注：机翻，未校。
Evolution of the human brain: when bigger is better 人脑的进化：越大越好
Michel A. Hofman*
- Netherlands Institute for Neuroscience, Royal Netherlands Academy of Arts and Sciences, Amsterdam, Netherlands
荷兰皇家艺术与科学学院荷兰神经科学研究所， 荷兰阿姆斯特丹
Comparative studies of the brain in mammals suggest that there are general architectural principles governing its growth and evolutionary development. We are beginning to understand the geometric, biophysical and energy constraints that have governed the evolution and functional organization of the brain and its underlying neuronal network. The object of this review is to present current perspectives on primate brain evolution, especially in humans, and to examine some hypothetical organizing principles that underlie the brain’s complex organization. Some of the design principles and operational modes that underlie the information processing capacity of the cerebral cortex in primates will be explored. It is shown that the development of the cortex coordinates folding with connectivity in a way that produces smaller and faster brains, then otherwise would have been possible. In view of the central importance placed on brain evolution in explaining the success of our own species, one may wonder whether there are physical limits that constrain its processing power and evolutionary potential. It will be argued that at a brain size of about 3500 cm3, corresponding to a brain volume two to three times that of modern man, the brain seems to reach its maximum processing capacity. The larger the brain grows beyond this critical size, the less efficient it will become, thus limiting any improvement in cognitive power.
对哺乳动物大脑的比较研究表明，有一般的结构原则控制着它的生长和进化发展。我们开始了解控制大脑及其潜在神经元网络的进化和功能组织的几何、生物物理和能量限制。本综述的目的是提出当前对灵长类动物大脑进化的看法，尤其是在人类中，并研究一些构成大脑复杂组织基础的假设组织原则。将探讨灵长类动物大脑皮层信息处理能力的一些设计原则和操作模式。结果表明，皮层的发育以产生更小、更快的大脑的方式协调折叠与连接，否则是可能的。鉴于大脑进化在解释我们自己物种的成功方面具有核心重要性，人们可能会想，是否存在限制其处理能力和进化潜力的物理限制。有人会说，在大约 3500 cm3 的大脑大小下，相当于现代人的 2 到 3 倍的大脑体积，大脑似乎达到了其最大处理能力。大脑长得越大超过这个临界大小，它的效率就越低，从而限制了认知能力的任何提高。
Introduction 介绍
The human brain contains about 100 billion neurons, more than 100,000 km of interconnections, and has an estimated storage capacity of 1.25 × 1012 bytes (Cherniak, 1990; Hofman, 2012). These impressive numbers have led to the idea that our cognitive capabilities are virtually without limit. The human brain, however, has evolved from a set of underlying structures that constrain its size, and the amount of information it can store and process. If the ability of an organism to process information about its environment is a driving force behind evolution, then the more information a system, such as the brain, receives, and the faster it can process this information, the more adequately it will be able to respond to environmental challenges and the better will be its chances of survival (Macphail and Bolhuis, 2001; Roth and Dicke, 2012; Hofman, 2014). The limit to any intelligent system therefore lies in its abilities to process and integrate large amounts of sensory information and to compare these signals with as many memory states as possible, and all that in a minimum of time. It implies that the functional capacity of a neuronal structure is inherently limited by its neural architecture and signal processing time (see e.g., Laughlin and Sejnowski, 2003; Buzsáki et al., 2013). The object of this review is to present current perspectives on primate brain evolution, especially in humans, and to examine some hypothetical organizing principles that underlie the brain’s complex organization. Some of the design principles and operational modes that underlie the information processing capacity of the cerebral cortex in primates will be explored, and it will be argued that with the evolution of the human brain we have nearly reached the limits of biological intelligence.
人脑包含大约 1000 亿个神经元，超过 100,000 公里的互连，估计存储容量为 1.25 × 1012 字节（Cherniak，1990 年;Hofman，2012 年）。这些令人印象深刻的数字导致了这样一种观点，即我们的认知能力几乎是无限的。然而，人脑是从一组限制其大小以及它可以存储和处理的信息量的底层结构演变而来的。如果一个有机体处理有关其环境信息的能力是进化背后的驱动力，那么一个系统（如大脑）接收到的信息越多，它处理这些信息的速度就越快，它就越能充分地应对环境挑战，它的生存机会就越大（Macphail 和 Bolhuis， 2001;Roth 和 Dicke，2012 年;Hofman，2014 年）。因此，任何智能系统的局限性在于它处理和整合大量感官信息的能力，并将这些信号与尽可能多的记忆状态进行比较，所有这些都是在最短的时间内完成的。这意味着神经元结构的功能能力本质上受到其神经结构和信号处理时间的限制（参见例如，Laughlin 和 Sejnowski，2003 年;Buzsáki et al.， 2013）。本综述的目的是提出当前对灵长类动物大脑进化的看法，尤其是在人类中，并研究一些构成大脑复杂组织基础的假设组织原则。将探讨灵长类动物大脑皮层信息处理能力的一些设计原则和操作模式，并论证随着人脑的进化，我们几乎达到了生物智能的极限。
Principles of Brain Evolution 大脑进化的原理
If we assume that biological intelligence in higher organisms is the product of processes of complex sensory information processing and mental faculties, responsible for the planning, execution and evaluation of intelligent behavior, variations among species in intelligence must in principle be observable in the neural substrate. In higher organisms, especially in primates, the complexity of the neural circuitry of the cerebral cortex is considered to be the neural correlate of the brain’s coherence and predictive power, and, thus, a measure of intelligence.
如果我们假设高等生物体的生物智能是复杂的感觉信息处理和心理官能过程的产物，负责规划、执行和评估智能行为，那么原则上必须在神经基质中观察到物种之间的智能变化。在高等生物体中，尤其是灵长类动物中，大脑皮层神经回路的复杂性被认为是大脑连贯性和预测能力的神经相关性，因此是智力的衡量标准。
The evolutionary expansion of the cerebral cortex, indeed, is among the most distinctive morphological features of mammalian brains. Particularly in species with large brains, and most notably in great apes and marine mammals, the brain becomes disproportionately composed of this cortical structure (Northcutt and Kaas, 1995; Striedter, 2005; Aboitiz and Montiel, 2012; Sherwood et al., 2012; Figure 1). The volume of cortical gray matter, for example, expressed as a percentage of total brain volume increases from about 25% for insectivores to 50% for humans (Frahm et al., 1982; Hofman, 1988), whereas the relative size of the entire cerebral cortex (including white matter) goes from 40% in mice to about 80% in humans (Hofman, 1988; Azevedo et al., 2009; Herculano-Houzel, 2009, 2012).
事实上，大脑皮层的进化扩张是哺乳动物大脑最独特的形态特征之一。特别是在具有大大脑的物种中，尤其是在类人猿和海洋哺乳动物中，大脑变得不成比例地由这种皮层结构组成（Northcutt 和 Kaas，1995 年;Striedter，2005 年;Aboitiz 和 Montiel，2012 年;Sherwood 等人，2012 年;图 1）。例如，皮质灰质的体积表示为占总脑体积的百分比，从食虫动物的约 25% 增加到人类的 50%（Frahm 等人，1982 年;Hofman， 1988），而整个大脑皮层（包括白质）的相对大小从小鼠的 40% 到人类的 80% 左右（Hofman， 1988;Azevedo et al.， 2009;Herculano-Houzel，2009 年、2012 年）。
FIGURE 1
Figure 1. Lateral views of the brains of some mammals to show the evolutionary development of the neocortex (gray). In the hedgehog almost the entire neocortex is occupied by sensory and motor areas. In the prosimian Galago the sensory cortical areas are separated by an area occupied by association cortex (AS). A second area of association cortex is found in front of the motor cortex. In man these anterior and posterior association areas are strongly developed. A, primary auditory cortex; AS, association cortex; Ent, entorhinal cortex; I, insula; M, primary motor cortex; PF, prefrontal cortex; PM, premotor cortex; S, primary somatosensory cortex; V, primary visual cortex. Modified with permission from Nieuwenhuys (1994).
图 1.一些哺乳动物大脑的侧视图，显示新皮层的进化发展（灰色）。在刺猬中，几乎整个新皮层都被感觉和运动区域占据。在 prosimian Galago 中，感觉皮层区域被关联皮层 （AS） 占据的区域隔开。第二个关联皮层区域位于运动皮层的前面。在人类中，这些前部和后部关联区域非常发达。A， 初级听觉皮层;AS，关联皮层;Ent，内嗅皮层;I， 岛叶;M， 初级运动皮层;PF，前额叶皮层;PM，前运动皮层;S， 初级体感皮层;V， 初级视觉皮层。经 Nieuwenhuys （1994） 许可修改。
On the other hand, the relative size of the cerebellum remains constant across phylogenetic groups, occupying about 10–15% of the total brain mass in different orders (Stephan et al., 1981). Comparative studies among four mammalian orders, including primates, have recently revealed that the absolute neuronal composition in the cerebral cortex covaries significantly with that of the cerebellum (Herculano-Houzel et al., 2008; Lent et al., 2012), showing that these two brain structures display coordinated growth during phylogenesis in mammals.
另一方面，小脑的相对大小在系统发育组中保持不变，以不同的顺序占据总脑质量的 10-15% 左右（Stephan 等人，1981 年）。包括灵长类动物在内的四种哺乳动物目之间的比较研究最近表明，大脑皮层中的绝对神经元组成与小脑的绝对神经元组成显著相关（Herculano-Houzel et al.， 2008;Lent et al.， 2012），表明这两个大脑结构在哺乳动物的系统发生过程中表现出协调生长。
Such a coordinated evolution of the cerebral cortex and cerebellum fits well with the recent clinical and experimental evidence suggesting an important role of the cerebellum in cognitive and affective functions, in close connection with cortical associative areas (for reviews, see Schmahmann, 2010; MacLeod, 2012). Although the cerebral cortex is not the only brain structure which was selected for in evolution for greater growth, as a result of growing environmental pressure for more sophisticated cognitive abilities, it has played a key role in the evolution of intelligence.
大脑皮层和小脑的这种协调进化与最近的临床和实验证据非常吻合，这些证据表明小脑在认知和情感功能中发挥着重要作用，与皮层联想区域密切相关（有关评论，参见 Schmahmann，2010 年;MacLeod，2012 年）。尽管大脑皮层并不是进化中唯一被选择用于更大增长的大脑结构，但由于环境对更复杂的认知能力的压力越来越大，它在智力的进化中发挥了关键作用。
Evolution of the Cerebral Cortex 大脑皮层的进化
It is now well established that the cerebral cortex forms as a smooth sheet populated by neurons that proliferate at the ventricular surface and migrate outwards along radial glial fibers (for reviews, see Cheung et al., 2007; Rakic, 2009). Differences in the duration of neurogenesis, which increases more rapidly with brain size for the cerebral cortex than for subcortical areas (Finlay et al., 2001; Charvet and Finlay, 2012), lead to a systematic increase in the ratio of the cortical to subcortical regions. Whereas in small brained species the cortical volume expands by virtue of a combined increase in surface area and cortical thickness, the increase of the cortical volume in species with a brain size of more than 3–4 cm3 is almost entirely due to a disproportionate expansion of the cortical surface area (Hofman, 1989). It is the increase of the cortical surface area beyond that expected for geometrically similar objects of different volumes which creates the need to cortical folding (Jerison, 1982; Todd, 1986; Hofman, 1989, 2012, Figure 2).
