Relationship Between Lateral Inhibitory Connections and the Topography of the Orientation Map in Cat Visual Cortex

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 microns 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 microns 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 degrees) to those of the parent somata. About 35% of the terminals were directed to sites representing oblique-orientation [+/- (30-60) degrees], and 22% of them terminated at cross-orientation sites [+/- (60-90) degrees]. 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 iso-orientation inhibition with a high impact between 100-400 and 800-1200 microns, strong cross-orientation inhibition at approximately 400-800 microns, and oblique-orientation inhibition between 300-500 and 700-900 microns 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.

Isodirectional Tuning of Adjacent Interneurons and Pyramidal Cells During Working Memory: Evidence for Microcolumnar Organization in PFC

“…Indeed, no evidence was found of feedforward inhibition in cross-correlations between simultaneously recorded FS and RS units, indicating a lack of functional inhibition between closely adjacent cells. However, isodirectional inhibition could occur between microcolumns, consistent with the findings of Thomson andcoworkers (1996, 1997), who reported considerable inhibition between FS interneurons and pyramidal cells at distances of ϳ50 -250 m. The differences in consensus of tuning between neighboring microcolumns may therefore provide the circuit basis for isodirectional inhibition, which serves to sharpen spatial tuning in a mechanism similar to that proposed for visual cortex (Crook et al 1997;Kisvarday et al 1994;Peres and Hochstein 1994;Ringach et al 1997;Somers et al 1995;Worgotter and Koch 1991).…”

“…10, bottom) by the spatial distribution of afferents to the principal sulcus from the contralateral hemisphere. In keeping with this model, it has been shown that basket cells project to nearby isooriented sites at 100 -400 m as well as to more distant cross-oriented sites 400 -800 m away (Kisvarday et al 1994). These columnar dimensions are in good accord with those reported for interdigitating columnar projections to the principal sulcus (Goldman-Rakic and Schwartz 1982) originating from the contralateral hemisphere and the posterior parietal cortex.…”

Pattern adaptation and cross-orientation interactions in the primary visual cortex

“…Indeed, each orientation column in the primary visual cortex sends both inhibitory and excitatory signals to all other orientation columns (Kisvárday and Eysel, 1993;Kisvárday et al, 1994Kisvárday et al, , 1997. There is, however, evidence suggesting that adaptation is caused by a decrease in the excitation received by a cortical cell rather than by an increase in inhibition.…”

Intracortical Origins of Interocular Suppression in the Visual Cortex

“…The fact that cross-orientation suppression is broadly tuned for orientation as well as spatial and temporal frequency (Bonds, 1989;DeAngelis et al, 1992;Sengpiel et al, 1995b;Allison et al, 2001) has been interpreted widely as an indication that it derives from inhibition exerted by a pool of cortical neurons with a wide range of stimulus preferences. A dense network of horizontal inhibitory connections (Kisvárday and Eysel, 1993;Kisvárday et al, 1994) appears ideally suited for this role. Indeed, pharmacological studies, in which either inhibitory inputs to the recorded neurons were blocked locally (Sillito, 1977(Sillito, , 1979 or neurons in nearby regions of cortex with differing orientation preferences were inactivated (Crook and Eysel, 1992;Crook et al, 1997Crook et al, , 1998, demonstrated a reduction in orientation selectivity, supporting the hypothesis that inhibitory interactions between neurons of different orientation preferences play an important role in the generation of cortical orientation selectivity (Sillito, 1979;Wörgötter and Koch, 1991;Somers et al, 1995;Carandini and Ringach, 1997).…”