Neural responses to polar, hyperbolic, and Cartesian gratings in area V4 of the macaque monkey

Jack L. Gallant, Charles Edward Connor, Subrata Rakshit, James W. Lewis, David C. Van Essen

Research output: Contribution to journalArticle

Abstract

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 with 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 that were all within a factor of 2 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 that were all within a factor of 2 of one another. 4. To identify cells that hurl 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 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 distributions 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 anti one selective for concentric or spiral gratings. There was no group whose primary selectivity was lot Cartesian gratings. 6. To determine whether cells belonging to identified classes were anatomically clustered, we compared the distribution of classified cells across electrode penetrations with 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 was 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. 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 with those obtained with full-field Cartesian and non-Cartesian gratings in 29 cells. Of the four 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 mm Cartesian responses. However, tuning for Cartesian grating length or width was demonstrated in rive 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 till 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 image encoding.

Original languageEnglish (US)
Pages (from-to)2718-2739
Number of pages22
JournalJournal of Neurophysiology
Volume76
Issue number4
StatePublished - Oct 1996
Externally publishedYes

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Macaca
Haplorhini
Neurons

ASJC Scopus subject areas

  • Physiology
  • Neuroscience(all)

Cite this

Gallant, J. L., Connor, C. E., Rakshit, S., Lewis, J. W., & Van Essen, D. C. (1996). Neural responses to polar, hyperbolic, and Cartesian gratings in area V4 of the macaque monkey. Journal of Neurophysiology, 76(4), 2718-2739.

Neural responses to polar, hyperbolic, and Cartesian gratings in area V4 of the macaque monkey. / Gallant, Jack L.; Connor, Charles Edward; Rakshit, Subrata; Lewis, James W.; Van Essen, David C.

In: Journal of Neurophysiology, Vol. 76, No. 4, 10.1996, p. 2718-2739.

Research output: Contribution to journalArticle

Gallant, JL, Connor, CE, Rakshit, S, Lewis, JW & Van Essen, DC 1996, 'Neural responses to polar, hyperbolic, and Cartesian gratings in area V4 of the macaque monkey', Journal of Neurophysiology, vol. 76, no. 4, pp. 2718-2739.
Gallant, Jack L. ; Connor, Charles Edward ; Rakshit, Subrata ; Lewis, James W. ; Van Essen, David C. / Neural responses to polar, hyperbolic, and Cartesian gratings in area V4 of the macaque monkey. In: Journal of Neurophysiology. 1996 ; Vol. 76, No. 4. pp. 2718-2739.
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abstract = "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 with 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 that were all within a factor of 2 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 that were all within a factor of 2 of one another. 4. To identify cells that hurl 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 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 distributions 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 anti one selective for concentric or spiral gratings. There was no group whose primary selectivity was lot Cartesian gratings. 6. To determine whether cells belonging to identified classes were anatomically clustered, we compared the distribution of classified cells across electrode penetrations with 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 was 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. 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 with those obtained with full-field Cartesian and non-Cartesian gratings in 29 cells. Of the four 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 mm Cartesian responses. However, tuning for Cartesian grating length or width was demonstrated in rive 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 till 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 image encoding.",
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T1 - Neural responses to polar, hyperbolic, and Cartesian gratings in area V4 of the macaque monkey

AU - Gallant, Jack L.

AU - Connor, Charles Edward

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AU - Lewis, James W.

AU - Van Essen, David C.

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N2 - 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 with 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 that were all within a factor of 2 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 that were all within a factor of 2 of one another. 4. To identify cells that hurl 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 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 distributions 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 anti one selective for concentric or spiral gratings. There was no group whose primary selectivity was lot Cartesian gratings. 6. To determine whether cells belonging to identified classes were anatomically clustered, we compared the distribution of classified cells across electrode penetrations with 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 was 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. 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 with those obtained with full-field Cartesian and non-Cartesian gratings in 29 cells. Of the four 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 mm Cartesian responses. However, tuning for Cartesian grating length or width was demonstrated in rive 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 till 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 image encoding.

AB - 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 with 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 that were all within a factor of 2 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 that were all within a factor of 2 of one another. 4. To identify cells that hurl 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 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 distributions 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 anti one selective for concentric or spiral gratings. There was no group whose primary selectivity was lot Cartesian gratings. 6. To determine whether cells belonging to identified classes were anatomically clustered, we compared the distribution of classified cells across electrode penetrations with 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 was 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. 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 with those obtained with full-field Cartesian and non-Cartesian gratings in 29 cells. Of the four 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 mm Cartesian responses. However, tuning for Cartesian grating length or width was demonstrated in rive 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 till 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 image encoding.

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