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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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Recording site-dependence of interhemispheric slow gamma relationship.(a) Depth profile of R/L ratio of slow gamma power. The pyramidal cell layer is the reference point, and positive values of distance indicate directions towards s.l-m. (b) Depth profile of interhemispheric slow gamma coherence. (*P<0.05, **P<0.01 and ***P<0.001 show the statistical significance between ISO versus ENR, respectively (t-test, NISO=8 for depth −200, 10 for depth −100 to 300, 9 for depth −400 and 500; NENR=10 for depth −200 to 200, 9 for depth 400 and 500). Error bars represent s.e.m.
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f5: Recording site-dependence of interhemispheric slow gamma relationship.(a) Depth profile of R/L ratio of slow gamma power. The pyramidal cell layer is the reference point, and positive values of distance indicate directions towards s.l-m. (b) Depth profile of interhemispheric slow gamma coherence. (*P<0.05, **P<0.01 and ***P<0.001 show the statistical significance between ISO versus ENR, respectively (t-test, NISO=8 for depth −200, 10 for depth −100 to 300, 9 for depth −400 and 500; NENR=10 for depth −200 to 200, 9 for depth 400 and 500). Error bars represent s.e.m.

Mentions: As a significant portion of CA1 s.r. innervation originates from the contralateral CA312, we next investigated the bilateral organization of oscillatory activities. To this end, we first calculated the cycle-by-cycle phase difference of the left and right CA1 s.r. gamma oscillations. The phase-difference histograms of slow gamma are plotted for an ISO rat and an ENR rat in Fig. 4a. The distribution for the ENR example has a smaller circular s.d., suggesting a more tightly coupled temporal coordination of bilateral gamma oscillations than ISO. To compute the phase relationship across all frequency ranges, we computed the magnitude squared coherence of bilateral LFPs during theta states for both ISO and ENR rats (Fig. 4b). Previous studies have demonstrated that theta, but not gamma, oscillations are highly coherent across hemispheres13, and our results confirmed this with a high mean interhemispheric CA1 s.r. theta coherence for both ISO and ENR groups (ISO: 0.799±0.022, NISO=10; ENR: 0.824±0.024, NENR=10). As reported, we also found overall lower coherence in the slow gamma band, but it was significantly higher in the ENR group than in the ISO group (0.430±0.0425 versus 0.231±0.0474, respectively, P=0.00583, t-test). In the ISO rats, the interhemispheric coherence was below 0.3 across the slow gamma band, indicating a desynchronized phase relationship between the hemispheres. In contrast, the coherence was prominently elevated in ENR, reaching a peak value of approximately 0.5 at ~36 Hz (Fig. 4b), suggesting that the synaptic inputs to both sides of CA1 are temporally more coordinated in ENR. In both ISO and ENR, the coherence was low in the fast gamma range and beyond. The gamma coherence enhancement for ENR was also seen for s.l-m. recordings, although to a smaller degree than s.r. (Figs 4c and 5b). Chronic treatment with ketamine (ENR+ket) significantly decreased the interhemispheric coherence (0.231±0.0529, P=0.00887, t-test; Fig. 4d). Interestingly, the second harmonic of theta showed a significant higher coherence in ENR (ISO: 0.497±0.0356, ENR: 0.667±0.0269, P=0.0013, t-test, NISO=10, NENR=10; Supplementary Fig. S4b). We also observed the laterally biased increase of gamma power and coherence in the stratum oriens (s.o.) (Fig. 5a), although it should be noted that the power of gamma is visibly smaller than that of s.r. Indeed, the average powers of gamma oscillations at s.o. (−200 μm from the pyramidal cell layer) were 20.3% and 13.9% of those of s.r. (+200 μm) in ISO and ENR, respectively.


Experience enhances gamma oscillations and interhemispheric asymmetry in the hippocampus.

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

Recording site-dependence of interhemispheric slow gamma relationship.(a) Depth profile of R/L ratio of slow gamma power. The pyramidal cell layer is the reference point, and positive values of distance indicate directions towards s.l-m. (b) Depth profile of interhemispheric slow gamma coherence. (*P<0.05, **P<0.01 and ***P<0.001 show the statistical significance between ISO versus ENR, respectively (t-test, NISO=8 for depth −200, 10 for depth −100 to 300, 9 for depth −400 and 500; NENR=10 for depth −200 to 200, 9 for depth 400 and 500). Error bars represent s.e.m.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f5: Recording site-dependence of interhemispheric slow gamma relationship.(a) Depth profile of R/L ratio of slow gamma power. The pyramidal cell layer is the reference point, and positive values of distance indicate directions towards s.l-m. (b) Depth profile of interhemispheric slow gamma coherence. (*P<0.05, **P<0.01 and ***P<0.001 show the statistical significance between ISO versus ENR, respectively (t-test, NISO=8 for depth −200, 10 for depth −100 to 300, 9 for depth −400 and 500; NENR=10 for depth −200 to 200, 9 for depth 400 and 500). Error bars represent s.e.m.
Mentions: As a significant portion of CA1 s.r. innervation originates from the contralateral CA312, we next investigated the bilateral organization of oscillatory activities. To this end, we first calculated the cycle-by-cycle phase difference of the left and right CA1 s.r. gamma oscillations. The phase-difference histograms of slow gamma are plotted for an ISO rat and an ENR rat in Fig. 4a. The distribution for the ENR example has a smaller circular s.d., suggesting a more tightly coupled temporal coordination of bilateral gamma oscillations than ISO. To compute the phase relationship across all frequency ranges, we computed the magnitude squared coherence of bilateral LFPs during theta states for both ISO and ENR rats (Fig. 4b). Previous studies have demonstrated that theta, but not gamma, oscillations are highly coherent across hemispheres13, and our results confirmed this with a high mean interhemispheric CA1 s.r. theta coherence for both ISO and ENR groups (ISO: 0.799±0.022, NISO=10; ENR: 0.824±0.024, NENR=10). As reported, we also found overall lower coherence in the slow gamma band, but it was significantly higher in the ENR group than in the ISO group (0.430±0.0425 versus 0.231±0.0474, respectively, P=0.00583, t-test). In the ISO rats, the interhemispheric coherence was below 0.3 across the slow gamma band, indicating a desynchronized phase relationship between the hemispheres. In contrast, the coherence was prominently elevated in ENR, reaching a peak value of approximately 0.5 at ~36 Hz (Fig. 4b), suggesting that the synaptic inputs to both sides of CA1 are temporally more coordinated in ENR. In both ISO and ENR, the coherence was low in the fast gamma range and beyond. The gamma coherence enhancement for ENR was also seen for s.l-m. recordings, although to a smaller degree than s.r. (Figs 4c and 5b). Chronic treatment with ketamine (ENR+ket) significantly decreased the interhemispheric coherence (0.231±0.0529, P=0.00887, t-test; Fig. 4d). Interestingly, the second harmonic of theta showed a significant higher coherence in ENR (ISO: 0.497±0.0356, ENR: 0.667±0.0269, P=0.0013, t-test, NISO=10, NENR=10; Supplementary Fig. S4b). We also observed the laterally biased increase of gamma power and coherence in the stratum oriens (s.o.) (Fig. 5a), although it should be noted that the power of gamma is visibly smaller than that of s.r. Indeed, the average powers of gamma oscillations at s.o. (−200 μm from the pyramidal cell layer) were 20.3% and 13.9% of those of s.r. (+200 μm) in ISO and ENR, respectively.

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