Receptive field scatter, topography and map variability in different layers of the hindpaw representation of rat somatosensory cortex

Exp Brain Res. 2004 Apr;155(4):485-99. doi: 10.1007/s00221-003-1755-3. Epub 2004 Jan 27.

Abstract

We recorded neurons extracellularly in layers II/III, IV, and V of the hindpaw representation of primary somatosensory cortex in anesthetized rats and studied laminar features of receptive fields (RFs) and representational maps. On average, RFs were smallest in layer IV and largest in layer V; however, for individual penetrations we found substantial deviations from this rule. Within the hindpaw representation, a distinct rostrocaudal gradient of RF size was present in all layers. While layer V RFs were generally largest independent of this gradient, layer IV RFs recorded caudally representing the proximal portions of the paw were larger than layer II/III RFs recorded rostrally representing the digits. The individual scatter of the locations of RFs across laminar groups was in the range of several millimeters, corresponding to about 25% of the average RF diameter. The cutaneous representations of the hindpaw in extragranular layers were confined to the areal extent defined by responsive sites in layer IV. Comparison between RFs determined quantitatively and by handplotting showed a reliable correspondence. Repeated measurements of RFs revealed spontaneous fluctuations of RF size of no more than 5% of the initial condition over an observation period of several hours. The topography and variability of cortical maps of the hindpaw representation were studied with a quantitative interpolation method taking into account the geometric centers of RFs and the corresponding cortical recording sites. On average, the overall topography in terms of preservation of neighborhood relations was present in all layers, although some individual maps showed severe distortions of topography. Factors contributing to map variability were overall position of the representation on the cortical surface, internal topography and spatial extent. Interindividual variability of map layout was always highest in the digit representations. Local topographic orderliness was lowest in layer V, but comparable in layers II/III and IV. Within layer IV, the lowest orderliness was observed in the digit representations. Our data emphasize a substantial variability of RF size, overlap and position across layers and within layers. At the level of representational maps, we found a similar degree of variability that often co-varied across layers, with little evidence for significant layer specificity. Laminar differences are likely to arise from the specific input-output pattern, layer-specific cell types and the connectivity between different layers. Our findings emphasizing similarities in the variability across layers support the notion of tightly coupled columnar interactions between different layers.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / physiology
  • Afferent Pathways / cytology
  • Afferent Pathways / physiology*
  • Animals
  • Body Patterning / physiology
  • Brain Mapping*
  • Female
  • Foot / innervation*
  • Foot / physiology
  • Male
  • Neural Pathways / cytology
  • Neural Pathways / physiology
  • Neuronal Plasticity / physiology
  • Physical Stimulation
  • Rats
  • Rats, Sprague-Dawley
  • Skin / innervation
  • Somatosensory Cortex / anatomy & histology*
  • Somatosensory Cortex / cytology
  • Somatosensory Cortex / physiology*
  • Toes / innervation
  • Toes / physiology
  • Touch / physiology*