Watamaniuk Scott N J, Bal Japjot, Heinen Stephen J
Department of Psychology, Wright State University, Dayton, Ohio 45435, and
The Smith Kettlewell Eye Research Institute, San Francisco, California 94115.
J Neurosci. 2017 Nov 22;37(47):11424-11430. doi: 10.1523/JNEUROSCI.2186-17.2017. Epub 2017 Oct 23.
Ocular smooth pursuit and fixation are typically viewed as separate systems, yet there is evidence that the brainstem fixation system inhibits pursuit. Here we present behavioral evidence that the fixation system modulates pursuit behavior outside of conscious awareness. Human observers (male and female) either pursued a small spot that translated across a screen, or fixated it as it remained stationary. As shown previously, pursuit trials potentiated the oculomotor system, producing anticipatory eye velocity on the next trial before the target moved that mimicked the stimulus-driven velocity. Randomly interleaving fixation trials reduced anticipatory pursuit, suggesting that a potentiated fixation system interacted with pursuit to suppress eye velocity in upcoming pursuit trials. The reduction was not due to passive decay of the potentiated pursuit signal because interleaving "blank" trials in which no target appeared did not reduce anticipatory pursuit. Interspersed short fixation trials reduced anticipation on long pursuit trials, suggesting that fixation potentiation was stronger than pursuit potentiation. Furthermore, adding more pursuit trials to a block did not restore anticipatory pursuit, suggesting that fixation potentiation was not overridden by certainty of an imminent pursuit trial but rather was immune to conscious intervention. To directly test whether cognition can override fixation suppression, we alternated pursuit and fixation trials to perfectly specify trial identity. Still, anticipatory pursuit did not rise above that observed with an equal number of random fixation trials. The results suggest that potentiated fixation circuitry interacts with pursuit circuitry at a subconscious level to inhibit pursuit. When an object moves, we view it with smooth pursuit eye movements. When an object is stationary, we view it with fixational eye movements. Pursuit and fixation are historically regarded as controlled by different neural circuitry, and alternating between invoking them is thought to be guided by a conscious decision. However, our results show that pursuit is actively suppressed by prior fixation of a stationary object. This suppression is involuntary, and cannot be avoided even if observers are certain that the object will move. The results suggest that the neural fixation circuitry is potentiated by engaging stationary objects, and interacts with pursuit outside of conscious awareness.
眼平滑追踪和注视通常被视为两个独立的系统,但有证据表明脑干注视系统会抑制追踪。在此,我们展示行为学证据,表明注视系统在意识觉知之外调节追踪行为。人类观察者(男性和女性)要么追踪在屏幕上平移的一个小点,要么在其静止时注视它。如先前所示,追踪试验增强了动眼系统,在目标移动之前的下一次试验中产生预期眼速,该眼速模仿了刺激驱动的速度。随机穿插注视试验减少了预期追踪,表明增强的注视系统与追踪相互作用,以抑制即将到来的追踪试验中的眼速。这种减少并非由于增强的追踪信号的被动衰减,因为穿插没有目标出现的“空白”试验并没有减少预期追踪。穿插短时间的注视试验减少了长时间追踪试验中的预期,表明注视增强比追踪增强更强。此外,在一个组块中增加更多的追踪试验并不能恢复预期追踪,这表明注视增强不会被即将进行的追踪试验的确定性所推翻,而是不受意识干预的影响。为了直接测试认知是否能克服注视抑制,我们交替进行追踪和注视试验以完美确定试验类型。然而,预期追踪仍未超过在相同数量的随机注视试验中观察到的水平。结果表明,增强的注视回路在潜意识层面与追踪回路相互作用以抑制追踪。当一个物体移动时,我们用平滑追踪眼动来观察它。当一个物体静止时,我们用注视眼动来观察它。追踪和注视在历史上被认为是由不同的神经回路控制的,并且在它们之间切换被认为是由有意识的决定所引导。然而,我们的结果表明,对静止物体的先前注视会主动抑制追踪。这种抑制是不由自主的,即使观察者确定物体将会移动也无法避免。结果表明,神经注视回路通过与静止物体的接触而增强,并在意识觉知之外与追踪相互作用。