Humans use saccadic eye movements to make frequent gaze changes, yet the associated full-field image motion is not perceived. The theory of saccadic suppression has been proposed to account for this phenomenon, but it is not clear whether suppression originates from a retinal signal at saccade onset or from the brain before saccade onset. Perceptually, visual sensitivity is reduced before saccades and enhanced afterward. Over the same time period, the perception of time is compressed and even inverted. We explore the origins and neural basis of these effects by recording from neurons in the dorsal medial superior temporal area (
Previous studies investigating the response properties of neurons in the primary visual cortex of cats and primates have shown that prolonged exposure to optimally oriented, high-contrast gratings leads to a reduction in responsiveness to subsequently presented test stimuli. We recorded from 119 neurons in cat V1 and V2 and found that in a high proportion of cells contrast adaptation also occurs for gratings oriented orthogonal to a neuron's preferred orientation, even though this stimulus did not elicit significant increases in spiking activity. Approximately 20% of neurons adapted equally to all orientations tested and a further 46% showed at least some adaptation to orthogonally oriented gratings, whereas 20% of neurons did not adapt to orthogonal gratings. The magnitude of contrast adaptation was positively correlated with adapting contrast, but was not related to the spiking activity of the cells. Highly direction selective neurons produced stronger adaptation to orthogonally oriented gratings than other neurons. Orientation-related adaptation was correlated with the rate of change of orientation tuning in consecutive cells along electrode penetrations that traveled parallel to the cortical layers. Nonoriented adaptation was most common in areas where orientation preference changed rapidly, whereas orientation-selective adaptation was most common in areas where orientation preference changed slowly. A minority of neurons did not show contrast adaptation (14%). No major differences were found between units in different cortical layers, V1 and V2, or between complex and simple cells. The relevance of these findings to the current understanding of adaptation within the context of orientation column architecture is discussed.
The responses of neurons in the middle temporal and medial superior temporal areas of macaque cortex are suppressed during saccades compared with saccade-like stimulus movements. We utilized the short-latency ocular following paradigm to show that this saccadic suppression is followed by postsaccadic enhancement of motion responses. The level of enhancement decays with a time constant of 100 ms from saccade end. The speed of ocular following is also enhanced after saccades and decays over a similar time course, suggesting a link between the neural and behavioral effects. There is some evidence that maximum postsaccadic enhancement occurs when cells are stimulated at their optimum speeds. Latencies of motion responses are saccade dependent: 37 ms for saccade-generated motion, 45 ms for motion in the half-second after saccades, and 70 ms with no prior saccades. The finding that saccades alter response latencies may partially explain perceptual time compression during saccades and time dilation after saccades.
The contribution of sensory neurons to perceptual decisions about external stimulus events has received much attention, but it is less clear how sensory responses are integrated over time to produce decisions that are both rapid and reliable. To address this issue, we recorded from middle temporal area and medial superior temporal area neurons in rhesus macaques performing a task requiring the detection and discrimination of unpredictable speed changes. We examined how neuronal activity encoded the sign of the speed change and predicted the animals' behavioral judgments and reaction times, with a focus on the timescales over which neuronal activity is informative. False detection trials, on which animals reported a speed change even though none had occurred, were grouped according to the animals' discrimination judgment. By comparing the neuronal responses between the two groups of false detection trials, we were able to predict the animals' choices from the sensory activity of single neurons at levels significantly better than chance. These choice probability measurements were strongest using spike counts in an 80 ms window ending 150 ms before a choice saccade began, but significant choice probabilities were observed in windows as short as 10 ms. While the maximum deviation in spiking rate following a speed change is evident in the transient response, averaging neuronal activity in longer time windows can be more informative about both the stimulus and the animals' behavioral judgments. Thus the timescales found in this study represent a trade-off between producing rapid reactions and overcoming the noise inherent in short time windows.
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