现在已经确定的是，大脑皮层形成一个光滑的片状，由神经元组成，这些神经元在心室表面增殖并沿着放射状神经胶质纤维向外迁移（有关评论，参见 Cheung 等人，2007 年;Rakic，2009 年）。神经发生持续时间的差异，大脑皮层的大脑大小比皮层下区域的神经发生持续时间增加得更快（Finlay等人，2001 年;Charvet 和 Finlay，2012 年），导致皮质与皮质下区域之比的系统性增加。在小脑物种中，皮质体积通过表面积和皮质厚度的组合增加而扩大，而在大脑大小超过 3-4 cm3 的物种中，皮质体积的增加几乎完全是由于皮质表面积的不成比例的扩大（Hofman，1989）。正是皮层表面积的增加超出了不同体积的几何相似物体的预期，这产生了皮层折叠的需求（Jerison，1982 年;Todd，1986 年;Hofman，1989 年，2012 年，图 2）。
FIGURE 2
Figure 2. Lateral views of the brains of some anthropoid primates showing the evolutionary expansion of the neocortex. Note the diverse configurations and gyral and sulcal patterns. Saimiri sciureus: E = 22 g; Macaca mulatta: E = 95 g; Pan troglodytes: E = 420 g; Homo sapiens: E = 1350 g. Reproduced with permission from Hofman (2007).
图 2.一些类人灵长类动物大脑的侧视图显示了新皮层的进化扩张。注意不同的配置以及回和沟模式。Saimiri sciureus：E = 22 克;猕猴：E = 95 克;泛穴居动物：E = 420 克;智人：E = 1350 克。经 Hofman （2007） 许可转载。
Consequently, the brains of larger species, like primates, are not well described by the ideal constructs of Euclidean geometry. Mandelbrot (1982) coined the word “fractal” to identify this group of complex geometric forms and developed the concept of fractal scaling to describe their organized variability. An important feature of fractal objects is that they are invariant, in a statistical sense, over a wide range of scales, a property that is known as scaling (for a review, see Hofman, 2012).
因此，较大的物种（如灵长类动物）的大脑并不能用欧几里得几何的理想结构很好地描述。Mandelbrot （1982） 创造了“分形”一词来识别这组复杂的几何形式，并发展了分形缩放的概念来描述它们的有组织可变性。分形对象的一个重要特征是，从统计学意义上讲，它们在很宽的尺度上是不变的，这一特性被称为缩放（有关评论，请参阅 Hofman，2012 年）。
In mammals with convoluted brains, among which are almost all primates, the cortical surface area, rather than being proportional to the 2/3 power of geometric similarity, is nearly a linear function of brain volume (Hofman, 1985a, 1989). It means that if a mouse brain (volume = 0.5 cm3) were scaled up as the two-thirds power to the size of the human brain (volume = 1400 cm3) it would have a cortical surface of only about 480 cm2. The actual surface area of the human cortex, however, is about 2000 cm2, which is more than four times larger than would be predicted assuming geometric similarity, indicating that mammalian brains change their shape by becoming folded as they increase in size.
在大脑复杂的哺乳动物中，其中几乎都是灵长类动物，皮质表面积几乎是大脑体积的线性函数，而不是与几何相似性的 2/3 次方成正比（Hofman， 1985a， 1989）。这意味着，如果将小鼠大脑（体积 = 0.5 cm3）放大到人脑大小（体积 = 1400 cm3）的三分之二倍，它的皮质表面将只有约 480 cm2。然而，人类皮层的实际表面积约为 2000 cm2，比假设几何相似性预测的表面积大四倍多，这表明哺乳动物的大脑随着尺寸的增加而折叠，从而改变其形状。
Mechanisms of Cortical Folding 皮质折叠的机制
Previous hypotheses about cortical folding have emphasized mechanisms intrinsic to the cortical gray matter (for reviews, see Hofman, 1989; Bayly et al., 2014). Van Essen (1997) suggested that extrinsic factors are more important and that tension along axons in the white matter is the primary driving force for cortical folding. By keeping the aggregate length of axonal and dendritic wiring low, tension should contribute to the compactness of neural circuitry throughout the cortex. Despite the many attempts to clarify the mechanical basis of cortical folding the process remains incompletely understood.
以前关于皮质折叠的假设强调了皮质灰质固有的机制（有关评论，请参见 Hofman，1989 年;Bayly等人，2014 年）。Van Essen （1997） 认为外在因素更为重要，白质中沿轴突的张力是皮质折叠的主要驱动力。通过保持轴突和树突布线的总长度较低，张力应该有助于整个皮层神经回路的紧凑性。尽管多次尝试阐明皮质折叠的机械基础，但该过程仍未完全了解。
Recently, Herculano-Houzel and colleagues have found that connectivity and cortical folding are directly related across species and that a simple model based on a white matter-based mechanism may account for increased cortical folding in the primate cerebral cortex (Herculano-Houzel et al., 2010; Mota and Herculano-Houzel, 2012; Ribeiro et al., 2013). They argue that the mechanical tension generated by the pattern of connectivity of fiber bundles traveling through white matter may account for the observed pattern of cortical surface convolutions. The authors propose the degree of tension, taken as directly proportional to the morphological characteristics of the fiber bundle (i.e., axonal length and average cross-sectional area, and the proportion of efferent neurons), determines how much the cortical surface folds inwards.
最近，Herculano-Houzel 及其同事发现，连接性和皮质折叠在不同物种之间直接相关，基于基于白质机制的简单模型可能解释了灵长类动物大脑皮层皮层折叠增加的原因（Herculano-Houzel et al.， 2010;Mota 和 Herculano-Houzel，2012 年;Ribeiro et al.， 2013）。他们认为，由穿过白质的纤维束的连接模式产生的机械张力可以解释观察到的皮层表面卷积模式。作者提出了张力程度，与纤维束的形态特征（即轴突长度和平均横截面积，以及传出神经元的比例）成正比，决定了皮质表面向内折叠的程度。
This model is used to explain how surface convolutions vary with brain size and how gray matter thickness varies. Thus, the local wiring and cortical folding is a simple strategy that helps to fit the large sheetlike cortex into a compact space and keeps cortical connections short. An important evolutionary advantage of this design principle is that it enables brains to be more compact and faster with increasing size (Harrison et al., 2002; Karbowski, 2003).
该模型用于解释表面卷积如何随大脑大小变化以及灰质厚度如何变化。因此，局部布线和皮质折叠是一种简单的策略，有助于将大片状皮层放入紧凑的空间并保持皮质连接较短。这种设计原则的一个重要进化优势是，它使大脑随着尺寸的增加而更加紧凑和更快（Harrison 等人，2002 年;Karbowski，2003 年）。
Scaling of the Primate Neocortex 灵长类动物新皮层的缩放
During the past decades considerable progress has been made in explaining the evolution of the cerebral cortex in terms of physical and adaptive principles (see e.g., Macphail and Bolhuis, 2001; Lefebvre, 2012; Roth and Dicke, 2012). In addition, a quantitative approach to the comparative morphology of the brain has made it possible to identify and formalize empirical regularities in the diversity of brain design, especially in the geometry of the cortex (e.g., Hofman, 1989, 2012; Changizi, 2001, 2007; Clark et al., 2001).
在过去的几十年里，从物理和适应原理的角度解释大脑皮层的进化方面取得了相当大的进展（参见例如，Macphail 和 Bolhuis，2001 年;Lefebvre，2012 年;Roth 和 Dicke，2012 年）。此外，大脑比较形态的定量方法使得识别和形式化大脑设计多样性的经验规律成为可能，尤其是在皮层的几何形状中（例如，Hofman，1989、2012;Changizi， 2001， 2007;Clark et al.， 2001）。
Analysis of the cerebral cortex in anthropoid primates, for example, revealed that the volume of the neocortex is highly predictable from absolute brain size (Hofman, 1989; Finlay and Darlington, 1995; Zhang and Sejnowski, 2000; Finlay et al., 2001; Hofman and Falk, 2012). The volume of the cortical gray matter, containing local networks of neurons that are wired by dendrites and mostly non-myelinated axons, is basically a linear function of brain volume, whereas the mass of long-range axons, forming the underlying white matter volume, increases disproportionately with brain size (Figure 3). As a result, the volume of gray matter expressed as a percentage of total brain volume is about the same for all anthropoid primates.
例如，对类人灵长类动物大脑皮层的分析表明，新皮层的体积可以从绝对大脑大小高度预测（Hofman，1989 年;Finlay 和 Darlington，1995 年;Zhang 和 Sejnowski，2000 年;Finlay等人，2001 年;Hofman 和 Falk，2012 年）。皮质灰质的体积，包含由树突连接的神经元的局部网络，主要是无髓轴突，基本上是脑体积的线性函数，而形成底层白质体积的长程轴突质量随着大脑大小的增加而不成比例地增加（图 3）。因此，所有类人灵长类动物的灰质体积（表示为总脑体积的百分比）大致相同。
FIGURE 3
Figure 3. Volumes of cerebral gray and white matter as a function of brain volume in anthropoid primates, including humans. Logarithmic scale. The slopes of the regression lines are 0.985 ± 0.009 (gray matter) and 1.241 ± 0.020 (white matter). Note the difference in the rate of change between gray matter (“neural elements”) and white matter (“neural connections”) as brain size increases. Reproduced with permission from Hofman (2001b).
图 3.包括人类在内的类人灵长类动物的脑灰质和白质体积与脑体积的函数。对数刻度。回归线的斜率为 0.985 ± 0.009（灰质）和 1.241 ± 0.020（白质）。请注意，随着大脑大小的增加，灰质（“神经元素”）和白质（“神经连接”）之间的变化率存在差异。经 Hofman （2001b） 许可转载。
The relative white matter volume, on the other hand, increases with brain size, from 9% in pygmy marmosets (Cebuella pygmaea) to about 35% in humans, the highest value in primates (Hofman, 1989). The non-linear nature of this process is further emphasized by plotting the relative volume of white matter as a function of brain size (Figure 4). The high correlation between both variables ensures that the curve, and its confidence limits, can be used for predictive purposes to estimate the volume of white matter relative to brain volume for a hypothetical primate. The model, for example, predicts a white matter volume of about 1470 cm3 for an anthropoid primate with a brain volume of 3000 cm3 (Hofman, 2001b, 2012). In other words, in such a large brained primate, white matter would comprise about half of the entire brain volume, compared to one-third in modern man.
另一方面，相对白质体积随着大脑大小的增加而增加，从侏儒狨猴 （Cebuella pygmaea） 的 9% 增加到人类的 35% 左右，这是灵长类动物的最高值（Hofman， 1989）。通过将白质的相对体积绘制为大脑大小的函数，进一步强调了这个过程的非线性性质（图 4）。两个变量之间的高度相关性确保曲线及其置信限可用于预测目的，以估计假设灵长类动物相对于脑体积的白质体积。例如，该模型预测脑体积为 3000 cm3 的类人灵长类动物的白质体积约为 1470 cm3（Hofman，2001b，2012）。换句话说，在这样一个大脑巨大的灵长类动物中，白质将占整个大脑体积的一半左右，而现代人的大脑体积只有三分之一。
FIGURE 4
Figure 4. Relative white matter volume as a function of brain volume in anthropoid primates. Semilogarithmic scale. The proportion of white matter increases with brain size, from 22% in a monkey brain of 100 cm3 to about 65% in a hypothetical primate with a brain size of 10,000 cm3. Modified with permission from Hofman (2008).
