Intra- and Interhemispheric Propagation of Electrophysiological Synchronous Activity and Its Modulation by Serotonin in the Cingulate Cortex of Juvenile Mice

PLoS One. 2016 Mar 1;11(3):e0150092. doi: 10.1371/journal.pone.0150092. eCollection 2016.

Abstract

Disinhibition of the cortex (e.g., by GABA -receptor blockade) generates synchronous and oscillatory electrophysiological activity that propagates along the cortex. We have studied, in brain slices of the cingulate cortex of mice (postnatal age 14-20 days), the propagation along layer 2/3 as well as the interhemispheric propagation through the corpus callosum of synchronous discharges recorded extracellularly and evoked in the presence of 10 μM bicuculline by electrical stimulation of layer 1. The latency of the responses obtained at the same distance from the stimulus electrode was longer in anterior cingulate cortex (ACC: 39.53 ± 2.83 ms, n = 7) than in retrosplenial cortex slices (RSC: 21.99 ± 2.75 ms, n = 5; p<0.05), which is equivalent to a lower propagation velocity in the dorso-ventral direction in ACC than in RSC slices (43.0 mm/s vs 72.9 mm/s). We studied the modulation of this propagation by serotonin. Serotonin significantly increased the latency of the intracortical synchronous discharges (18.9% in the ipsilateral hemisphere and 40.2% in the contralateral hemisphere), and also increased the interhemispheric propagation time by 86.4%. These actions of serotonin were mimicked by the activation of either 5-HT1B or 5-HT2A receptors, but not by the activation of the 5-HT1A subtype. These findings provide further knowledge about the propagation of synchronic electrical activity in the cerebral cortex, including its modulation by serotonin, and suggest the presence of deep differences between the ACC and RSC in the structure of the local cortical microcircuits underlying the propagation of synchronous discharges.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 8-Hydroxy-2-(di-n-propylamino)tetralin / pharmacology
  • Amphetamines / pharmacology
  • Animals
  • Bicuculline / pharmacology
  • Electric Stimulation
  • Electrophysiological Phenomena / drug effects*
  • GABA-A Receptor Antagonists / pharmacology
  • Gyrus Cinguli / drug effects*
  • Gyrus Cinguli / metabolism
  • Gyrus Cinguli / physiology*
  • Male
  • Mice, Inbred C57BL
  • Receptor, Serotonin, 5-HT1B / metabolism
  • Receptor, Serotonin, 5-HT2A / metabolism
  • Serotonin / pharmacology*
  • Serotonin Receptor Agonists / pharmacology
  • Time Factors

Substances

  • Amphetamines
  • GABA-A Receptor Antagonists
  • Receptor, Serotonin, 5-HT1B
  • Receptor, Serotonin, 5-HT2A
  • Serotonin Receptor Agonists
  • Serotonin
  • 8-Hydroxy-2-(di-n-propylamino)tetralin
  • 4-iodo-2,5-dimethoxyphenylisopropylamine
  • Bicuculline

Grants and funding

This work was supported by Generalitat Valenciana (Spain) PROMETEO II program grant 2014/014 and Fundación Navarro-Trípodi (Alicante, Spain) grant 2008. The funders had no role in study design, data collection and analysis, decisión to publish, or preparation of the manuscript.