Department of Integrative Physiology, Graduate School of Medicine, University of Yamanashi, Chuo-shi, Yamanashi 409-3898, Japan
Department of Integrative Physiology, Graduate School of Medicine, University of Yamanashi, Chuo-shi, Yamanashi 409-3898, Japan.
J Neurosci. 2023 Aug 16;43(33):5893-5904. doi: 10.1523/JNEUROSCI.0451-23.2023. Epub 2023 Jul 26.
The overrepresentation of centrifugal motion in the middle temporal visual area (area MT) has long been thought to provide an efficient coding strategy for optic flow processing. However, this overrepresentation compromises the detection of approaching objects, which is essential for survival. In the present study, we revisited this long-held notion by reanalyzing motion selectivity in area MT of three macaque monkeys (two males, one female) using random-dot stimuli instead of spot stimuli. We found no differences in the number of neurons tuned to centrifugal versus centripetal motion; however, centrifugally tuned neurons showed stronger tuning than centripetally tuned neurons. This was attributed to the heightened suppression of responses in centrifugal neurons to centripetal motion compared with that of centripetal neurons to centrifugal motion. Our modeling implies that this intensified suppression accounts for superior detection performance for weak centripetal motion stimuli. Moreover, through Fisher information analysis, we establish that the population sensitivity to motion direction in peripheral vision corresponds well with retinal motion statistics during forward locomotion. While these results challenge established concepts, considering the interplay of logarithmic Gaussian receptive fields and spot stimuli can shed light on the previously documented overrepresentation of centrifugal motion. Significantly, our findings reconcile a previously found discrepancy between MT activity and human behavior, highlighting the proficiency of peripheral MT neurons in encoding motion direction efficiently. The efficient coding hypothesis states that sensory neurons are tuned to specific, frequently experienced stimuli. Whereas previous work has found that neurons in the middle temporal (MT) area favor centrifugal motion, which results from forward locomotion, we show here that there is no such bias. Moreover, we found that the response of centrifugal neurons for centripetal motion was more suppressed than that of centripetal neurons for centrifugal motion. Combined with modeling, this provides a solution to a previously known discrepancy between reported centrifugal bias in MT and better detection of centripetal motion by human observers. Additionally, we show that population sensitivity in peripheral MT neurons conforms to an efficient code of retinal motion statistics during forward locomotion.
长期以来，人们一直认为，中间颞区视觉区（area MT）中离心运动的过度表现为光流处理提供了一种有效的编码策略。然而，这种过度表现会影响对接近物体的检测，这对生存至关重要。在本研究中，我们使用随机点刺激代替点刺激，重新分析了三只猕猴（两只雄性，一只雌性）的 area MT 中的运动选择性，从而重新审视了这一长期存在的观点。我们发现，对离心运动和向心运动敏感的神经元数量没有差异；然而，离心调谐神经元的调谐强度强于向心调谐神经元。这归因于与向心神经元相比，离心神经元对向心运动的反应抑制增强。我们的模型表明，这种增强的抑制解释了对弱向心运动刺激的优越检测性能。此外，通过 Fisher 信息分析，我们确定了在向前运动过程中，外周视觉中群体对运动方向的敏感性与视网膜运动统计数据非常吻合。虽然这些结果挑战了已建立的概念，但考虑到对数高斯感受野和点刺激的相互作用，可以揭示先前记录的离心运动过度表现的原因。重要的是，我们的发现调和了 MT 活动和人类行为之间先前发现的差异，突出了外周 MT 神经元在有效编码运动方向方面的出色能力。有效编码假说指出，感觉神经元对特定的、经常经历的刺激具有调谐性。虽然之前的工作发现，中间颞区（MT）区域的神经元偏向于由向前运动产生的离心运动，但我们在这里表明，这种偏向并不存在。此外，我们发现，离心神经元对向心运动的反应比向心神经元对离心运动的反应抑制更强。结合建模，这为之前报道的 MT 中离心偏向与人类观察者更好地检测向心运动之间的已知差异提供了一个解决方案。此外，我们表明，在向前运动过程中，外周 MT 神经元的群体敏感性符合视网膜运动统计的有效编码。