图 4.相对白质体积与类人灵长类动物脑体积的函数关系。半对数刻度。白质的比例随着大脑大小的增加而增加，从 100 cm3 的猴子大脑中的 22% 增加到大脑大小为 10,000 cm3 的假设灵长类动物的 65% 左右。经 Hofman （2008） 许可修改。
Volumetric measurements of gray and white matter in the neocortex of anthropoid primates have shown that the “universal scaling law” of neocortical gray to white matter applies separately for frontal and non-frontal lobes and that changes in the frontal (but not non-frontal) white matter volume are associated with changes in other parts of the brain, including the basal ganglia, a group of subcortical nuclei functionally linked to executive control (Smaers et al., 2010; Sherwood et al., 2012; Sherwood and Smaers, 2013). These comparative analyses indicate that the evolutionary process of neocorticalization in primates is mainly due to the progressive expansion of the axonal mass that implement global communication, rather than to the increase in the number of cortical neurons and the importance of high neural connectivity in the evolution of brain size in anthropoid primates.
类人灵长类动物新皮层灰质和白质的体积测量表明，新皮层灰质到白质的“通用缩放定律”分别适用于额叶和非额叶，额叶（但不是非额叶）白质体积的变化与大脑其他部分的变化有关，包括基底神经节， 一组功能上与执行控制相关的皮层下核（Smaers等人，2010 年;Sherwood 等人，2012 年;Sherwood 和 Smaers，2013 年）。这些比较分析表明，灵长类动物新皮层化的进化过程主要是由于实现整体通信的轴突质量的逐渐扩大，而不是皮层神经元数量的增加和高度神经连接在类人灵长类动物大脑大小进化中的重要性。
Organization of the Cerebral Cortex 大脑皮层的组织
Evolutionary changes in the cerebral cortex have occurred mainly parallel to the cortical surface (tangentially) and have been sharply constrained in the vertical (radial) dimension, which makes it especially well suited for the elaboration of multiple projections and mapping systems. A mosaic of functionally specialized areas have indeed been found in the mammalian cortex, some of the functions being remarkably diverse (Kaas, 2000, 2008, 2012; Schoenemann, 2006; Krubitzer, 2007; Krubitzer and Dooley, 2013; Ribeiro et al., 2013). At the lower processing levels of the cortex, these maps bear a fairly simple topographical relationship to the world, but in higher areas precise topography is sacrificed for the mapping of more abstract functions. Here, selected aspects of the sensory input are combined in ways that are likely to be relevant to the animal. Human brains, in particular, are distinguished not only by their size but also by a greater proportion of their cortical surface allocated to higher-order association cortex rather than primary sensory and motor areas (Van Essen and Dierker, 2007; Glasser et al., 2013). This observation suggests that relatively more of the human cerebral cortex is dedicated to conceptual as opposed to perceptual and motor processing.
大脑皮层的进化变化主要平行于皮层表面（切向）发生，并且在垂直（径向）维度上受到严重限制，这使得它特别适合于多个投影和映射系统的阐述。在哺乳动物皮层中确实发现了功能特化区域的马赛克，其中一些功能非常多样化（Kaas，2000、2008、2012;Schoenemann， 2006;Krubitzer，2007 年;Krubitzer 和 Dooley，2013 年;Ribeiro et al.， 2013）。在皮层的较低处理水平上，这些地图与世界有着相当简单的地形关系，但在更高的区域，为了绘制更抽象的功能，牺牲了精确的地形。在这里，感觉输入的选定方面以可能与动物相关的方式组合在一起。特别是人类大脑，其特点不仅在于它们的大小，还在于其皮层表面的更大比例分配给高阶关联皮层，而不是初级感觉和运动区域（Van Essen 和 Dierker，2007 年;Glasser et al.， 2013）。这一观察表明，人类大脑皮层的相对更多区域专门用于概念，而不是感知和运动处理。
Using modern anatomical tracing methods, physiological recordings and mapping studies it has been established that each sensory modality is mapped several times in different areas, with about a dozen representations of the visual world and a half a dozen each of auditory inputs and somatosensory sensations. In fact, the maps differ in the attributes of the stimulus represented, in how the field is emphasized, and in the types of computations performed. Clearly, the specifications of all these representations means that functional maps can no longer be considered simply as hard-wired neural networks. They are much more flexible than previously thought and are continually modified by feedback and lateral interactions. These dynamic changes in maps, which seem likely to result from local interactions and modulations in the cortical circuits, provide the plasticity necessary for adaptive behavior and learning. Although species vary in the number of cortical areas they posses, and in the patterns of connections within and between areas, the structural organization of the primate neocortex is remarkably similar.
使用现代解剖学追踪方法、生理记录和映射研究，已经确定每种感觉模式在不同区域被多次映射，大约有十几种视觉世界的表现形式，以及听觉输入和体感感觉各六种。事实上，这些映射在所表示的刺激的属性、场的强调方式以及执行的计算类型方面有所不同。显然，所有这些表示的规范意味着函数映射不能再简单地被视为硬连线神经网络。它们比以前认为的要灵活得多，并且会通过反馈和横向交互不断修改。地图中的这些动态变化似乎可能是由皮层回路中的局部相互作用和调制引起的，为适应性行为和学习提供了必要的可塑性。尽管物种拥有的皮层区域数量以及区域内和区域之间的连接模式各不相同，但灵长类动物新皮层的结构组织非常相似。
Cortical Network Circuitry 皮质网络电路
The tremendous increase in the cortical surface without a comparable increase in its thickness during mammalian evolution has been explained in the context of the radial-unit hypothesis of cortical development (for reviews, see Rakic, 2007, 2009). According to this model, neocortical expansion is the result of changes in proliferation kinetics that increase the number of radial columnar units without changing the number of neurons within each unit significantly. Therefore the evolutionary expansion of the neocortex in primates is mainly the result of an increase in the number of radial columns.
在哺乳动物进化过程中，皮层表面的巨大增加而其厚度没有相应的增加，这已经在皮层发育的桡骨单位假说的背景下进行了解释（有关评论，请参见 Rakic，2007,2009）。根据该模型，新皮层扩张是增殖动力学变化的结果，它增加了放射状柱状单位的数量，而没有显着改变每个单位内的神经元数量。因此，灵长类动物新皮层的进化扩张主要是径向柱数量增加的结果。
The widespread occurrence of these neocortical columns, furthermore, qualifies them to be considered as fundamental building blocks in neural evolution (Mountcastle, 1997; Rockland, 2010; Buxhoeveden, 2012). It has become evident that these cortical circuits integrate at higher levels of information processing, as a result of the hierarchical organization of the brain, thus enabling the system to combine dissimilar views of the world. It implies that if we seek the neural basis of biological intelligence, including mind-like properties and consciousness, we can hardly localize it in a specific region of the brain, but must suppose it to involve all those regions through whose activity an organism is able to construct an adequate model of its external world, perhaps it may even encompass the entire neo- and subcortical network. Although the details of the interpretation of the columnar organization of the neocortex are still controversial (for recent reviews, see Da Costa and Martin, 2010; Rockland, 2010), it is evident that the potential for brain evolution results not from the unorganized aggregation of neurons but from cooperative association by the self-similar compartmentalization and hierarchical organization of neural circuits and the invention of fractal folding, which reduces the interconnective axonal distances.
此外，这些新皮层柱的广泛出现使它们有资格被认为是神经进化的基本组成部分（Mountcastle，1997 年;Rockland， 2010;Buxhoeveden，2012 年）。很明显，由于大脑的等级组织，这些皮层回路在更高层次的信息处理中集成，从而使系统能够结合不同的世界观。这意味着，如果我们寻求生物智能的神经基础，包括类似心智的特性和意识，我们几乎无法将其定位在大脑的特定区域，但必须假设它涉及有机体能够通过其活动构建其外部世界的适当模型的所有区域，也许它甚至可能包括整个新皮层和皮层下网络。尽管对新皮层柱状组织的解释细节仍然存在争议（有关最近的评论，请参见 Da Costa 和 Martin，2010 年;Rockland， 2010），很明显，大脑进化的潜力不是来自神经元的无组织聚集，而是来自神经回路的自相似区室化和分层组织以及分形折叠的发明的合作关联，这减少了互连轴突距离。
Comparative studies furthermore indicate that variability in subtle subcomponents of the columnar organization in human and non-human primates, such as the composition of the interneuron subtypes, are a primary source of interspecific differences in minicolumn morphology among species (Raghanti et al., 2010; Sherwood et al., 2012). Humans deviate from other primates in having a greater width of minicolumns in specific cortical areas, especially in the prefrontal cortex, owing to constituents of the peripheral neuropil space (Buxhoeveden and Casanova, 2002; Semendeferi et al., 2011). These findings support the idea that human evolution, after the split from the common ancestor with chimpanzees, was accompanied by discrete modifications in local circuitry and interconnectivity of selected parts of the brain (see e.g., Semendeferi et al., 2002; Allen, 2009; Teffer and Semendeferi, 2012). The differences in columnar diameter among primates, however, is only minor compared to the dramatic variation in overall cortex size. Thus it seems that the main cortical change during evolution has presumably been an increase in the number, rather than the size of these neural circuits.
比较研究进一步表明，人类和非人类灵长类动物柱状组织的细微亚组分的可变性，例如中间神经元亚型的组成，是物种间小柱形态种间差异的主要来源（Raghanti等人，2010 年;Sherwood et al.， 2012）。由于周围神经细胞空间的成分，人类与其他灵长类动物的不同之处在于，在特定皮层区域，特别是在前额叶皮层中，具有更大宽度的迷你柱（Buxhoeveden 和 Casanova，2002 年;Semendeferi et al.， 2011）。这些发现支持这样一种观点，即人类进化在从黑猩猩的共同祖先中分离出来后，伴随着局部电路的离散改变和大脑选定部分的互连性（参见例如，Semendeferi 等人，2002 年;Allen，2009 年;Teffer 和 Semendeferi，2012 年）。然而，与整体皮层大小的巨大变化相比，灵长类动物之间柱状直径的差异只是微小的。因此，似乎进化过程中的主要皮层变化可能是这些神经回路数量的增加，而不是大小的增加。
Cortical Circuits: Architecture and Wiring 皮质回路：架构和布线
The evolutionary expansion of the neocortex in primates, as we have seen, is mainly the result of an increase in the number of radial columns, of which the architecture may have been under selective evolutionary pressure in different mammalian lineages in response to encephalization and specializations of cognitive abilities. We are beginning to understand some of the geometric and biophysical constraints that have governed the evolution of these neural networks (see e.g., Chklovskii et al., 2002; Klyachko and Stevens, 2003; Laughlin and Sejnowski, 2003; Rockland, 2010). To operate efficiently within these constraints, nature has optimized the structure and function of these processing units with design principles similar to those used in electronic devices and communication networks. In fact, the basic structural uniformity of the cerebral cortex suggests that there are general architectural principles governing its growth and evolutionary development (Cherniak, 1995, 2012; Rakic, 1995; Hofman, 2001a, 2007).
