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

Neural responses to polar, hyperbolic, and Cartesian gratings in area V4 of the macaque monkey
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DOI:
10.1152/jn.1996.76.4.2718
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发表时间:
1996-10-01
影响因子:
2.5
通讯作者:
VanEssen, DC
VanEssen, DC
中科院分区:
医学3区
文献类型:
--
作者:
Gallant, JL;Connor, CE;VanEssen, DC

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1.我们研究了麻醉猕猴视觉V4区103个神经元对两类新的视觉刺激,极性和双曲正弦光栅的反应。我们在理论和实验上都怀疑,这些刺激对表征参与形态分析中间阶段的细胞是有用的。与传统的笛卡尔正弦光栅得到的响应进行比较。对整个细胞群体进行了五次独立的神经反应定量分析。对于每个细胞,直接比较对最有效的笛卡尔、极坐标和双曲线光栅的响应。在103个细胞中的18个中,由一个刺激类引起的峰值响应与由其余两个类引起的峰值响应显著不同。在剩下的85个细胞中,74个细胞对三种刺激类别的反应峰值都在2倍以内。信息论分析的试验对每个刺激的反应表明,所有,但两个细胞作为一个整体传输的重要信息的刺激集。对每个刺激类别的信息传输进行比较,发现103个细胞中有23个细胞传输的一类信息量与其余两类信息量显著不同。在剩下的80个细胞中,有55个细胞对三种刺激类别的信息传输速率都在2倍之内。为了识别在各种刺激空间中具有有序调谐曲线的细胞,用简单的高斯模型拟合对每个刺激类别的响应。调谐曲线成功地拟合的数据,从至少一个刺激类中的98个103细胞,这样的拟合获得了至少两个类中的87个细胞。单个神经元表现出广泛的调谐配置文件,响应峰值分散在各个刺激空间;有没有大的差异,在不同的刺激类获得的调谐曲线的宽度或位置的分布。5.根据神经元在刺激集上的反应曲线,采用层次聚类分析和多维标度两种客观方法对神经元进行分类。这两种分析产生了定性相似的结果。最明显的一组细胞对双曲光栅具有高度选择性。大多数细胞分为两组,有选择性的极性光栅:一个选择性的径向光栅和一个选择性的同心或螺旋光栅。没有一个小组的主要选择性是笛卡尔光栅。为了确定属于识别类别的细胞是否在解剖学上聚集,我们将电极穿透处的分类细胞的分布与如果细胞随机分布时预期的分布进行了比较。具有相似反应特征的细胞通常在解剖学上聚集。一个位置测试被用来确定是否响应配置文件是敏感的精确的刺激位置。笛卡尔和非笛卡尔光栅的一个子集,在几个位置和附近的感受野。该测试在来自本研究的13个细胞和来自早期研究的28个细胞上进行。所有的细胞都表现出显着程度的不变性,在他们的选择性跨越变化的刺激位置高达0.5经典的感受野直径。使用长度和宽度测试来确定偏好非笛卡尔光栅的细胞是否对笛卡尔光栅长度或宽度具有选择性。笛卡尔光栅短或窄于经典的感受野的反应进行了比较与全场笛卡尔和非笛卡尔光栅在29个细胞。在主测试中显示出对非笛卡尔光栅的显著偏好的四个细胞中,没有一个显示出对笛卡尔光栅长度或宽度的调谐,这将解释它们的非笛卡尔响应。然而,在样本中的其他五个单元中证明了对笛卡尔光栅长度或宽度的调谐。V4神经元的人口显示出明显的偏见,有利于极性和双曲线刺激,他们的反应,有些细胞对这些刺激具有高度的选择性。笛卡尔刺激本身不能解释大多数细胞对非笛卡尔刺激的反应。事实上,几乎所有的细胞都传达了关于所有三种刺激类别的重要信息,并且大多数细胞在多个类别中具有可识别的调谐曲线,这表明V4细胞既不是简单的特征检测器,也不是单一限制刺激空间内的简单过滤器。针对多个刺激类别的调谐可以反映特定的视觉处理功能或诸如有效图像编码的一般原理。
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 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 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 and one selective for concentric or spiral gratings. There was no group whose primary selectivity was for 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 non-Cartesian responses. However, tuning for Cartesian gratings length or width was demonstrated in five 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 image encoding.