An abrupt developmental shift in callosal modulation of sleep-related spindle bursts coincides with the emergence of excitatory-inhibitory balance and a reduction of somatosensory cortical plasticity

Amy Jo Marcano-Reik; Tuhina Prasad; Joshua A Weiner; Mark S Blumberg

doi:10.1037/a0020774

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An abrupt developmental shift in callosal modulation of sleep-related spindle bursts coincides with the emergence of excitatory-inhibitory balance and a reduction of somatosensory cortical plasticity

Journal article

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An abrupt developmental shift in callosal modulation of sleep-related spindle bursts coincides with the emergence of excitatory-inhibitory balance and a reduction of somatosensory cortical plasticity

Amy Jo Marcano-Reik, Tuhina Prasad, Joshua A Weiner and Mark S Blumberg

Behavioral neuroscience, Vol.124(5), pp.600-611

10/2010

DOI: 10.1037/a0020774

PMCID: PMC2955326

PMID: 20939660

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https://www.ncbi.nlm.nih.gov/pmc/articles/2955326View

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Abstract

Transecting the corpus callosum of postnatal day (P)1-6 rats disinhibits the production of spindle bursts (SBs) within primary somatosensory cortex (S1), most notably during periods of sleep-related myoclonic twitching. Here we investigated developmental changes in this callosally mediated disinhibition and its association with cortical plasticity. Recordings in P2-15 subjects revealed that callosotomy-induced disinhibition is a transient feature of early development that disappears abruptly after P6. This abrupt switch was accompanied by sharp decreases in myoclonic twitching and equally sharp increases in spontaneous SBs and in the number of GABAergic and glutamatergic presynaptic terminals in S1. Expression of the K+Cl- cotransporter 2 (KCC2) also increased across these ages. To determine whether these developmental changes are associated with alterations in cortical plasticity, pups were callosotomized at P1, P6, or P8, and tested over the subsequent week. Regardless of age, callosotomy immediately disrupted SBs evoked by forepaw stimulation. Over the next week, the P1 and P6 callosotomy groups exhibited full recovery of function; in contrast, the P8 group did not exhibit recovery of function, thus indicating an abrupt decrease in cortical plasticity between P6 and P8. Together, our data demonstrate that callosotomy-induced disinhibition is a transient phenomenon whose disappearance coincides with the onset of increased intrinsic connectivity, establishment of excitatory-inhibitory balance, and diminished plasticity in S1. Accordingly, our findings indicate that callosotomy-induced disinhibition of twitch-related SBs is a bioassay of somatosensory cortical plasticity and, in addition, support the hypothesis that myoclonic twitches, like retinal waves, actively contribute to cortical development and plasticity.

Electroencephalography

Muscimol - pharmacology

Age Factors

Somatosensory Cortex - growth & development

gamma-Aminobutyric Acid - metabolism

Evoked Potentials, Somatosensory - drug effects

Male

Neural Inhibition - physiology

Evoked Potentials, Somatosensory - physiology

Neuronal Plasticity - physiology

Recovery of Function - physiology

Female

Sleep - physiology

Bicuculline - analogs & derivatives

Animals, Newborn

Somatosensory Cortex - drug effects

Rats

Bicuculline - pharmacology

Symporters - metabolism

Animals

Corpus Callosum - physiology

Presynaptic Terminals - metabolism

Corpus Callosum - growth & development

Glutamic Acid - metabolism

Neural Inhibition - drug effects

Somatosensory Cortex - metabolism

Details

Title: Subtitle: An abrupt developmental shift in callosal modulation of sleep-related spindle bursts coincides with the emergence of excitatory-inhibitory balance and a reduction of somatosensory cortical plasticity
Creators: Amy Jo Marcano-Reik - Department of Psychology, University of Iowa, Iowa City, IA 52242, USA
Tuhina Prasad
Joshua A Weiner
Mark S Blumberg
Resource Type: Journal article
Publication Details: Behavioral neuroscience, Vol.124(5), pp.600-611
DOI: 10.1037/a0020774
PMID: 20939660
PMCID: PMC2955326
NLM abbreviation: Behav Neurosci
ISSN: 0735-7044
eISSN: 1939-0084
Publisher: United States
Grant note: MH50701 / NIMH NIH HHS R01 MH050701 / NIMH NIH HHS MH66424 / NIMH NIH HHS K02 MH066424 / NIMH NIH HHS R01 HD063071 / NICHD NIH HHS R29 MH050701 / NIMH NIH HHS
Language: English
Date published: 10/2010
Academic Unit: Liberal Arts and Science Admin; Psychiatry; Psychological and Brain Sciences; Iowa Neuroscience Institute; Biology
Record Identifier: 9983997989002771

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