正如我们所看到的，灵长类动物新皮层的进化扩张主要是径向柱数量增加的结果，其中的结构可能在不同的哺乳动物谱系中受到选择性进化压力，以响应脑化和认知能力的专业化。我们开始了解控制这些神经网络进化的一些几何和生物物理约束（参见 Chklovskii 等人，2002 年;Klyachko 和 Stevens，2003 年;Laughlin 和 Sejnowski，2003 年;Rockland，2010 年）。为了在这些限制下有效运行，大自然使用类似于电子设备和通信网络中使用的设计原则优化了这些处理单元的结构和功能。事实上，大脑皮层的基本结构一致性表明，有一般的结构原则支配着它的生长和进化发展（Cherniak， 1995， 2012;Rakic， 1995;Hofman，2001a，2007 年）。
Recent studies in primates have shown that the number of neurons underneath a unit area of cortical surface is not constant and varies linearly with neuronal density, a parameter that is neither related to cortical size nor to the total number of neurons (Herculano-Houzel et al., 2008; Wang et al., 2008; Herculano-Houzel, 2009). These studies indicate that the cortical column varies both in size and number of neurons, which is in accordance with predictions based on computational models (Hofman, 1985b). Indeed, comparative morphological differences between cortical areas and species cast doubt on the notion of a universal cortical module or minicolumn (DeFelipe et al., 2002). Furthermore, a review of extrinsic thalamocortical and intrinsic excitatory pathways in the rodent barrel cortex by Feldmeyer (2012), shows that neurons and their interconnections are not static but are dynamically regulated by behavioral state and synaptic plasticity (see also Budd and Kisvárday, 2012).
最近对灵长类动物的研究表明，皮层表面单位面积下的神经元数量不是恒定的，并且与神经元密度呈线性变化，该参数与皮层大小或神经元总数无关（Herculano-Houzel et al.， 2008;Wang et al.， 2008;Herculano-Houzel，2009 年）。这些研究表明，皮层柱的大小和神经元数量都不同，这与基于计算模型的预测一致（Hofman，1985b）。事实上，皮层区域和物种之间的比较形态差异对通用皮层模块或迷你柱的概念提出了怀疑（DeFelipe et al.， 2002）。此外，Feldmeyer （2012） 对啮齿动物桶皮层中外源性丘脑皮层和内源性兴奋性通路的回顾表明，神经元及其互连不是静态的，而是受行为状态和突触可塑性动态调节的（另见 Budd 和 Kisvárday，2012 年）。
Principles of Neural Wiring 神经布线的原理
Studies in mammals have shown that in species with convoluted brains the mass of interconnective nerve fibers, forming the underlying white matter, is proportional to the 1.28 power of brain volume (Hofman, 1988, 1991), meaning that the cortical white matter is a fractal system. As a result, the total cortical surface area, including all gyri and sulci, scales approximately as the 2/3 power of the white matter volume.
对哺乳动物的研究表明，在具有迂回大脑的物种中，构成底层白质的相互连接神经纤维的质量与脑体积的 1.28 次方成正比（Hofman，1988,1991），这意味着皮质白质是一个分形系统。因此，总皮质表面积，包括所有脑回和脑沟，大约为白质体积的 2/3 次方。
In other words, the surface area of the cerebral cortex, and with that the total number of cortical columns, is geometrically similar with the amount of white matter, i.e., with the number and length of the interconnective nerve fibers. In small species with non-convoluted brains a similar relationship was found between the cortical surface area and the mass of myelinated nerve fibers (Hofman, 1991, see also Hofman, 2012). A fractal dimension of D = 2.70, as found for convoluted brains (Mandelbrot, 1982; Hofman, 1991), suggests a high degree of parallel processing to take place in the cerebral cortex and emphasizes the processing and/or transfer of information across cortical regions in highly corticalized mammals, such as monkeys and apes, rather than within regions. To reach the state of integral parallelism in which each neural component has its own terminal, the length and number of the interconnective axons must be reduced in order to set limits to the axonal mass.
换句话说，大脑皮层的表面积以及皮质柱的总数在几何上与白质的数量相似，即与互连神经纤维的数量和长度相似。在具有非卷曲大脑的小物种中，在皮质表面积和有髓神经纤维的质量之间发现了类似的关系（Hofman，1991 年，另见 Hofman，2012 年）。D = 2.70 的分形维数，如卷曲大脑所发现的（Mandelbrot，1982 年;Hofman， 1991）表明大脑皮层中发生高度的并行处理，并强调在高度皮层化的哺乳动物（如猴子和猿类）的皮层区域之间而不是区域内跨皮层区域处理和/或传递信息。为了达到每个神经成分都有自己的末端的积分平行状态，必须减少互连轴突的长度和数量，以便对轴突质量设置限制。
Therefore the most obvious problem imposed by large brains is increasing distances among the neuronal somata of functionally related regions and the inevitable lengthening of their essential communication lines, the axons. Importantly, the axonal length and volume increase much more rapidly than the number of neurons. Furthermore, a proportional increase of neurons and connections would inevitably lead to a rapid increase of synaptic path length, defined as the average number of monosynaptic connections in the shortest path between two neurons (Watts and Strogatz, 1998; Buzsáki and Draguhn, 2004; Sporns et al., 2004). So that the path length can be maintained, short cut connections can be inserted, resulting in small-world- and scale-free-type networks (Sporns et al., 2007; Bullmore and Sporns, 2012).
因此，大大脑带来的最明显的问题是功能相关区域的神经元胞体之间的距离增加，以及它们的基本通信线（轴突）不可避免地延长。重要的是，轴突长度和体积的增加速度比神经元的数量快得多。此外，神经元和连接的比例增加将不可避免地导致突触路径长度的快速增加，突触路径长度定义为两个神经元之间最短路径中单突触连接的平均数量（Watts 和 Strogatz，1998 年;Buzsáki 和 Draguhn，2004 年;Sporns et al.， 2004）。为了保持路径长度，可以插入短切连接，从而产生小世界和无标度类型的网络（Sporns et al.， 2007;Bullmore 和 Sporns，2012 年）。
Although such a solution can effectively decrease path length within the neocortex, the increased lengths of the axons and the associated increased travel time of the action potentials still pose serious problems. As compensation for these excessive delays, axon caliber and myelination should be increased (Innocenti et al., 2013). An indication that larger brains deploy both more shortcuts (long-range connections) and larger-caliber axons is that the volume of the white matter increased at 4/3 power of the volume of gray matter during the course of evolution. Although the white matter occupies only 6% of the neocortical volume in hedgehogs, it exceeds 40% in humans (Hofman, 1988; Herculano-Houzel, 2009).
尽管这种解决方案可以有效地减少新皮层内的路径长度，但轴突长度的增加和相关的动作电位传播时间的增加仍然会带来严重的问题。作为对这些过度延迟的补偿，应增加轴突口径和髓鞘形成（Innocenti等人，2013 年）。较大的大脑同时部署更多捷径（长距离连接）和更大口径轴突的一个迹象是，在进化过程中，白质的体积以灰质体积的 4/3 的幂增加。虽然白质在刺猬体内仅占新皮层体积的 6%，但在人类中超过 40%（Hofman，1988 年;Herculano-Houzel，2009 年）。
Wen and Chklovskii (2005) have shown that the competing requirements for high connectivity and short conduction delay may lead naturally to the observed architecture of the mammalian neocortex. Obviously, the brain functionally benefits from high synaptic connectivity and short conduction delays. A magnetic resonance imaging study, furthermore, focusing specifically on the prefrontal cortex, has shown that the volume of the white matter underlying prefrontal areas is disproportionately larger in humans than in other primates (Schoenemann et al., 2005). It suggests that the connectional elaboration of the prefrontal cortex, which mediates such important behavioral domains as planning, aspects of language, attention and social and temporal information processing, has played a key role in human brain evolution.
温 和 Chklovskii （2005） 已经表明，对高连接性和短传导延迟的竞争要求可能自然导致观察到的哺乳动物新皮层的结构。显然，大脑在功能上受益于高突触连接和短传导延迟。此外，一项专门针对前额叶皮层的磁共振成像研究表明，人类前额叶区域下方的白质体积比其他灵长类动物大得多（Schoenemann et al.， 2005）。它表明，前额叶皮层的联系阐述在人脑进化中发挥了关键作用，前额叶皮层介导了计划、语言方面、注意力以及社会和时间信息处理等重要行为领域。
Although the frontal lobe as a whole has not been differentially enlarged throughout human evolution (Semendeferi and Damasio, 2000; Teffer and Semendeferi, 2012), there is increasing evidence for its reorganization, as some regions with known functional correlates are either bigger or smaller in the human brain than expected when compared with the same region in great apes. Comparative studies, for example, suggest that the human prefrontal cortex differs from that of closely related primate species less in relative size than it does in organization (for a review, see Teffer and Semendeferi, 2012). Specific reorganizational events in neural circuitry may have taken place either as a consequence of adjusting to increases in size or as adaptive responses to specific selection pressures. It appears that the evolution of the human brain was accompanied by discrete modifications in local circuitry and interconnectivity of selected parts of the brain and that these species-specific adaptations may effect these parts differently (Striedter, 2005; Schoenemann, 2006). But the similarity in brain design among primates, including humans, indicates that brain systems among related species are internally constrained and that the primate brain could only evolve within the context of a limited number of potential forms.
尽管在整个人类进化过程中，额叶作为一个整体并没有被差异性地扩大（Semendeferi 和 Damasio，2000 年;Teffer 和 Semendeferi，2012 年），有越来越多的证据表明它的重组，因为与类人猿的相同区域相比，一些具有已知功能相关性的区域在人脑中比预期的要大或小。例如，比较研究表明，人类前额叶皮层与密切相关的灵长类动物的皮层在相对大小上的差异小于在组织上的差异（有关评论，请参阅 Teffer 和 Semendeferi，2012 年）。神经回路中的特定重组事件可能是由于适应大小增加的结果或作为对特定选择压力的适应性反应而发生的。似乎人脑的进化伴随着局部电路的离散改变和大脑选定部分的互连性，并且这些物种特异性的适应可能会对这些部分产生不同的影响（Striedter，2005 年;Schoenemann，2006 年）。但是，包括人类在内的灵长类动物大脑设计的相似性表明，相关物种之间的大脑系统受到内部限制，灵长类动物的大脑只能在有限数量的潜在形式的情况下进化。
Neocortical Wiring 新皮质布线
In the neocortex, billions of neurons are interconnected via a massive yet highly organized network of axonal and dendritic wiring. This wiring enables both near and distant neurons to coordinate their responses to external stimulation. Specific patterns of cortical activity generated within this network have been found to correlate with cognitive and perceptual functions (Wang, 2010). Understanding the organizing principles of cortical wiring, therefore, represents a central goal toward explaining human cognition and perception in health and disease. Despite more than a century of endeavor, however, the organizing principles and function of cortical connectivity are not well understood (see e.g., Douglas and Martin, 2004; Bohland et al., 2009; Budd and Kisvárday, 2013)
在新皮层中，数十亿个神经元通过一个庞大但高度组织化的轴突和树突布线网络相互连接。这种连接使近处和远处的神经元能够协调它们对外部刺激的反应。已发现该网络内产生的皮层活动的特定模式与认知和感知功能相关（Wang，2010）。因此，了解皮质布线的组织原理代表了解释人类对健康和疾病的认知和感知的中心目标。然而，尽管经过一个多世纪的努力，皮层连接的组织原理和功能仍未得到很好的理解（参见例如，Douglas 和 Martin，2004 年;Bohland 等人，2009 年;Budd 和 Kisvárday，2013 年）
Recent network studies, using diffusion tensor imaging (DTI), have demonstrated that not only the neurons in the neocortex are structurally and functionally highly organized, but that it also holds for the wiring of the brain (Van den Heuvel and Sporns, 2011; Wedeen et al., 2012). The interconnecting white matter axonal pathways are not a mass of tangled wires, as thought for a long time, but they form a rectilinear three-dimensional grid continuous with the three principal axes of development. The topology of the brain’s long-range communication network looks like a 3-D chess board with a number of highly connected neocortical and subcortical hub regions. Structural connectivity networks, as defined by DTI, have identified a common hub in the medial parietal cortex of humans, chimpanzees, and macaque monkeys. However, the apparent lack of medial prefrontal hubs in humans that are present in chimpanzees and macaque monkeys, coupled with evidence of increased gyrification in human prefrontal cortex, suggests important evolutionary changes in the connectivity of human prefrontal cortex (Preuss, 2011; Li et al., 2013; for a review, see Rilling, 2014).
