On the Division of Cortical Cells Into Simple and Complex Types: A Comparative Viewpoint

Abstract

Ibbotson, M. R., N.S.C. Price, and N. A. Crowder. On the division of cortical cells into simple and complex types: a comparative viewpoint. J Neurophysiol 93: 3699 -3702, 2005. First published January 19, 2005 doi:10.1152/jn.01159.2004. Hubel and Weisel introduced the concept of cells in cat primary visual cortex being partitioned into two categories: simple and complex. Subsequent authors have developed a quantitative measure to distinguish the two cell types based on the ratio between modulated responses at the stimulus frequency (F 1 ) and unmodulated (F 0 ) components of the spiking responses to drifting sinusoidal gratings. It has been shown that cells in anesthetized cat and monkey cortex have bimodal distributions of F 1 /F 0 ratios. A clear local minimum or dip exists in the distribution at a ratio close to unity. Here we present a comparison of the distributions of the F 1 /F 0 ratios between cells in the primary visual cortex of the eutherian cat and marsupial Tammar wallaby, Macropus eugenii. This is the first quantitative description of any marsupial cortex using the F 1 /F 0 ratio and follows earlier papers showing that cells in wallaby cortex are tightly oriented and spatial frequency tuned. The results reveal a bimodal distribution in the wallaby F 1 /F 0 ratios that is very similar to that found in the rat, cat, and monkey. Discussion focuses on the mechanisms that could lead to such similar cell distributions in animals with diverse behaviors and phylogenies. I N T R O D U C T I O NHubel and Weisel (1962) first categorized cells in the primary visual cortices of cats into two distinct cell types: simple and complex. The distinction was based on the spiking responses of cells during four visual tests. Simple cells 1) have spatially segregated ON and OFF regions within their receptive fields; 2) show summation within each subregion; 3) have antagonistic ON and OFF subregions; and 4) have responses that can be predicted based on the organization of their receptive field (RF) subregions. Cells that did not meet all or any of these criteria were classified as complex. Since the pioneering observations of Hubel and Weisel, a method was developed to quantify the simple and complex categories based on the spiking responses of the cells to moving sinusoidal gratings (De Valois et al. 1982; Movshon et al. 1978a,b; for review, Skottun et al. 1991). The method calculates the mean response of the cells above spontaneous rate during the period of motion (F 0 ) and the amplitude of oscillations at the fundamental temporal frequency of the stimulus (F 1 ). An F 1 /F 0 ratio is then calculated. Skottun et al. (1991) showed that, when the ratios were plotted for a large population of cells in cat and monkey V1, the neurons fell into a bimodal distribution with peaks at ratios of 1.7 and 0.2-0.3. There was a clear minimum or dip close to an F 1 /F 0 ratio of unity. Separating the neuron types based on those with F 1 /F 0 ratios Ͼ1 or Ͻ1 produced a distribution that correlated well with the classifications based ...

The linearity and selectivity of neuronal responses in awake visual cortex

“…While previous studies have clearly demonstrated that F1/F0 ratios are bimodally distributed in the anesthetized animal (De Valois et al, 1982; Dean & Tolhurst, 1983; Ibbotson et al, 2005; Mata & Ringach, 2005; Priebe et al, 2004; Ringach, Shapley et al, 2002; Schiller et al, 1976b; Skottun et al, 1991), the number of studies that used the F1/F0 ratio as a criteria to classify cortical cells is much larger than the number of studies that have demonstrated a significant bimodal distribution (see Table 1). There are multiple examples of studies that measured the distribution of F1/F0 ratios and failed to find significance for bimodality as, for example, Mata & Ringach (2005) in anesthetized primate and Heimel et al (2005) in anesthetized squirrel.…”

A computational theory of visual receptive fields

“…Bardy et al (2006) have shown that the response properties of some classes of complex cells can be converted to putative simple cells depending on influences originating from the classical receptive field. The experimental results can, however, be strongly dependent on the experimental conditions (Kagan et al 2002; Mata and Ringach 2005; Chen et al 2002) and bimodal distributions have been found by Kagan et al (2002), Ibbitson et al (2005), and Chen et al (2002). Moreover, Martinez and Alonso (2003) argue that a large body of neurophysiological evidence indicates that simple cells are a separate population from the total of cortical cells in cat visual cortex.…”

Phase sensitivities, excitatory summation fields, and silent suppressive receptive fields of single neurons in the parastriate cortex of the cat

“…It has been reported in the past that the frequency distributions of F1/F0 spike-response ratios (to optimized grating patches) of neurons recorded from areas V1 of anesthetized domestic cats (Li et al 2003;Movshon et al 1978aMovshon et al , 1978bSkottun et al 1991), macaques (De Valois et al 1982;Ringach et al 2002;Skottun et al 1991), laboratory rats (Girman et al 1999), house mice (Niell and Stryker 2008), and tammar wallabies (Ibbotson et al 2005) are not unimodal, with frequency "dip" at the intermediate F1/F0 ratios of 0.7-1.3, that is, close to the ratio of 1. The apparent bimodality of frequency distribution of F1/F0 spike-response ratios has been invoked in support of the argument that in area V1, at least, cells with F1/F0 ratios Ͼ1 and these with ratios Ͻ1 represent two distinct groups of neurons.…”