Relationship between lateral inhibitory connections and the topography of the orientation map in cat visual cortex

Z. Kisvárday, D. S. Kim, U. T. Eysel, T. Bonhoeffer

Research output: Contribution to journalArticle

84 Citations (Scopus)

Abstract

The functional and structural topography of lateral inhibitory connections was investigated in visual cortical area 18 using a combination of optical imaging and anatomical tracing techniques in the same tissue. Orientation maps were obtained by recording intrinsic signals in regions of 8.4-19 mm2. To reveal the inhibitory connections provided by large basket cells, biocytin was iontophoretically injected at identified orientation sites guided by the pattern of surface blood vessels. The axonal and dendritic fields of two retrogradely labelled large basket cells were reconstructed in layer III. Their axonal fields extended up to 1360 μm from the parent somata. In addition to single basket cells, the population of labelled basket cell axons was also studied. For this analysis anterogradely labelled basket axons running horizontally over 460-1280 μm from the core of an injection site in layer III were taken into account. The distribution of large basket cell terminals according to orientation preferences of their target regions was quantitatively assessed. Using the same spatial resolution as the orientation map, a frequency distribution of basket cell terminals dependent on orientation specificity could be derived. For individual basket cells, the results showed that, on average, 43% of the terminals provided input to sites showing similar orientation preferences (±30°) to those of the parent somata. About 35% of the terminals were directed to sites representing oblique-orientation [±(30-60)°], and 22% of them terminated at cross-orientation sites [±(60-90)°]. Furthermore, the possible impact of large basket cells on target cells at different distances and orientation preferences was estimated by comparing the occurrence of orientation preferences with the occurrence of basket terminals on the distance scale. It was found that a basket cell could elicit isb-orientation inhibition with a high impact between 100-400 and 800-1200 μm, strong cross-orientation inhibition at -400-800 μm, and oblique-orientation inhibition between 300-500 and 700-900 μm from the parent soma. The non-isotropic topography of large basket axons suggests a complex function for this cell class, possibly including inhibition related to orientation and direction selectivity depending on the location of the target cells and possible target selectivity.

Original languageEnglish
Pages (from-to)1619-1632
Number of pages14
JournalEuropean Journal of Neuroscience
Volume6
Issue number10
DOIs
Publication statusPublished - 1994

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Visual Cortex
Cats
Carisoprodol
Axons
Optical Imaging
Running
Blood Vessels

Keywords

  • Basket cells
  • Optical recording
  • Orientation selectivity
  • Single cell reconstruction
  • Visual cortex

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Relationship between lateral inhibitory connections and the topography of the orientation map in cat visual cortex. / Kisvárday, Z.; Kim, D. S.; Eysel, U. T.; Bonhoeffer, T.

In: European Journal of Neuroscience, Vol. 6, No. 10, 1994, p. 1619-1632.

Research output: Contribution to journalArticle

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abstract = "The functional and structural topography of lateral inhibitory connections was investigated in visual cortical area 18 using a combination of optical imaging and anatomical tracing techniques in the same tissue. Orientation maps were obtained by recording intrinsic signals in regions of 8.4-19 mm2. To reveal the inhibitory connections provided by large basket cells, biocytin was iontophoretically injected at identified orientation sites guided by the pattern of surface blood vessels. The axonal and dendritic fields of two retrogradely labelled large basket cells were reconstructed in layer III. Their axonal fields extended up to 1360 μm from the parent somata. In addition to single basket cells, the population of labelled basket cell axons was also studied. For this analysis anterogradely labelled basket axons running horizontally over 460-1280 μm from the core of an injection site in layer III were taken into account. The distribution of large basket cell terminals according to orientation preferences of their target regions was quantitatively assessed. Using the same spatial resolution as the orientation map, a frequency distribution of basket cell terminals dependent on orientation specificity could be derived. For individual basket cells, the results showed that, on average, 43{\%} of the terminals provided input to sites showing similar orientation preferences (±30°) to those of the parent somata. About 35{\%} of the terminals were directed to sites representing oblique-orientation [±(30-60)°], and 22{\%} of them terminated at cross-orientation sites [±(60-90)°]. Furthermore, the possible impact of large basket cells on target cells at different distances and orientation preferences was estimated by comparing the occurrence of orientation preferences with the occurrence of basket terminals on the distance scale. It was found that a basket cell could elicit isb-orientation inhibition with a high impact between 100-400 and 800-1200 μm, strong cross-orientation inhibition at -400-800 μm, and oblique-orientation inhibition between 300-500 and 700-900 μm from the parent soma. The non-isotropic topography of large basket axons suggests a complex function for this cell class, possibly including inhibition related to orientation and direction selectivity depending on the location of the target cells and possible target selectivity.",
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