最近使用弥散张量成像 （DTI） 的网络研究表明，不仅新皮层中的神经元在结构和功能上高度组织化，而且它也适用于大脑的布线（Van den Heuvel 和 Sporns，2011 年;Wedeen et al.， 2012）。相互连接的白质轴突通路并不像长期以来认为的那样是一团缠结的电线，而是形成一个与三个发展主轴连续的直线三维网格。大脑远程通信网络的拓扑结构看起来像一个 3-D 棋盘，有许多高度连接的新皮层和皮层下枢纽区域。DTI 定义的结构连接网络已经在人类、黑猩猩和猕猴的内侧顶叶皮层中确定了一个共同的枢纽。然而，人类明显缺乏黑猩猩和猕猴中存在的内侧前额叶枢纽，再加上人类前额叶皮层回旋增加的证据，表明人类前额叶皮层连接性发生了重要的进化变化（Preuss，2011 年;Li et al.， 2013;有关评论，请参阅 Rilling，2014 年）。
The competing requirements for high connectivity and short conduction delay may lead naturally to the observed architecture of the human neocortex. Obviously, the brain functionally benefits from high synaptic connectivity and short conduction delays. The design of the primate brain is such that it may perform a great number of complex functions with a minimum expenditure of energy and material both in the performance of the functions and in the construction of the system. In general there will be a number of adequate designs for an object, which, for practical purposes, will all be equivalent.
对高连接性和短传导延迟的竞争要求可能自然而然地导致了观察到的人类新皮层结构。显然，大脑在功能上受益于高突触连接和短传导延迟。灵长类动物大脑的设计使其可以在功能执行和系统构建方面以最少的能量和材料消耗执行大量复杂的功能。一般来说，一个对象会有许多适当的设计，而实际上，这些设计都是等效的。
We have shown that in species with convoluted brains the fraction of mass devoted to wiring seems to increase much slower than that needed to maintain a high degree of connectivity between the neural networks (Hofman, 2007, 2012). These findings are in line with a model of neuronal connectivity (Deacon, 1990; Ringo, 1991) which says that as brain size increases there must be a corresponding fall in the fraction of neurons with which any neuron communicates directly. The reason for this is that if a fixed percentage of interconnections is to be maintained in the face of increased neuron number, then a large fraction of any brain size increase would be spent maintaining such degree of wiring, while the increasing axon length would reduce neural computational speed (Ringo et al., 1994). The human brain, for example, has an estimated interconnectivity of the order of 103, based on data about the number of modular units and myelinated nerve fibers (Hofman, 2012). This implies that each cortical module is connected to a thousand other modules, and that the mean number of processing steps, or synapses, in the path interconnecting these modules, is about two.
我们已经表明，在大脑复杂的物种中，用于布线的质量分数的增加速度似乎比维持神经网络之间高度连接所需的质量要慢得多（Hofman，2007,2012）。这些发现与神经元连接的模型一致（Deacon，1990 年;Ringo， 1991），该研究指出，随着大脑大小的增加，与任何神经元直接通信的神经元的比例必须相应下降。这样做的原因是，如果要在神经元数量增加的情况下保持固定百分比的互连，那么任何大脑大小增加的很大一部分将用于维持这种程度的布线，而增加的轴突长度会降低神经计算速度（Ringo et al.， 1994）。例如，根据有关模块化单元和有髓神经纤维数量的数据，人脑的互连性估计为 103 左右（Hofman，2012）。这意味着每个皮层模块都连接到一千个其他模块，并且在互连这些模块的路径中，处理步骤或突触的平均数量约为两个。
Herculano-Houzel et al. (2010) have shown that in primates the mass of the white matter scales linearly across species with its number of non-neuronal cells, which is expected to be proportional to the total length of myelinated axons in the white matter. Decreased connectivity in the brain is compatible with previous suggestions that neurons in the cerebral cortex are connected as a small-world network and should slow down the increase in global conduction delay in cortices with larger numbers of neurons (Sporns et al., 2004, 2007; Wang et al., 2008; Bohland et al., 2009).
Herculano-Houzel 等人（2010 年）表明，在灵长类动物中，白质的质量随非神经元细胞的数量在物种之间呈线性比例，预计这与白质中有髓轴突的总长度成正比。大脑中连接性降低与之前的建议相一致，即大脑皮层中的神经元作为一个小世界网络连接，并且应该减缓神经元数量较多的皮层中全局传导延迟的增加（Sporns 等人，2004 年、2007 年;Wang et al.， 2008;Bohland et al.， 2009）。
Recently, Perin et al. (2013) examined theoretically the role of arbor morphology and neuronal density on the emergence of spatially overlapping clusters of recurrently connected cortical neurons. These clusters are generated by repeatedly applying the common neighbor wiring rule until the network structure stabilizes. In this rule the probability of connection between a pair of neurons is proportional to the number of connections they have in common (Perin et al., 2011). The authors report arbor extent limits the size and number of neuronal clusters, which they propose could form innate, elemental cortical groupings.
最近，Perin 等人（2013 年）从理论上研究了心轴形态和神经元密度对空间重叠的反复连接的皮层神经元簇的出现的作用。这些集群是通过重复应用公共邻居布线规则生成的，直到网络结构稳定下来。在这个规则中，一对神经元之间连接的概率与它们共有的连接数量成正比（Perin et al.， 2011）。作者报告说，乔木范围限制了神经元簇的大小和数量，他们认为神经元簇可以形成先天的基本皮质分组。
To group neurons into clusters interacting over relatively short distances allows these groups to inform as many adjacent clusters of neurons about the state of the “emitting” cluster with as little as possible redundancy of information. Figure 5 shows a simple schematic diagram illustrating the effect of increasing the number of functional cortical units on the number of interconnections. When the units are connected to all others by separate fibers and when each additional unit becomes connected with each of the already existing ones, then the number of connections © is related to the number of units (U) according to the equation: C = U (U−1), which is nearly equivalent to C = U2. In such a system the number of connections increases much faster than the number of units. Generally, the growth of connections to units is a factorial function of the number of units in a fully connected network and a linear function of the number of units in a minimally connected network.
将神经元分组为在相对较短距离内相互作用的集群，允许这些集群以尽可能少的信息冗余将“发射”集群的状态通知尽可能多的相邻神经元集群。图 5 显示了一个简单的示意图，说明了增加功能性皮层单元数量对互连数量的影响。当单元通过单独的光纤连接到所有其他单元时，并且当每个附加单元都与每个已经存在的单元连接时，连接数 （C） 与单元数 （U） 相关，根据以下公式：C = U （U-1），这几乎相当于 C = U2。在这样的系统中，连接数的增长速度比单元数的增长速度要快得多。通常，单元连接数的增长是完全连接网络中单元数的阶乘函数和最小连接网络中单元数的线性函数。
FIGURE 5
Figure 5. The problem of network allometry is represented by two neural circuits that exhibit local and global connectivity, respectively. These diagrams depict that the number of bilateral connections © grows much faster than the number of units (U) in a fully connected network: C = U (U−1) than in a binary system, where the growth of connections is a linear function of the number of units. Reproduced with permission from Hofman (2008).
图 5.网络异速生长问题由两个神经回路表示，它们分别表现出局部和全局连接。这些图表描述了在完全连接的网络中，双边连接数 （C） 的增长速度比单元数 （U） 快得多：C = U （U-1） 比在二进制系统中增长，其中连接的增长是单元数的线性函数。经 Hofman （2008） 许可转载。
Once the brain has grown to a point where the bulk of its mass is in the form of connections, then further increases (as long as the same ratio in interconnectivity is maintained) will be unproductive. Increases in number of units will be balanced by decreased performance of those units due to the increased conduction time. This implies that large brains may tend to show more specialization in order to maintain processing capacity. Indeed, an increase in the number of distinct cortical areas with increasing brain size has been reported (Kaas, 2000, 2012; Striedter, 2005). It may even explain why large-brained species may develop some degree of brain lateralization as a direct consequence of size. If there is evolutionary pressure on certain functions that require a high degree of local processing and sequential control, such as linguistic communication in human brains, these will have a strong tendency to develop in one hemisphere.
一旦大脑长到其大部分质量以连接的形式出现的程度，那么进一步增加（只要保持相同的互连比率）将是无益的。由于传导时间增加，单元数量的增加将与这些单元的性能下降相平衡。这意味着大型大脑可能倾向于表现出更多的专业化，以保持处理能力。事实上，据报道，随着大脑大小的增加，不同皮质区域的数量增加（Kaas，2000 年，2012 年;Striedter，2005 年）。它甚至可以解释为什么大脑物种可能会因为体型的直接而发展出某种程度的大脑偏侧化。如果某些功能存在进化压力，需要高度的局部处理和顺序控制，例如人脑中的语言交流，那么这些功能将有很强的倾向在一个半球发展。
Biological Limits to Information Processing 信息处理的生物学限制
Although the cerebral cortex is not the only brain structure which was selected for in evolution to expand, as a result of growing environmental pressure for more sophisticated cognitive abilities, it has played a key role in the evolution of information processing in the mammalian brain. The primate cortex, as we have seen, has evolved from a set of underlying structures that constrain its size, and the amount of information it can store and process. If the ability of an organism to process information about its environment is a driving force behind evolution, then the more information a system, such as the brain, receives, and the faster it can process this information, the more adequately it will be able to respond to environmental challenges and the better will be its chances of survival (Hofman, 2003). The limit to any intelligent system therefore lies in its abilities to process and integrate large amounts of sensory information and to compare these signals with as many memory states as possible, and all that in a minimum of time. It implies that the functional capacity of a neuronal structure is inherently limited by its neural architecture and signal processing time (see e.g., Hofman, 2001a; Laughlin and Sejnowski, 2003; Changizi and Shimojo, 2005).
尽管大脑皮层并不是进化中唯一被选中进行扩展的大脑结构，但由于环境对更复杂的认知能力的压力越来越大，它在哺乳动物大脑信息处理的进化中发挥了关键作用。正如我们所看到的，灵长类动物皮层是从一组限制其大小以及它可以存储和处理的信息量的底层结构进化而来的。如果一个有机体处理有关其环境信息的能力是进化背后的驱动力，那么一个系统（如大脑）接收到的信息越多，它处理这些信息的速度就越快，它就越能充分地应对环境挑战，它的生存机会就越大（霍夫曼， 2003）. 因此，任何智能系统的局限性在于它处理和整合大量感官信息的能力，并将这些信号与尽可能多的记忆状态进行比较，所有这些都是在最短的时间内完成的。这意味着神经元结构的功能能力本质上受到其神经结构和信号处理时间的限制（参见例如，Hofman，2001a;Laughlin 和 Sejnowski，2003 年;Changizi 和 Shimojo，2005 年）。
The processing or transfer of information across cortical regions, rather than within regions, in large-brained primates can only be achieved by reducing the length and number of the interconnective axons in order to set limits to the axonal mass. The number of interconnective fibers can be reduced, as we have seen, by compartmentalization of neurons into modular circuits in which each module, containing a large number of neurons, is connected to its neural environment by a small number of axons. The length of the interconnective fibers can be reduced by folding the cortical surface and thus shortening the radial and tangential distances between brain regions. Local wiring—preferential connectivity between nearby areas of the cortex—is a simple strategy that helps keep cortical connections short. In principle, efficient cortical folding could further reduce connection length, in turn reducing white matter volume and conduction times (Young, 1993; Scannell et al., 1995; Chklovskii et al., 2004; Buzsáki et al., 2013). Thus the development of the cortex does seem to coordinate folding with connectivity in a way that could produce smaller and faster brains.
