Learning Objectives
By the end of this section, you should be able to
- 4.2.1 Explain the concept of homology.
- 4.2.2 Articulate differences in structural organization of the telencephalon of birds and mammals.
- 4.2.3 Explain two opposing views to define homologies across the vertebrate telencephalon.
There are several challenges in comparing the nervous systems of different species. As is evident from Figure 4.2, brain structures are highly diverse.
Comparative neuroscientists use the concept of homology to compare neural structures across species. Homology is a fundamental concept in comparative neuroscience and in biology generally. We will provide examples below. It is the term used to describe structures or organs that evolved from a shared ancestor. Identifying homologous structures may seem easy, especially when considering two closely related species where brain regions appear similar, as is the case in humans and chimpanzees. However, identifying equivalent brain regions becomes increasingly challenging in distantly related species because they share relatively few structural and genetic similarities. In those species that are distantly related, homologies can be controversial.
Comparing neural structures
In this section, we discuss homology and how it is used to compare neural structures in different species. As mentioned above, homologous structures share an evolutionary ancestry. Organ systems can be considered homologous regardless as to their function. One well known example concerns the mammalian forelimbs, which are homologous across mammals. These structures are considered homologous across species because they have similar patterns in bone structure, which reflect their shared ancestry. Yet, forelimbs take on many functions. For example, bats have evolved wings to fly, whales have evolved fins to swim, and horses have long hoofed legs to walk and gallop. Although forelimbs support different functions in different animals, forelimbs are homologous across mammals because the anatomical structures that make up forelimbs are recognizable across mammals and arise from a common ancestor.
Comparative neuroscience typically relies on identifying corresponding brain parts across species. Major anatomical divisions and brain nuclei are considered homologous if these structures emerge from shared ancestry (i.e., homology). While this concept might appear relatively straightforward at first, identifying corresponding brain parts becomes a thorny problem when applied to distantly related species (Striedter, 2005). Scientists seeking to define homologous structures search for shared similarities in traits present in the last common ancestor. But which similarities they focus on can vary. Homologous characters may be neuroanatomical features (e.g., connectivity patterns) or genes expressed by different cell populations in adulthood, but they can also be based on developmental processes such as spatiotemporal patterns of gene expression. Importantly, focusing on developmental or adult phenotypes as a basis for homology can yield different conclusions (Medina and Reiner, 2000; Briscoe, 2019).
In the next section, we will discuss the issue of defining homologies across the brains of birds and mammals as one controversial example. We will discuss how the use of different characters to define homologous structures may lead to different conclusions. We will also discuss this challenging case because it is the investigation of challenging cases that deepens our understanding of homology.
Marked differences in anatomical organization between birds and mammals
As discussed previously, the brain is typically divided into three major regions that can be defined early in development. These are the forebrain, midbrain, and hindbrain. The forebrain is composed of the telencephalon and diencephalon. The telencephalon includes the cerebral cortex and several subcortical structures (e.g., basal ganglia, amygdala, hippocampus) (see Chapter 1 Structure and Function of the Nervous System: Cells and Anatomy). In some species, the cerebral cortex makes up much of the telencephalon. We first discuss the basic features of the mammalian telencephalon before discussing how this basic organization of the mammalian telencephalon differs from that of birds.
The mammalian cerebral cortex consists of grey and white matter (see Chapter 1 Structure and Function of the Nervous System: Cells and Anatomy). The grey matter largely contains cell bodies of neurons and glial cells. The white matter contains glial cells and axons coursing within and across cortical and subcortical structures. In the white matter, many of these axons are surrounded by a fatty sheath called myelin. It is myelin that gives the white matter its white color. In mammals, there is a clear distinction between the white and grey matter with cell bodies of neurons separated from the white matter, which consists of axons. The top half of Figure 4.3 show this segregated organization in a human and a mouse brain, on the left and right respectively.
The grey matter also has a specific organization of interest. The mammalian cerebral cortex grey matter is typically organized into six layers (layers I-VI), shown in a mouse brain on the left side of Figure 4.4. Each cortical layer has a characteristic distribution of neuronal and glial populations with each layer possessing stereotypical patterns of efferent (outgoing) and afferent (incoming) projections.
The basic organization of the mammalian cerebral cortex stands in sharp contrast to the structural organization of the avian telencephalon. At first glance, the telencephalon of birds appears drastically different from mammals. First, whereas the mammalian cerebral cortex consists of grey and white matter, there is no such distinction between grey versus white matter in the avian telencephalon, shown on the bottom of Figure 4.3. Rather, the axons of bird brains course through cell bodies with no segregation between cell bodies and axons. Second, whereas the mammalian cerebral cortex is organized into layers, neurons and glial cells in birds are primarily clustered into nuclei, shown on the right side of Figure 4.4.
