Three-dimensional distribution of sensory stimulation-evoked neuronal activity of spinal dorsal horn neurons analyzed by in vivo calcium imaging

PLoS One. 2014 Aug 6;9(8):e103321. doi: 10.1371/journal.pone.0103321. eCollection 2014.

Abstract

The spinal dorsal horn comprises heterogeneous populations of interneurons and projection neurons, which form neuronal circuits crucial for processing of primary sensory information. Although electrophysiological analyses have uncovered sensory stimulation-evoked neuronal activity of various spinal dorsal horn neurons, monitoring these activities from large ensembles of neurons is needed to obtain a comprehensive view of the spinal dorsal horn circuitry. In the present study, we established in vivo calcium imaging of multiple spinal dorsal horn neurons by using a two-photon microscope and extracted three-dimensional neuronal activity maps of these neurons in response to cutaneous sensory stimulation. For calcium imaging, a fluorescence resonance energy transfer (FRET)-based calcium indicator protein, Yellow Cameleon, which is insensitive to motion artifacts of living animals was introduced into spinal dorsal horn neurons by in utero electroporation. In vivo calcium imaging following pinch, brush, and heat stimulation suggests that laminar distribution of sensory stimulation-evoked neuronal activity in the spinal dorsal horn largely corresponds to that of primary afferent inputs. In addition, cutaneous pinch stimulation elicited activities of neurons in the spinal cord at least until 2 spinal segments away from the central projection field of primary sensory neurons responsible for the stimulated skin point. These results provide a clue to understand neuronal processing of sensory information in the spinal dorsal horn.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Calcium / metabolism*
  • Calcium Signaling / physiology*
  • Evoked Potentials / physiology*
  • Female
  • Fluorescence Resonance Energy Transfer
  • Mice
  • Mice, Inbred ICR
  • Microscopy, Confocal
  • Posterior Horn Cells / cytology*
  • Posterior Horn Cells / metabolism*

Substances

  • Calcium

Grants and funding

This work was supported by Grants-in-Aid for Scientific Research (http://www.jsps.go.jp/english/e-grants/index.html) from the Japanese Ministry of Education, Culture, Sports, Science and Technology, to KN (#24590736), SM (#24590735), and SI (#23659322). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.