Neural Responses to Polar, Hyperbolic, and Cartesian Gratings in Area V4 of
the Macaque Monkey.
Gallant, Jack L., Charles E. Connor, Subrata Rakshit, James W. Lewis, and
David C. Van Essen.
Division of Biology, California Institute of Technology, Pasadena, CA,
91125 and Department of Anatomy and Neurobiology, Washington University School
of Medicine, St. Louis, MO, 63110.
APStracts 3:0140N, 1996.
SUMMARY AND CONCLUSIONS
1) We studied the responses of 103 neurons in visual area V4 of anesthetized
macaque monkeys to two novel classes of visual stimuli, polar and hyperbolic
sinusoidal gratings. We suspected on both theoretical and experimental grounds
that these stimuli would be useful for characterizing cells involved in
intermediate stages of form analysis. Responses were compared to those
obtained with conventional Cartesian sinusoidal gratings. Five independent,
quantitative analyses of neural responses were carried out on the entire
population of cells. 2) For each cell, responses to the most effective
Cartesian, polar, and hyperbolic grating were compared directly. In 18 of 103
cells, the peak response evoked by one stimulus class was significantly
different from the peak response evoked by the remaining two classes. Of the
remaining 85 cells, 74 had response peaks for the three stimulus classes which
were all within a factor of two of one another. 3) An information-theoretic
analysis of the trial-by-trial responses to each stimulus showed that all but
two cells transmitted significant information about the stimulus set as a
whole. Comparison of the information transmitted about each stimulus class
showed that 23 of 103 cells transmitted a significantly different amount of
information about one class than about the remaining two classes. Of the
remaining 80 cells, 55 had information transmission rates for the three
stimulus classes which were all within a factor of two of one another. 4) In
order to identify cells that had orderly tuning profiles in the various
stimulus spaces, responses to each stimulus class were fit with a simple
Gaussian model. Tuning curves were successfully fit to the data from at least
one stimulus class in 98 out of 103 cells, and such fits were obtained for at
least two classes in 87 cells. Individual neurons showed a wide range of
tuning profiles, with response peaks scattered throughout the various stimulus
spaces; there were no major differences in the distribution of the widths or
positions of tuning curves obtained for the different stimulus classes. 5)
Neurons were classified according to their response profiles across the
stimulus set with two objective methods, hierarchical cluster analysis and
multidimensional scaling. These two analyses produced qualitatively similar
results. The most distinct group of cells was highly selective for hyperbolic
gratings. The majority of cells fell into one of two groups that were
selective for polar gratings; one selective for radial gratings, and one
selective for concentric or spiral gratings. There was no group whose primary
selectivity was for Cartesian gratings. 6) In order to determine whether cells
belonging to identified classes were anatomically clustered, we compared the
distribution of classified cells across electrode penetrations to the
distribution that would be expected if the cells were distributed randomly.
Cells with similar response profiles were often anatomically clustered. 7) A
position test was used to determine whether response profiles were sensitive
to precise stimulus placement. A subset of Cartesian and non-Cartesian
gratings were presented at several positions in and near the receptive field.
The test was run on 13 cells from the present study and 28 cells from an
earlier study (Gallant et al., 1993). All cells showed a significant degree of
invariance in their selectivity across changes in stimulus position of up to
0.5 classical receptive field diameters. 8) A length and width test was used
to determine whether cells preferring non-Cartesian gratings were selective
for Cartesian grating length or width. Responses to Cartesian gratings shorter
or narrower than the classical receptive field were compared to those obtained
with full-field Cartesian and non-Cartesian gratings in 29 cells. Of the 4
cells that had shown significant preferences for non-Cartesian gratings in the
main test, none showed tuning for Cartesian grating length or width that would
account for their non-Cartesian responses. However, tuning for Cartesian
grating length or width was demonstrated in 5 other cells in the sample. 9)
The population of V4 neurons displayed a clear bias in their responses in
favor of polar and hyperbolic stimuli, and some cells were highly selective
for these stimuli. The Cartesian stimuli alone could not explain the responses
of most cells to non-Cartesian stimuli. The fact that nearly all cells
conveyed significant information about all three stimulus classes, and that
most had identifiable tuning curves in multiple classes, suggests that V4
cells are neither simple feature detectors nor simple filters within a single
restricted stimulus space. Tuning for multiple stimulus classes may reflect a
particular visual processing function or a general principle such as efficient
Received 17 April 1995; accepted in final form 18 April 1996.
APS Manuscript Number J262-5.
Article publication pending J. Neurophysiol.
ISSN 1080-4757 Copyright 1996 The American Physiological Society.
Published in APStracts on 4 July 96