在大脑灵长类动物中，跨皮层区域而不是区域内的信息处理或传递只能通过减少互连轴突的长度和数量来实现，以便对轴突质量设置限制。正如我们所看到的，通过将神经元划分为模块化电路来减少互连纤维的数量，其中每个模块都包含大量神经元，通过少量轴突连接到其神经环境。可以通过折叠皮质表面来缩短脑区之间的径向和切向距离来减少互连纤维的长度。本地布线（皮层附近区域之间的优先连接）是一种有助于保持皮层连接较短的简单策略。原则上，有效的皮质折叠可以进一步缩短连接长度，进而减少白质体积和传导时间（Young，1993 年;Scannell 等人，1995 年;Chklovskii 等人，2004 年;Buzsáki et al.， 2013）。因此，皮层的发育似乎确实以一种可以产生更小、更快的大脑的方式协调折叠与连接。
Wang et al. (2008) have shown that there are functional trade-offs in white matter axonal scaling in mammals. They found that the composition of white matter shifts from compact, slow-conducting, and energetically expensive unmyelinated axons to large, fast-conducting, and energetically inexpensive myelinated axons. The fastest axons have conduction times of 1–5 ms across the neocortex and <1 ms from the eye to the brain, suggesting that in select sets of communicating fibers, large brains reduce transmission delays and metabolic firing costs at the expense of increased volume. Delays and potential imprecision in cross-brain conduction times are especially great in unmyelinated axons, which may transmit information via firing rate rather than precise spike timing. In the neocortex, axon size distributions can account for the scaling of per-volume metabolic rate and suggest a maximum supportable firing rate, averaged across all axons, of 7 ± 2 Hz. Clearly, the white matter architecture must follow a limited energy budget to optimize both volume and conduction time (for a review, see Buzsáki et al., 2013).
Wang 等人 （2008） 表明，哺乳动物的白质轴突扩展存在功能权衡。他们发现，白质的组成从紧凑、慢传导且能量昂贵的无髓轴突转变为大、快速传导且能量低廉的有髓轴突。最快的轴突在新皮层的传导时间为 1-5 毫秒，从眼睛到大脑的传导时间为 <1 毫秒，这表明在选定的通信纤维组中，大大脑以减少传输延迟和代谢放电成本，但代价是体积增加。跨脑传导时间的延迟和潜在的不精确性在无髓轴突中尤其严重，它可能通过发射速率而不是精确的尖峰时间来传递信息。在新皮层中，轴突大小分布可以解释每体积代谢率的缩放，并表明所有轴突的平均最大可支持放电速率为 7 ± 2 Hz。显然，白质结构必须遵循有限的能量预算，以优化体积和传导时间（有关评论，请参见 Buzsáki 等人，2013 年）。
Another way to keep the aggregate length of axonal and dendritic wiring low, and with that the conduction time and metabollic costs, is to increase the degree of cortical folding. A major disadvantage of this evolutionary strategy, however, is that an increase in the relative number of gyri can only be achieved by reducing the gyral width. At the limit, the neurons in the gyri would be isolated from the remainder of the nervous system, since there would no longer be any opening for direct contact with the underlying white matter. Prothero and Sundsten (1984) therefore introduced the concept of the gyral “window,” which represents the hypothetical plane between a gyrus and the underlying white matter through which nerve fibers running to and from the gyral folds must pass. According to this hypothesis, there would be a brain size where the gyral “window” area has an absolute maximum. A further increase in the size of the brain beyond that point, i.e., at 2800 cm3, would increase the cortical surface area, but the “window” would decrease, leading to a lower degree of neuronal integration and an increase in response time.
另一种保持轴突和树突布线总长度较低的方法是增加皮质折叠的程度。然而，这种进化策略的一个主要缺点是，只有通过减小回宽度才能实现回的相对数量的增加。在极限下，脑回中的神经元将与神经系统的其余部分隔离，因为不再有任何与底层白质直接接触的开口。因此，Prothero 和 Sundsten （1984） 引入了回“窗”的概念，它代表了回和下面的白质之间的假设平面，进出脑回皱襛的神经纤维必须通过该平面。根据这个假设，脑回 “窗口” 区域具有绝对最大值，其中将有一个大脑大小。超过该点后，大脑大小进一步增加，即 2800 cm3，将增加皮质表面积，但“窗口”会减少，导致神经元整合程度降低和响应时间增加。
The remarkably high correlation between gray matter, white matter and brain size in anthropoid primates ensures that the proposed model can be used for predictive purposes to estimate the volume of white matter relative to brain volume for a hypothetical primate (Hofman, 2001b). Model studies of the growth of the neocortex at different brain sizes, using a conservative scenario, revealed that with a brain size of about 3500 cm3 the total volume of the subcortical areas (i.e., cerebellum, brain stem, diencephalon, etc.) reaches a maximum value (Figure 6). Increasing the size of the brain beyond that point, following the same design principle, would lead to a further increase in the size of the neocortex, but to a reduction of the subcortical volume. Consequently, primates with very large brains (e.g., over 5 kg) may have a declining capability for neuronal integration despite their larger number of cortical neurons.
类人灵长类动物的灰质、白质和大脑大小之间的高度相关性确保了所提出的模型可用于预测目的，以估计假设灵长类动物相对于脑体积的白质体积（Hofman，2001b）。使用保守情景对不同大脑大小的新皮层生长的模型研究表明，当大脑大小约为 3500 cm3 时，皮层下区域（即小脑、脑干、间脑等）的总体积达到最大值（图 6）。遵循相同的设计原则，将大脑的大小增加到该点之后，将导致新皮层的大小进一步增加，但会导致皮层下体积的减少。因此，具有非常大的大脑（例如，超过 5 公斤）的灵长类动物尽管皮层神经元数量较多，但神经元整合能力可能会下降。
FIGURE 6
Figure 6. The number of connections ©, cortical processing units (U) and level of interconnectivity (I) in the primate neocortex as a function of brain size. Semi-logarithmic scale. Values are normalized to one at a brain volume of 100 cm3, the size of a monkey brain. Note that the number of myelinated axons increases much faster than the number of cortical processing units (see also Figure 5). The human cerebrum, for example, contains 6 times more myelinated axons than that of a rhesus monkey, whereas the number of cortical processing units is only 3 times larger. Dashed lines show the potential evolutionary pathway of these neural network elements in primates with very large brains, i.e., beyond the hypothetical upper limit of the brain’s processing power (see text and Figure 7). Note that a further exponential growth in the number of cortical processing units, without an increase in the number of connections, will lead to a decrease in connectivity between these units and thus to more local wiring. Reproduced with permission from Hofman (2012).
图 6.灵长类动物新皮层的连接数量 （C）、皮层处理单元 （U） 和互连水平 （I） 与大脑大小的函数关系。半对数刻度。值在 100 cm 3 的脑体积（猴子脑的大小）时标准化为 1。请注意，有髓轴突的数量比皮质处理单元的数量增加得快得多（另见图 5）。例如，人类大脑包含的有髓轴突是恒河猴的 6 倍，而皮质处理单元的数量仅大 3 倍。虚线显示了这些神经网络元素在具有非常大大脑的灵长类动物中的潜在进化途径，即超出了大脑处理能力的假设上限（见文本和图 7）。请注意，皮质处理单元的数量进一步呈指数级增长，而连接数量没有增加，将导致这些单元之间的连接减少，从而导致更多的本地布线。经 Hofman （2012） 许可转载。
Limits to Human Brain Evolution 人脑进化的极限
A progressive enlargement of the hominid brain started about 2.5 million years ago, probably from a bipedal, australopithecine form with a brain size comparable to that of a modern chimpanzee (see e.g., Falk, 2007, 2012; Robson and Wood, 2008; De Sousa and Cunha, 2012; Schoenemann, 2013). Since then, a threefold increase in endocranial volume has taken place, leading to one of the most complex and efficient structures in the animated universe, the human brain. Explanations for the evolution of the human brain are mainly focusing on selection pressures of the physical environment (climate, diet, food availabilty) and those of the social environment (group size, coalition formation, parental care). Although attempts have been made to discriminate between ecological and social theories (see e.g., Leigh, 2004; Dunbar and Shultz, 2007a,b; Lefebvre, 2012; Roth and Dicke, 2012; Willemet, 2013) there has been little effort to develop an explanatory framework that integrates the many social, ecological, and life history correlates of brain size that have been identified. Obviously, they all play a role in explaining the marked differences in brain size between humans and apes, but in which way and to what extent is far from clear at this moment. We will need better studies of cognition and behavior, along with comparative brain studies, to answer these questions.
大约 250 万年前，原始人大脑的逐渐扩大开始，可能是从两足南方古猿形式开始的，其大脑大小与现代黑猩猩相当（参见例如，Falk，2007 年，2012 年;Robson 和 Wood，2008 年;De Sousa 和 Cunha，2012 年;Schoenemann，2013 年）。从那时起，颅内体积增加了三倍，导致了动画宇宙中最复杂、最有效的结构之一，即人脑。对人脑进化的解释主要集中在物理环境（气候、饮食、食物供应）和社会环境（群体规模、联盟形成、父母照顾）的选择压力上。尽管已经尝试区分生态和社会理论（参见例如，Leigh，2004 年;Dunbar 和 Shultz，2007a，b;Lefebvre，2012 年;Roth 和 Dicke，2012 年;Willemet，2013 年）几乎没有努力开发一个解释框架，该框架整合了已确定的许多与大脑大小相关的社会、生态和生活史相关性。显然，它们都在解释人类和猿类之间大脑大小的显着差异方面发挥了作用，但目前尚不清楚以何种方式以及以何种程度存在。我们需要更好的认知和行为研究，以及比较大脑研究，来回答这些问题。
Despite these difficulties in explaining the selection pressures of the evolution of the human brain, comparative neuroimaging studies in primates have identified the underlying neural substrate and unique features of the human brain (for a review see, Rilling, 2014). These studies, for example, have clarified how the dramatic differences in brain size between humans and chimpanzees develop. First, human brains are already twice as large as chimpanzee brains from an early point in gestation (16 weeks). Although both show an increase in growth velocity at this time, they diverge sharply at 22 weeks of gestation, when human brain growth continues to accelerate, whereas chimpanzee brain growth decelerates. Finally, during early infancy, humans experience a very rapid increase in white matter volume that significantly exceeds that found in chimpanzees (see e.g., Sakai et al., 2013).
尽管在解释人脑进化的选择压力方面存在这些困难，但灵长类动物的比较神经影像学研究已经确定了人脑的潜在神经基质和独特特征（有关评论，参见 Rilling，2014 年）。例如，这些研究阐明了人类和黑猩猩之间大脑大小的巨大差异是如何形成的。首先，从妊娠早期（16 周）开始，人类的大脑就已经是黑猩猩大脑的两倍大。尽管此时两者的生长速度都显示增加，但它们在妊娠 22 周时急剧分化，此时人类大脑生长继续加速，而黑猩猩大脑生长减慢。最后，在婴儿早期，人类的白质体积会非常迅速地增加，这大大超过了黑猩猩的白质体积（参见 Sakai 等人，2013 年）。
In view of the central importance placed on brain evolution in explaining the success of our species, one may wonder whether there are physical limits that constrain its processing power and evolutionary potential. The human brain has evolved from a set of underlying structures that constrain its size, and the amount of information it can store and process. In fact, there are a number of related factors that interact to limit brain size, factors that can be divided into two categories: (1) energetic constraints and (2) neural processing constraints (see e.g., Hofman, 2001b, 2012; Wang et al., 2008; Herculano-Houzel, 2009).
