Increase of neuronal response variability at higher processing levels as revealed by simultaneous recordings

J Neurophysiol. 2005 Jun;93(6):3548-59. doi: 10.1152/jn.01288.2004. Epub 2005 Feb 16.

Abstract

A key problem for neuronal information processing is the variability of spike trains, something that is likely to constrain the encoding of sensory signals. We measured interspike-interval variability (coefficient of variation) as well as spike-count variability (Fano factor) in the metathoracic auditory system of locusts. We performed simultaneous intracellular recordings at the first three processing levels to establish identical physiological conditions. This allows us to assess whether variability is generated anew or is reduced during synaptic transmission and processing. Both the interspike-interval variability as well as the spike-count variability revealed similar trends and showed an increase from the periphery to higher processing levels. This result was confirmed by single-cell recordings. A comparison of ascending interneurons coding for sound direction and those encoding sound patterns showed that the latter respond more reliably to repeated stimulus presentations. In general, the variability of spiking responses was much lower than expected from a Poisson process. Furthermore, we observed a strong dependence of variability on the spike rate, which differed at the three levels investigated. The differences in spike rates account for most of the differences in variability observed between processing levels. For auditory receptors, we found a good agreement between the Fano factor and the squared coefficient of variation, suggesting similarities to a renewal process of spike generation at the periphery. At the level of interneurons, the Fano factor was lower than the squared coefficient of variation; this indicates a higher reliability than expected from the interspike-interval distribution.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acoustic Stimulation / methods
  • Action Potentials / physiology*
  • Animals
  • Auditory Pathways / physiology*
  • Brain / cytology*
  • Dose-Response Relationship, Radiation
  • Female
  • Grasshoppers
  • Male
  • Models, Neurological
  • Neural Inhibition / physiology
  • Neurons / classification
  • Neurons / physiology*
  • Reaction Time / physiology
  • Sound Localization / physiology
  • Time Factors