Herbert Wertheim School of Optometry & Vision Science, University of California, Berkeley.
Department of Computer Science, Northwestern University, Illinois, United States of America.
PLoS Comput Biol. 2024 Jan 11;20(1):e1011783. doi: 10.1371/journal.pcbi.1011783. eCollection 2024 Jan.
Neurons throughout the brain modulate their firing rate lawfully in response to sensory input. Theories of neural computation posit that these modulations reflect the outcome of a constrained optimization in which neurons aim to robustly and efficiently represent sensory information. Our understanding of how this optimization varies across different areas in the brain, however, is still in its infancy. Here, we show that neural sensory responses transform along the dorsal stream of the visual system in a manner consistent with a transition from optimizing for information preservation towards optimizing for perceptual discrimination. Focusing on the representation of binocular disparities-the slight differences in the retinal images of the two eyes-we re-analyze measurements characterizing neuronal tuning curves in brain areas V1, V2, and MT (middle temporal) in the macaque monkey. We compare these to measurements of the statistics of binocular disparity typically encountered during natural behaviors using a Fisher Information framework. The differences in tuning curve characteristics across areas are consistent with a shift in optimization goals: V1 and V2 population-level responses are more consistent with maximizing the information encoded about naturally occurring binocular disparities, while MT responses shift towards maximizing the ability to support disparity discrimination. We find that a change towards tuning curves preferring larger disparities is a key driver of this shift. These results provide new insight into previously-identified differences between disparity-selective areas of cortex and suggest these differences play an important role in supporting visually-guided behavior. Our findings emphasize the need to consider not just information preservation and neural resources, but also relevance to behavior, when assessing the optimality of neural codes.
大脑中的神经元会根据感觉输入有规律地调节它们的发放率。神经计算理论假设,这些调制反映了一个受约束的优化过程的结果,在这个过程中,神经元旨在稳健而有效地表示感觉信息。然而,我们对这种优化在大脑不同区域之间的变化的理解还处于起步阶段。在这里,我们表明,神经感觉反应沿着视觉系统的背侧流变换,这与从优化信息保持向优化感知辨别转变一致。我们关注双眼视差的表示——双眼视网膜图像的细微差异,重新分析了猕猴大脑区域 V1、V2 和 MT(中颞)中描述神经元调谐曲线的测量值。我们将这些测量值与使用 Fisher 信息框架在自然行为中遇到的双眼视差统计数据进行了比较。跨区域的调谐曲线特征差异与优化目标的转变一致:V1 和 V2 的群体水平反应更符合最大化关于自然发生的双眼视差的编码信息,而 MT 的反应则转向最大化支持视差辨别能力。我们发现,向偏好更大视差的调谐曲线的转变是这种转变的关键驱动因素。这些结果为以前在皮层的视差选择性区域之间发现的差异提供了新的见解,并表明这些差异在支持视觉引导行为中起着重要作用。我们的发现强调,在评估神经代码的最优性时,不仅需要考虑信息保持和神经资源,还需要考虑与行为的相关性。