w/v, supplemented with 0.5% w/v sucrose; ENR+ket). The ENR+ket rats did not show any apparent behavioural abnormalities (Supplementary Fig. S6). Ketamine administration and laterality showed a significant degree of interaction (two-way ANOVA, F(1, 16)=6.88, P=0.0185). Moreover, the slow gamma power of ENR+ket group was significantly smaller than that of ENR group in both sides (left: P=0.0425, right: P=0.0218, Shaffer’s method, NENR=10, NENR+ket=8; Fig. 3a). The fast gamma, too, showed a significant interaction of ketamine and laterality (F(1, 16)=11.8, P=0.0034). We observed no difference in the (R/L)θ between ENR+ket and ENR (P=0.734, t-test). In contrast, (R/L)γs in the ketamine-treated rats was significantly lower than ENR rats (P=0.000455, t-test), and surprisingly shifted below 1 (0.873±0.0528), indicating a left dominance of slow gamma oscillations (P=0.0472, t-test). Similarly, (R/L)γf for ENR+ket was 0.771±0.0428 (P=0.0011, t-test) and significantly different from ENR (P=0.000010, t-test; Fig. 3c). Acute administration of ketamine (intramuscular injection, 3.0 mg kg−1) just before recording in enriched environment-reared rats (ENR+a-ket) did not show the effects of chronic ketamine administration (R/Lγs=1.22±0.041, P=0.750, ENR versus ENR+a-ket; R/Lγf=1.05±0.044, P=0.137, ENR versus ENR+a-ket, t-test, NENR+a-ket=4; Fig. 3c).

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