Interactive effects among several stimulus parameters on the responses of striate cortical complex cells

Academic Article

Abstract

  • Although neurons within the visual system are often described in terms of their responses to particular patterns such as bars and edges, they are actually sensitive to many different stimulus features, such as the luminances making up the patterns and the duration of presentation. Many different combinations of stimulus parameters can result in the same neuronal response, raising the problem of how the nervous system can extract information about visual stimuli from such inherently ambiguous responses. It has been shown that complex cells transmit significant amounts of information in the temporal modulation of their responses, raising the possibility that different stimulus parameters are encoded in different aspects of the response. To find out how much information is actually available about individual stimulus parameters, we examined the interactions among three stimulus parameters in the temporally modulated responses of striate cortical complex cells. Sixteen black and white patterns were presented to two awake monkeys at each of four luminance-combinations and five durations, giving a total of 320 unique stimuli. Complex cells were recorded in layers 2 and 3 of striate cortex, with the stimuli centered on the receptive fields as determined by mapping with black and white bars. An analysis of variance (ANOVA) was applied to these data with the three stimulus parameters of pattern, the luminance-combinations, and duration as the independent variables. The ANOVA was repeated with the magnitude and three different aspects of the temporal modulation of the response as the dependent variables. For the 19 neurons studied, many of the interactions between the different stimulus parameters were statistically significant. For some response measures the interactions accounted for more than one-half of the total response variance. We also analyzed the stimulus-response relationships with the use of information theoretical techniques. We defined input codes on the basis of each stimulus parameter alone, as well as their combinations, and output codes on the basis of response strength, and on three measures of temporal modulation, also taken individually and together. Transmitted information was greatest when the response of a neuron was interpreted as a temporally modulated message about combinations of all three stimulus parameters. The interaction terms of the ANOVA suggest that the response of a complex cell can only be interpreted as a message about combinations of all three stimulus parameters. However, the information about a single parameter was not completely obscured even when the other parameters were varied, i.e., the response of a complex cell could be interpreted as a message about any single stimulus parameter. The three-part temporal code carried at least twice as much stimulus-dependent information as the response strength alone. Every aspect of the response carried more information about the stimulus pattern than about any other stimulus parameter. No single aspect of the response was dedicated to any particular stimulus parameter. However, the proportion of the information about the luminance-combinations and duration was greater in the temporal modulation of the response than in the response strength. The significant interactions among stimulus parameters shown by the ANOVA means that the effect on a neuronal response of changing one stimulus parameter is a function of the values of the other parameters. Thus, the value of any single stimulus parameter cannot be determined from a neuronal response by simply subtracting the effects of the other stimulus parameters, as a linear model would suggest. However, information theory does not assume a linear model, and it showed that with a nonlinear system the response of a neuron can be interpreted as a message about single stimulus parameters and not just about combinations of parameters.
  • Authors

    Published In

    Digital Object Identifier (doi)

    Author List

  • Gawne TJ; Richmond BJ; Optican LM
  • Start Page

  • 379
  • End Page

  • 389
  • Volume

  • 66
  • Issue

  • 2