鉴于大脑进化在解释我们物种的成功方面具有核心重要性，人们可能会想，是否存在限制其处理能力和进化潜力的物理限制。人脑是从一组限制其大小以及它可以存储和处理的信息量的底层结构演变而来的。事实上，有许多相关因素相互作用以限制大脑大小，这些因素可以分为两类：（1） 能量约束和 （2） 神经处理约束（参见例如，Hofman，2001b，2012;Wang et al.， 2008;Herculano-Houzel，2009 年）。
Energetic Limits 能量极限
The human brain generates about 15 watts (W) in a well insulated cavity of about 1500 cm3. From an engineering point of view, removal of sufficient heat to prevent thermal overload could be a significant problem. But the brain is actively cooled by blood and not simply by heat conduction from the surface of the head. So the limiting factor is how fast the heat can be removed from the brain by blood flow. It has been suggested by Falk (1990) and others that the evolution of a “cranial radiator” in hominids helped provide additional cooling to delicate and metabolically expensive parts of the brain, such as the cerebral cortex. This vascular cooling mechanism would have served as a “prime releaser” that permitted brain size to increase dramatically during human evolution. So, to increase cooling efficiency in a larger brain, either the blood must be cooler when it first enters the structure, or the flow-rate must be increased above current levels.
人脑在大约 1500 cm3 的绝缘良好的腔中产生约 1500 瓦 （W） 的功率。从工程角度来看，去除足够的热量以防止热过载可能是一个重大问题。但是大脑是通过血液主动冷却的，而不仅仅是通过头部表面的热传导。因此，限制因素是血液流动从大脑中带走热量的速度。Falk （1990） 和其他人提出，原始人中“颅辐射器”的进化有助于为大脑中脆弱且代谢昂贵的部分（例如大脑皮层）提供额外的冷却。这种血管冷却机制将作为“主要释放剂”，允许大脑大小在人类进化过程中急剧增加。因此，为了提高较大大脑的冷却效率，血液在首次进入结构时必须较低，或者必须将流速提高到当前水平以上。
Another factor related to blood flow has to do with the increasing energy requirements of a larger brain, a problem that is exacerbated by the high metabolic cost of this organ. It is unlikely, however, that the rate of blood flow or the increasing volume used by the blood vessels in the brain—in human about 4%—constrain its potential size. A bigger brain is metabolically possible because our cardiovascular system could evolve to transport more blood at greater pressure to meet the increased demand. This should not be taken to imply that thermal and metabolic mechanisms play no role at all in setting limits to brain size. Ultimately, energetic considerations will dictate and restrict the size of any neuron-based system, but as theoretical analyses indicate, thermal and metabolic factors alone are unlikely to constrain the potential size of our brain until it has increased to at least ten times its present size (Cochrane et al., 1995).
与血流相关的另一个因素与较大大脑不断增长的能量需求有关，该器官的高代谢成本加剧了这一问题。然而，血流速率或大脑中血管使用的增加体积（在人类中约为 4%）不太可能限制其潜在大小。更大的大脑在代谢上是可能的，因为我们的心血管系统可以进化为在更大的压力下输送更多的血液，以满足增加的需求。这不应被视为意味着热和代谢机制在设定大脑大小的限制方面根本没有作用。最终，能量考虑将决定和限制任何基于神经元的系统的大小，但正如理论分析所表明的那样，仅靠热和代谢因素不太可能限制我们大脑的潜在大小，直到它增加到至少十倍于现在的大小（Cochrane et al.， 1995）。
The same holds for extrinsic developmental constraints that have to do with pelvic anatomy (related to bipedalism), parturition, and maternal and fetal mortality. Although these factors are relevant in human evolution it is unlikely that they are setting limits to human brain growth. In primates, for example, selection for increased brain size is associated with precociality, resulting in a cascade of evolutionary effects including increased birth space and single births, prolonged periods of postnatal development, a proportionate delay in maturation and reproductive rate and, thus, an increase in “generation time” (Leigh, 2004). It means that natural selection operates on brain size at the expense of growth and reproduction, which could explain its correlation with life span (Hofman, 1993). This evolutionary strategy is most obvious when considering the evolution of our own species, where there has been a presumed twofold increase in life span associated with a more than threefold increase in brain size in a mere 2.5 million years (Hofman, 1984). So any further expansion of the adult human brain beyond its present size may take place without a radical change in its fetal/neonatal developmental schedule.
这与盆腔解剖结构（与双足行走有关）、分娩以及孕产妇和胎儿死亡率有关的外在发育限制也是如此。尽管这些因素与人类进化有关，但它们不太可能限制人类大脑的生长。例如，在灵长类动物中，选择增加大脑大小与性早熟有关，导致一连串的进化效应，包括出生空间和单胎增加、出生后发育时间延长、成熟和繁殖率的成比例延迟，因此，“世代时间”增加（Leigh，2004）。这意味着自然选择以牺牲生长和繁殖为代价来作用于大脑大小，这可以解释它与寿命的相关性（Hofman， 1993）。这种进化策略在考虑我们自己物种的进化时最为明显，据推测，在短短 250 万年内，大脑大小的寿命增加了两倍以上，而大脑大小增加了三倍多（Hofman，1984）。因此，成人大脑的任何进一步扩张都可能超过其目前的大小，而不会彻底改变其胎儿/新生儿的发育时间表。
Neural-Processing Limits 神经处理限制
The limit to any neural system lies in its ability to process and integrate large amounts of information in a minimum of time and therefore its functional capacity is inherently limited by its neural architecture and signal processing time. The scaling model of the geometry of the neocortex, for example, predicts an absolute upper limit to primate brain size (Hofman, 2001b; Figure 7). Without a radical change in the macroscopic organization of the brain, however, this hypothetical limit will never be approached, since at that point (ca. 8750 cm3) the brain would consist entirely of cortical neurons, and their interconnections, leaving no space for any other brain structure.
任何神经系统的极限在于它在最短的时间内处理和整合大量信息的能力，因此它的功能能力本质上受到其神经结构和信号处理时间的限制。例如，新皮层几何的缩放模型预测了灵长类动物大脑大小的绝对上限（Hofman， 2001b;图 7）。然而，如果大脑的宏观组织没有根本性的变化，这个假设的极限将永远不会接近，因为在那个时候（约 8750 cm3），大脑将完全由皮层神经元及其互连组成，没有为任何其他大脑结构留下空间。
FIGURE 7
Figure 7. Relative subcortical volume as a function of brain volume. The predicted subcortical volume (i.e., brain volume—predicted neocortex volume) must be zero at zero brain size. Likewise, the subcortical volume will be zero when the brain is exclusively composed of cortical gray and white matter. At a brain size of 3575 cm3 the subcortical volume has a maximum (see also Figure 6). The maximum simulated value for the subcortical volume (366 cm3) is then taken as 100%. The larger the brain grows beyond this critical size, the less efficient it will become. Assuming constant design, it follows that this model predicts an upper limit to the brain’s processing power. Modern humans are at about two-third of that maximum. Modified with permission from Hofman (2001b).
图 7.相对皮质下体积与脑体积的函数关系。在大脑大小为零时，预测的皮层下体积（即脑体积 - 预测的新皮层体积）必须为零。同样，当大脑完全由皮质灰质和白质组成时，皮层下体积将为零。在 3575 cm 3 的大脑大小下，皮层下体积具有最大值（另见 图6）。皮质下体积的最大模拟值 （366 cm 3） 取 100%。大脑长得越大，超过这个临界大小，它的效率就越低。假设设计恒定，因此该模型预测了大脑处理能力的上限。现代人类大约处于这个最大值的三分之二。经 Hofman （2001b） 许可修改。
Cochrane et al. (1995) looked at the different ways in which the brain could evolve to process more information or work more efficiently. They argue that the human brain has (almost) reached the limits of information processing that a neuron-based system allows and that our evolutionary potential is constrained by the delicate balance maintained between conduction speed, duration of the electrical pulse (pulse width), synaptic processing time, and neuron density. By modeling the information processing capability per unit time of a human-type brain as a function of interconnectivity and axonal conduction speed they found that the human brain lies about 20–30% below the optimal, with the optimal processing ability corresponding to a brain about twice the current volume. Any further enhancement of human brain power would require a simultaneous improvement of neural organization, signal processing and thermodynamics. Such a scenario, however, is an unrealistic biological option and must be discarded because of the trade-off that exists between these factors.
Cochrane et al. （1995） 研究了大脑进化以处理更多信息或更有效地工作的不同方式。他们认为，人脑已经（几乎）达到了基于神经元的系统所允许的信息处理极限，我们的进化潜力受到传导速度、电脉冲持续时间（脉冲宽度）、突触处理时间和神经元密度之间保持的微妙平衡的限制。通过将人类大脑每单位时间的信息处理能力建模为互连性和轴突传导速度的函数，他们发现人脑比最佳状态低约 20-30%，最佳处理能力对应于大脑大约是当前体积的两倍。人类脑力的任何进一步增强都需要同时改进神经组织、信号处理和热力学。然而，这种情况是一种不切实际的生物学选择，由于这些因素之间存在权衡，因此必须放弃。
Of course, extrapolations based on brain models, such as the ones presented here, implicitly assume a continuation of brain developments that are on a par with growth rates in the past. One cannot exclude the possibility of new structures evolving in the brain, or a higher degree of specialization of existing brain areas, but within the limits of the existing “Bauplan” there does not seem to be an incremental improvement path available to the human brain. At a brain size of about 3500 cm3, corresponding to a brain volume two to three times that of modern man, the brain seems to reach its maximum processing capacity. The larger the brain grows beyond this critical size, the less efficient it will become, thus limiting any improvement in cognitive power.
当然，基于大脑模型的推断（例如此处介绍的模型）隐含地假设大脑发育的持续性与过去的增长率相当。我们不能排除大脑中新结构进化的可能性，或者现有大脑区域更高程度的专业化的可能性，但在现有的“Bauplan”的限制内，人脑似乎没有可用的渐进式改进路径。在大约 3500 cm3 的大脑大小下，相当于现代人的两到三倍的大脑体积，大脑似乎达到了其最大处理能力。大脑长得越大超过这个临界大小，它的效率就越低，从而限制了认知能力的任何提高。
Concluding Remarks 结束语
The evolution of the neocortex in primates is mainly characterized by the development and multiplication of clusters of neurons which are strongly interconnected and in physical proximity. Since these clusters of neurons are organized in vertical columns, an increase in the number and complexity of the neuronal networks will be reflected by an expansion of the cortical surface area beyond that expected for geometric similar brains. As a result the cortical surface area fractally evolves into a volume with increasing brain size.