The nomenclature to define regions of the avian telencephalon are also distinct from those used in mammals. The avian telencephalon is subdivided into the striatum, and the hyper, meso, and nidopallium. The meso- and nidopallium are organized into nuclei whereas the dorsal pallium has a layered organization, but only consists of at most three layers. These major differences in anatomical structures have contributed to challenges in defining homologies across the telencephalon of birds and mammals.
The differences in structural organization between birds and mammals are accompanied by differences in connectivity patterns, which further complicates the search for homologies. The hyper, meso, and nidopallium of the bird cortex receive input from the thalamus and process sensory information, including visual, somatosensory and auditory information. For example, the hyperpallium receives extensive visual input and the nidopallium processes somatosensory information. In mammals, in contrast, these kinds of sensory inputs project primarily to layer IV neurons spread along the cortical surface. The bottom of Figure 4.4 exemplifies these two organizations.
Some researchers have used connectivity patterns as a tool to define homologies, but others have used other criteria to define homologous structures across the telencephalon of birds and mammals. Depending on what criteria a researcher uses, they can come up with completely different ideas of which structures are homologous in birds and mammals. In the next section, we will learn more about one specific area of uncertainty in this field.
Definition and challenges: comparing bird brains to those of mammals
In this section, we detail conflicting definitions of homologous structures across the mammalian telencephalic structures in birds. Two opposing hypotheses in this debate are illustrated in Figure 4.5. As we will see below, some of the conflicting views here arise depending on which scale of investigation a researcher uses. Recall that scale refers to the biological level of organization. Here, we will see conflicting results between what the macro-scale (connectivity) suggests are homologous structures in birds and mammals and what the micro-scale (developmental gene expression) suggests are homologous structures.
Perspective from connections: Some researchers have focused especially on patterns of afferent and efferent projections in the avian pallium to define homologous structures between the avian and mammalian telencephalon (Karten, 1991). As we discussed above, in mammals, much of the cerebral cortex consists of primary cortical areas that receive extensive thalamic input and process sensory information. Those areas include the primary visual cortex, the primary somatosensory cortex, and the primary auditory cortex (see Chapter 9 Touch and Pain). The avian dorsal ventricular ridge (DVR) contains discrete nuclei (including those of the mesopallium and nidopallium) that receive extensive thalamic input (Butler, 1995; Butler et al., 2000). Researchers have used these insights to argue that the dorsal ventricular ridge of birds is homologous to the mammalian cerebral cortex. This is known as the isocortex-DVR hypothesis.
Perspective from development: Other researchers have reminded the community that homologous structures can take on different functions across species. That is, homology between structures arises from shared ancestry, which may or may not serve the same function across species. Think back to how bat wings fly, whale fins swim, etc. In this case, we are not looking at function. Rather, we are considering the evolutionary origins of populations of cells, an area called field homology. Field homology refers to populations of cells that derive from evolutionary conserved regions but may be populated across diverse morphological structures. Indeed, there are a number of cases where cells are generated in one location and migrate over long distances in the central nervous system (Corbin et al., 2001). Many researchers focus on developmental field homologies to define homologous cell populations. Typically, looking at developmental fields means that researchers focus on transcriptional (gene expression) landscapes in the embryo as a basis for defining homologies. These fields thus represent the basic units for comparisons.
To better understand what we mean when we say we are defining a developmental field, let’s consider transcriptionally defined subdivisions as it applies to defining the homologous structure for the bird DVR in mammals. In this case, researchers have used a combination of genes to transcriptionally define fields (populations of cells that are similar to each other) and define comparable brain regions across species. For example, there are several genes, including Pax6, Tbr1, Nkx-2.1, and Dlx-2 that are expressed in specific locations during development. These genes are expressed in clusters of cells and can be used to define homologous areas because we know of their migratory patterns so we know where they will end up in adulthood. Evaluating spatiotemporal patterns of gene expression during development has been used to argue that the precursors in the DVR give rise to the amygdala in mammals and give rise to nido- and mesopallium in birds (Puelles et al., 2002). Therefore, large regions of the avian telencephalon that might be considered homologous to the cerebral cortex in mammals based on adult connectivity could be considered homologous to the mammalian amygdala when considered based on developmental fields (Striedter, 1994). In this case, consideration of homology based on developmental fields is called the claustroamygdala-DVR hypothesis, which stipulates that mammalian homologues of the DVR consist of the claustrum, endopiriform nuclei, and amygdala (Butler et al., 2012).
Defining homologous structures between species is a crucial effort, as this effort forms the foundation for any comparison between species. We have focused on developmental processes and connectivity patterns as two different ways to identify homologous structures. Researchers who focus on adult patterns of connectivity consider the lateral and ventral pallium to be homologous to the mammalian cortex because the lateral and ventral pallium of birds and the cortex of mammals both receive inputs from sensory thalamus. Researchers who focus on gene expression from a developmental perspective place an emphasis on developmental patterns. In contrast, other researchers may support the notion that the meso and nidopallium in birds are homologous to the mammalian amygdala. This challenging case illustrates the difficulty in defining which features are relevant and should be used as a basis to compare highly divergent brains.