Integration of sensory quanta in cuneate nucleus neurons in vivo

PLoS One. 2013;8(2):e56630. doi: 10.1371/journal.pone.0056630. Epub 2013 Feb 8.

Abstract

Discriminative touch relies on afferent information carried to the central nervous system by action potentials (spikes) in ensembles of primary afferents bundled in peripheral nerves. These sensory quanta are first processed by the cuneate nucleus before the afferent information is transmitted to brain networks serving specific perceptual and sensorimotor functions. Here we report data on the integration of primary afferent synaptic inputs obtained with in vivo whole cell patch clamp recordings from the neurons of this nucleus. We find that the synaptic integration in individual cuneate neurons is dominated by 4-8 primary afferent inputs with large synaptic weights. In a simulation we show that the arrangement with a low number of primary afferent inputs can maximize transfer over the cuneate nucleus of information encoded in the spatiotemporal patterns of spikes generated when a human fingertip contact objects. Hence, the observed distributions of synaptic weights support high fidelity transfer of signals from ensembles of tactile afferents. Various anatomical estimates suggest that a cuneate neuron may receive hundreds of primary afferents rather than 4-8. Therefore, we discuss the possibility that adaptation of synaptic weight distribution, possibly involving silent synapses, may function to maximize information transfer in somatosensory pathways.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cats
  • Humans
  • Inhibitory Postsynaptic Potentials
  • Intracellular Space / metabolism
  • Medulla Oblongata / cytology*
  • Medulla Oblongata / physiology*
  • Neurons / cytology*
  • Neurons, Afferent / cytology
  • Physical Stimulation
  • Synapses / metabolism
  • Touch Perception / physiology

Grant support

The work was supported by SENSOPAC (an Integrated Project funded by the EU under FP6, IST-028056-SENSOPAC), The Hand Embodied (THE) (an Integrated Project funded by the EU under FP7, project number 248587), the French Medical Research Foundation (project number FDT20090916556), the Swedish Research Council (project number 08291, 08667), a Linné grant (project number 60012701) from the Swedish Research Council, The Knut and Alice Wallenberg Foundation (project number KAW 2004.0119) and the Medical Faculty at Lund University. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.