灵长类动物新皮层的进化主要以神经元簇的发育和繁殖为特征，这些神经元簇紧密相连且在物理上接近。由于这些神经元簇以垂直列的形式组织，因此神经元网络数量和复杂性的增加将反映为皮层表面积的扩大超出了几何相似大脑的预期范围。结果，皮质表面积分形演变成一个体积，随着大脑尺寸的增加。
It is evident that the potential for brain evolution results not from the unorganized aggregation of neurons but from cooperative association by the self-similar compartmentalization and hierarchical organization of neural circuits and the invention of cortical folding, which reduces the interconnective axonal distances. The competing requirements for high connectivity and short conduction delay may lead naturally to the observed architecture of the primate neocortex. Obviously, the brain functionally benefits from high synaptic connectivity and short conduction delays. The design of the primate brain is such that it may perform a great number of complex functions with a minimum expenditure of energy and material both in the performance of the functions and in the construction of the system. In general there will be a number of adequate designs for an object, which, for practical purposes, will all be equivalent.
很明显，大脑进化的潜力不是来自神经元的无组织聚集，而是来自神经回路的自相似区室化和分层组织以及皮层折叠的发明的合作关联，这减少了互连轴突距离。对高连接性和短传导延迟的竞争要求可能自然地导致了观察到的灵长类动物新皮层的结构。显然，大脑在功能上受益于高突触连接和短传导延迟。灵长类动物大脑的设计使其可以在功能执行和系统构建方面以最少的能量和材料消耗执行大量复杂的功能。一般来说，一个对象会有许多适当的设计，而实际上，这些设计都是等效的。
The similarity in brain design among primates, including humans, indicates that brain systems among related species are internally constrained and that the primate brain could only evolve within the context of a limited number of potential forms. It means that internal factors of brain design may be the primary determinants constraining the evolution of the brain and that geometric similarity among species in the functional organization of the brain may be derived from a common ancestor rather than being immediately evolved in response to specific environmental conditions.
灵长类动物（包括人类）大脑设计的相似性表明，相关物种之间的大脑系统受到内部限制，灵长类动物的大脑只能在有限数量的潜在形式的情况下进化。这意味着大脑设计的内部因素可能是限制大脑进化的主要决定因素，并且大脑功能组织中物种之间的几何相似性可能来自一个共同的祖先，而不是响应特定的环境条件而立即进化。
Conflict of Interest Statement 利益冲突声明
The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
作者声明，该研究是在没有任何可能被解释为潜在利益冲突的商业或财务关系的情况下进行的。
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Keywords: brain evolution, cerebral cortex, cortical design, neural networks, information processing, intelligence, primates, human neocortex
Citation: Hofman MA (2014) Evolution of the human brain: when bigger is better. Front. Neuroanat. 8:15. doi: 10.3389/fnana.2014.00015
Received: 12 December 2013; Accepted: 10 March 2014;
Published online: 27 March 2014.
Edited by:
Suzana Herculano-Houzel, Universidade Federal do Rio de Janeiro, Brazil
Reviewed by:
Danilo Bzdok, Research Center Jülich, Germany
Dean Falk, Florida State University, USA
Jeroen Bert Smaers, Stony Brook University, USA
Copyright © 2014 Hofman. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Michel A. Hofman, Netherlands Institute for Neuroscience, Royal Netherlands Academy of Arts and Sciences, Meibergdreef 47, 1105 BA Amsterdam, Netherlands e-mail: m.hofman@nin.knaw.nl
Disclaimer: All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
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Frontiers | Evolution of the human brain: when bigger is better
https://www.frontiersin.org/journals/neuroanatomy/articles/10.3389/fnana.2014.00015/full
聪明人的大脑有更大更快的神经元
Brains of smarter people have bigger and faster neurons
21 December 2018
Scientists working within the Human Brain Project have for the first time uncovered a direct relation between brain cell size and IQ level. As they describe in the journal eLife, larger neurons in the so-called temporal lobe of the brain that generate electrical signals with higher speed are related to faster processing rates and intelligence level as assessed in standard IQ testing.
在人脑计划中工作的科学家首次发现了脑细胞大小和 IQ 水平之间的直接关系。正如他们在 eLife 杂志中所描述的那样，在所谓的大脑颞叶中以更高的速度产生电信号的较大神经元与标准智商测试中评估的更快的处理速率和智力水平有关。
Our brain works through the activity of its almost 100 billion neurons that each collect, process and pass on information in the form of electrical signals. But so far, not much had been known about how the differences in the properties of these cells from person to person matter for human cognitive abilities like intelligence.
我们的大脑通过其近 1000 亿个神经元的活动来工作，每个神经元都以电信号的形式收集、处理和传递信息。但到目前为止，人们对这些细胞特性的差异在人与人之间有何影响对人类认知能力（如智力）的影响知之甚少。
Some evidence had suggested that the size of so-called dendrites, the long branched out protrusions through which each neuron receives signals from thousands of other cells, might play a role: Especially in brain areas that integrate different types of information, such as the frontal and temporal lobes, brain cells have bigger dendrites. In these brain areas the cortex, where most of the neurons are, is also thicker in people with higher IQ. Theoretical studies additionally predicted that larger dendrites may help cells to initiate electrical signals faster.
一些证据表明，所谓的树突的大小，即每个神经元接收来自数千个其他细胞的信号的长分支突起，可能起到了作用：特别是在整合不同类型信息的大脑区域，如额叶和颞叶，脑细胞的树突更大。在这些大脑区域，大多数神经元所在的皮层在智商较高的人中也更厚。理论研究还预测，较大的树突可能有助于细胞更快地启动电信号。
But because of the very difficult access to human living neurons it was an open question until now whether any of these cellular properties could be proven to actually relate to human intelligence.
但是，由于很难获得人类活的神经元，直到现在，这些细胞特性中的任何一个是否可以证明真的与人类智能有关，这仍然是一个悬而未决的问题。
A collaboration of basic neuroscientists at the Free University Amsterdam with neurosurgeons and clinical psychologists at Amsterdam University Medical Center now made it possible to find out whether smarter brains are indeed better equipped with faster and bigger cells. “The study is the first to take the single cell perspective and link cellular properties to human intelligence”, explains senior author Prof. Huib Mansvelder, an expert for cellular neuroscience who is working within the Human Brain Project.
阿姆斯特丹自由大学的基础神经科学家与阿姆斯特丹大学医学中心的神经外科医生和临床心理学家合作，现在可以发现更聪明的大脑是否确实拥有更快、更大的细胞。“这项研究是第一个从单细胞的角度将细胞特性与人类智能联系起来的研究”，资深作者、在人脑项目中工作的细胞神经科学专家 Huib Mansvelder 教授解释说。
The Dutch team studied 46 people who needed surgery for brain tumors or epilepsy. Each patient took an IQ test before the operation, as part of a presurgery assesment. To access the diseased part deep in the brain, surgeons commonly have to remove small undamaged samples of temporal lobe. These samples still contained living cells that the scientists studied. Both the size and dendritic complexity of the cells, as well as their electrical signals – so called action potentials – were measured in the lab and compared with the IQ scores.
荷兰团队研究了 46 名需要手术治疗脑瘤或癫痫的人。作为术前评估的一部分，每位患者在手术前都进行了 IQ 测试。为了进入大脑深处的患病部分，外科医生通常必须取出小的未受损颞叶样本。这些样本仍然包含科学家研究的活细胞。细胞的大小和树突状复杂性，以及它们的电信号（所谓的动作电位）都在实验室中测量，并与 IQ 分数进行比较。
Summary of the approach: The scientist were able to collect an information-rich multidimensional data set from human subjects including single cell physiology, neuronal morphology, MRI and IQ test scores. The area of the brain highlighted in blue indicates the location of cortical thickness measurements, The black square indicates the typical origin of resected cortical tissue
方法总结：科学家能够从人类受试者中收集信息丰富的多维数据集，包括单细胞生理学、神经元形态学、MRI 和 IQ 测试分数。以蓝色突出显示的大脑区域表示皮质厚度测量的位置，黑色方块表示切除的皮质组织的典型来源
They found that cells from people with higher IQ have longer, more complex dendrites and faster action potentials especially during increased activity. With computational modelling they could also show that neurons with larger dendrites and faster action potentials can process more information coming in and can pass more detailed information on to other neurons.
他们发现，智商较高的人的细胞具有更长、更复杂的树突和更快的动作电位，尤其是在活动增加时。通过计算建模，他们还可以证明具有更大树突和更快动作电位的神经元可以处理更多的传入信息，并且可以将更详细的信息传递给其他神经元。
“Traditionally, research on human intelligence focuses on three main strategies: brain imaging studies of brain structure and function, genetic studies to find genes associated with intelligence, and behavioral psychology”, explains Huib Mansvelder Behavioral psychological studies have shown that higher IQ scores are associated with faster reaction times of subjects. The new findings provide a cellular explanation for this association and links findings from the separate approaches, explaining how identified genes for intelligence can lead to increased cortical thickness, larger neurons as well as faster reaction times in people with higher IQ.
“传统上，人类智力研究侧重于三个主要策略：大脑结构和功能的脑成像研究、寻找与智力相关的基因的遗传研究以及行为心理学”，Huib Mansvelder 解释说。行为心理学研究表明，较高的智商分数与受试者更快的反应时间有关。新发现为这种关联提供了细胞解释，并将来自不同方法的结果联系起来，解释了已识别的智力基因如何导致智商较高的人的皮质厚度增加、神经元变大以及反应时间更快。
Thereby, the study connects levels of organization in the human brain from function of cells to circuits to behavior. “That is one of the major goals for us working together with all these partners from other disciplines of neuroscience in the Human Brain Project, to link the different levels of knowledge about the brain”, the scientist says. Follow-up studies are already planned. “As the IQ number is the summarized result of a wide range of tests, we now have the opportunity to dig into the data and have a closer look at which skills in particular are correlated the most to these cell features.”
因此，该研究将人脑中的组织层次从细胞功能到回路再到行为联系起来。这位科学家说：“这是我们在人脑项目中与来自神经科学其他学科的所有这些合作伙伴合作的主要目标之一，以将有关大脑的不同知识层次联系起来。后续研究已经计划进行中。“由于 IQ 值是各种测试的汇总结果，我们现在有机会深入研究数据并仔细研究哪些技能与这些细胞特征最相关。”
Faster action potentials and bigger dendrites to receive and process more synaptic information may seem like a small difference between neurons. However, since our brain consists of close to 100 billion neurons, this effect rapidly multiplies to a large effect on the computational potential of the brain as a whole: “It’s a small step at the level of a single neuron, a giant leap for the computational power of the brain”, says Mansvelder.
更快的动作电位和更大的树突来接收和处理更多的突触信息，这似乎是神经元之间的一个小差异。然而，由于我们的大脑由近 1000 亿个神经元组成，这种效应迅速成倍增加，对整个大脑的计算潜力产生了很大影响：“这是在单个神经元水平上迈出的一小步，是大脑计算能力的巨大飞跃”，
Publication in eLife:
Large and fast human pyramidal neurons associate with intelligence
Authors: Natalia A. Goriounova, Djai B. Heyer, René Wilbers, Matthijs B. Verhoog, Michele Giugliano, Christophe Verbist, Joshua Obermayer, Amber Kerkhofs, Harriët Smeding, Maaike Verberne, Sander Idema, Johannes C. Baayen, Anton W. Pieneman, Christiaan P.J. de Kock, Martin Klein, Huibert D. Mansvelder.
https://elifesciences.org/articles/41714 , Doi: 10.7554/eLife.41714
Contact:
Prof. Huib Mansvelder
h.d.mansvelder@vu.nl
Prof. Huib Mansvelder heads the Department of Integrative Neurophysiology at the Free University of Amsterdam. His research team is leading in areas like single cell modelling and measurements on living human neurons. In the HBP he contributes to the research area of Human Brain Organization, which studies the complexity of the brain from the level of gene expression and molecules up to the high-level phenomena of cognition.
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Brains of smarter people have bigger and faster neurons
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