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Ponto-geniculo-occipital-wave suppression amplifies lateral geniculate nucleus cell-size changes in monocularly
J P Shaffery1, H P Roffwarg, S G Speciale
1Department of Psychiatry and Human Behavior, Division of Neurobiology and Behavior Research, University of Mississippi Medical Center, 2500 N. State Street, Jackson, MS 39216-4505, USA.
Insights
Eliminating ponto-geniculo-occipital (PGO)-wave activity during REM sleep amplifies visual plasticity in the lateral geniculate nucleus (LGN). This highlights REM sleep
Area of Science:
- Neuroscience
- Developmental Biology
- Sleep Science
Background:
- The critical period for visual system development in cats is sensitive to visual input and sleep states.
- Previous studies showed that REM sleep deprivation amplifies monocular deprivation effects on LGN cell size.
Purpose of the Study:
- To investigate if eliminating PGO-wave activity, specifically, during REM sleep enhances visual plasticity in the LGN.
- To compare the effects of PGO-wave suppression with general REM sleep deprivation.
Main Methods:
- Bilateral pontomesencephalic lesions were used to eliminate PGO-wave activity in the LGN of kittens.
- Lesions were performed at post-natal day 42, coinciding with the start of monocular deprivation.
- Sleep-wake proportions and REM sleep tonic activities were preserved post-lesion.
Main Results:
- PGO-wave suppressed animals showed increased LGN interlaminar cell-size disparity, similar to REM sleep-deprived animals.
- Smaller A1/A-interlaminar ratios indicated enhanced plasticity in both PGO-wave suppressed and REM sleep-deprived groups compared to monocular deprivation alone.
- While cell-size changes differed, both methods enhanced LGN cell plasticity.
Conclusions:
- Selective elimination of REM sleep phasic activity (PGO-waves) at the LGN enhances visual plasticity during development.
- The REM sleep state may play a role in limiting plasticity and variability during central nervous system maturation.
- Altered visual input evokes greater LGN cell plasticity when combined with REM sleep modulation.
Abstract:
We have previously shown that during the post-natal critical period of development of the cat visual system, 1 week of instrumental rapid eye movement (REM) sleep deprivation (IRSD) during 2 weeks of monocular deprivation (MD) results in significant amplification of the effects of solely the 2-week MD on cell-size in the binocular segment of the lateral geniculate nucleus (LGN) [36,40]. In this study, we examined whether elimination of ponto-geniculo-occipital (PGO)-wave phasic activity in the LGN during REM sleep (REMS), rather than suppression of all REMS state-related activity, would similarly yield enhanced plasticity effects on cell-size in LGN. PGO-activity was eliminated in LGN by bilateral pontomesencephalic lesions [8,32]. This method of removing phasic activation at the level of the LGN preserved sleep and wake proportions as well as the tonic activities (low voltage, fast frequency ECoG and low amplitude EMG) that characterize REM sleep. The lesions were performed in kittens on post-natal day 42, at the end of the first week of the 2-week period of MD, the same age when IRSD was started in the earlier study. LGN interlaminar cell-size disparity increased in the PGO-wave-suppressed animals as it had in behaviorally REM sleep-deprived animals. Smaller A1/A-interlaminar ratios reflect the increased disparity effect in both the REM sleep- and PGO-suppressed groups compared to animals subjected to MD-alone. With IRSD, the effect was achieved because the occluded eye-related, LGN A1-lamina cells tended to be smaller relative to their size after MD-alone, whereas after PGO-suppressing lesions, the A1-lamina cells retained their size and the non-occluded eye-related, A-lamina cells tended to be larger than after MD-alone. Despite this difference, for which several possible explanations are offered, these A1/A-interlaminar ratio data indicate that in conjunction either with suppression of the whole of the REMS state or selective removal of REM sleep phasic activity at the LGN, altered visual input evokes more LGN cell plasticity during the developmental period than it would otherwise. These data further support involvement of the REM sleep state in reducing susceptibility to plasticity changes and undesirable variability in the course of normative CNS growth and maturation.