Washington National Primate Research Center, Seattle, Washington 98195; Department of Physiology and Biophysics, University of Washington, Seattle, Washington 98195; and University of Washington School of Medicine, Seattle, Washington 98195
Washington National Primate Research Center, Seattle, Washington 98195; Department of Physiology and Biophysics, University of Washington, Seattle, Washington 98195; and University of Washington School of Medicine, Seattle, Washington 98195.
J Neurosci. 2018 Mar 7;38(10):2430-2441. doi: 10.1523/JNEUROSCI.2432-17.2018. Epub 2018 Jan 31.
Primates rely predominantly on vision to gather information from the environment and neurons representing visual space and gaze position are found in many brain areas. Within the medial temporal lobe, a brain region critical for memory, neurons in the entorhinal cortex of macaque monkeys exhibit spatial selectivity for gaze position. Specifically, the firing rate of single neurons reflects fixation location within a visual image (Killian et al., 2012). In the rodents, entorhinal cells such as grid cells, border cells, and head direction cells show spatial representations aligned to visual environmental features instead of the body (Hafting et al., 2005; Sargolini et al., 2006; Solstad et al., 2008; Diehl et al., 2017). However, it is not known whether similar allocentric representations exist in primate entorhinal cortex. Here, we recorded neural activity in the entorhinal cortex in two male rhesus monkeys during a naturalistic, free-viewing task. Our data reveal that a majority of entorhinal neurons represent gaze position and that simultaneously recorded neurons represent gaze position relative to distinct spatial reference frames, with some neurons aligned to the visual image and others aligned to the monkey's head position. Our results also show that entorhinal neural activity can be used to predict gaze position with a high degree of accuracy. These findings demonstrate that visuospatial representation is a fundamental property of entorhinal neurons in primates and suggest that entorhinal cortex may support relational memory and motor planning by coding attentional locus in distinct, behaviorally relevant frames of reference. The entorhinal cortex, a brain area important for memory, shows striking spatial activity in rodents through grid cells, border cells, head direction cells, and nongrid spatial cells. The majority of entorhinal neurons signal the location of a rodent relative to visual environmental cues, representing the location of the animal relative to space in the world instead of the body. Recently, we found that entorhinal neurons can signal location of gaze while a monkey explores images visually. Here, we report that spatial entorhinal neurons are widespread in the monkey and these neurons are capable of showing a world-based spatial reference frame locked to the bounds of explored images. These results help connect the extensive findings in rodents to the primate.
灵长类动物主要依赖视觉从环境中获取信息,许多大脑区域都存在代表视觉空间和注视位置的神经元。在大脑内侧颞叶这个对记忆至关重要的区域,猕猴的内嗅皮层中的神经元对注视位置具有空间选择性。具体来说,单个神经元的放电率反映了视觉图像内的注视位置(Killian 等人,2012 年)。在啮齿动物中,网格细胞、边界细胞和头部方向细胞等内嗅细胞表现出与视觉环境特征对齐的空间表示,而不是与身体对齐(Hafting 等人,2005 年;Sargolini 等人,2006 年;Solstad 等人,2008 年;Diehl 等人,2017 年)。然而,目前尚不清楚在灵长类动物的内嗅皮层中是否存在类似的无参照系表示。在这里,我们在两只雄性恒河猴进行自然观看任务时记录了内嗅皮层的神经活动。我们的数据表明,大多数内嗅神经元表示注视位置,同时记录的神经元表示相对于不同空间参照系的注视位置,一些神经元与视觉图像对齐,另一些神经元与猴子的头部位置对齐。我们的结果还表明,内嗅神经活动可以高度准确地预测注视位置。这些发现表明,视觉空间表示是灵长类动物内嗅神经元的基本特性,并表明内嗅皮层可能通过在不同的、与行为相关的参照系中编码注意力位置来支持关系记忆和运动规划。内嗅皮层是大脑中与记忆有关的重要区域,在啮齿动物中通过网格细胞、边界细胞、头部方向细胞和非网格空间细胞表现出惊人的空间活动。大多数内嗅神经元表示相对于视觉环境线索的啮齿动物位置,代表动物相对于世界空间而不是身体的位置。最近,我们发现猴子在视觉探索图像时,内嗅神经元可以发出注视位置的信号。在这里,我们报告说,在猴子中,空间内嗅神经元分布广泛,这些神经元能够显示出与探索图像边界锁定的基于世界的空间参照系。这些结果有助于将啮齿动物中的广泛发现与灵长类动物联系起来。