Evolutionary Perspective on the Brain

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Evolutionary Perspective on the Brain

GrillnerRobertson16 shows how an evolutionary, comparative perspective, comparing the Lamprey with mammalian basal ganglia structures, provides important insights into the core functionality of these networks. If a core set of mechanisms is strongly conserved over evolutionary time, then it is clear what the "core" functionality of that system is, providing strong guidance for constructing computational models that should certainly capture that core functionality.

It is also noteworthy that this evolutionary perspective is strongly tied to the developmental processes that shape the embryonic brain (e.g., "ontogeny recapitulates phylogeny", at least to some extent). The genetic "knobs" available for evolutionary forces to tweak are principally the duration and location of cell proliferation during embryogenesis, along with various migratory guidance factors that determine who goes where and when -- this is why ontogeny recapitulates phylogeny -- our brains are built up progressively through waves of cell division steps that reflect the branching points of evolutionary choices.

Garcia-CaleroPuelles20 provides an important historical perspective on the field, describing two schools: the orthodox "columnar" approach vs. the heterodox "radial" approach (favored by these authors). The columnar approach is based on coronal slices of adult brains (along arbitrary stereotactic axes), while the radial approach fully embraces the developmental process that is fundamentally "tubular" or radial:

• ventricular is the inside of the tube, superficial is the outer part of the tube
• "vertical" axis: basal (ventral) and roof (dorsal or alar).

This primordial tube then gets tortuously folded in all manner of ways to fit into the physical space available, creating a complex jumble of adjacencies that would be much simpler to understand by unfolding and flattening everything back into its original simple tubular shape:

The radial approach is the attempt to do this unfolding. It has been particularly successful in understanding the jumble of brain areas that constitute the amygdala, which is a core brain structure spanning multiple brain levels.

Also, the telencephelon (where the cerebral cortex is), is a "evagination" that squirts out beyond the primordial subcortical neural tube -- it may have somewhat different rules.

• pallium = dorsal telencephalon = cerebral cortex
• subpallium = ventral telencephalon = basal ganglia

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Garcia-CaleroPuelles20

Garcia-Calero, E., & Puelles, L. (2020). Histogenetic Radial Models as Aids to Understanding Complex Brain Structures: The Amygdalar Radial Model as a Recent Example. Frontiers in Neuroanatomy, 14. https://www.frontiersin.org/articles/10.3389/fnana.2020.590011

See above for overall historical framing. The rest of the paper gets into some deep details that are somewhat hard (for me) to appreciate.

Brain parts having only one FMU, or just a few similarly structured FMUs, are ‘‘simple’’ to explain and understand from a typical partial example (case of the neural retina and cerebellum), whereas regions having many FMUs are as ‘‘complex’’ as the number of FMUs and their respective differential behavior may impose. Nevertheless, such complexes remain amenable to analysis as long as we identify first the involved FMUs and their differential properties (see the case of the pallial amygdala below).

The immature neurons may move radially or tangentially within the histogenetic radial units (or stay put where they are), following different patterns. Such displacements may be reflected ultimately as inside-out or outside-in arrangements of older vs. younger neurons (e.g., the inside-out mammalian isocortex; Angevine and Sidman, 1961; Rakic, 1974; Bayer and Altman, 1991; Noctor et al., 2004 vs. the outside-in mammalian thalamus; McAllister and Das, 1977; Altman and Bayer, 1989). Histogenetic options, in the form of nuclear, layered, or reticular disposition of single or mixed cell types in the mantle stratum of the radial units, are related to multiple combinations of more or less shared (or complementary) adhesion molecules and receptor expression at the surface of the cells. This includes, for example, the large family of cadherin adhesion molecules, which depend on calcium and form homotypic attachments (Figure 5; Yoon et al., 2000; Redies et al., 2001; Stoya et al., 2014: Müller et al., 2004).

Finally, neuronal survival depends on securing appropriate trophic support through connectivity, using axonal navigation to find suitable targets, resulting in efficient synapsis formation with functionally adapted afferents and targets. Such connectivity patterns are controlled by differential genomic readout by each cell type, as a part of their differentiation within the FMU, and make use of the local combinatorial molecular profile.

This confers to the types of synaptic contact they establish specific interactive functional properties acted upon over time by natural selection (producing adaptive fitness). Connections can be established both between different neurons of the same radial histogenetic unit and with neurons of neighboring or distant units. Interestingly, axons seem to be able to distinguish when they pass from one radial unit into another. Some visibly produce collaterals at each unit crossed, or at specific non-sequential units, or generate them only when they reach the main targeted unit (Figure 6). How they do this selecting trick remains obscure (possibly there are local differential signals in the intercellular matrix of each FMU to which axons are sensitive, or there is a local response of the axonal growth cone membrane towards discontinuities in the molecular cell surface epitopes encountered on the glial processes of the different areas). Selective navigation of axons through permissive local environments, and the formation of trophic functional synapses, stabilize the hodological neural structure that interconnects FMUs (Puelles et al., 2008). In this sense, connectivity patterns also depend on relative neurogenetic timing, since depending on its birthdate each neuronal type has a particular sequence of migration and differentiation which opens specific windows of opportunity for establishing correct (biologically useful) connections (Bayer and Altman, 1987).

For instance, the basilar pontine nuclei form after a selective two-step tangential migration from the rhombic lip, while diverse sets of GABAergic subpallial interneurons migrate tangentially indiscriminately into most cortical and nuclear pallial areas. The migrated cells incorporate evolutionarily into the local circuitry of the receiving FMU, presumably under natural selection of resulting improvements in biological fitness. Such tangential migrations are much more common and varied in type than was initially thought 50 years ago (e.g., see some hypothalamic ones reported by Díaz et al., 2015). This property to acquire ectopic fates (perhaps analogous in some molecular aspects to the rich connective properties of axons) adds complexity to the neural histogenetic program (Marín and Rubenstein, 2001; Puelles, 2001; Garcia-Calero, 2005; Puelles et al., 2008; Murillo et al., 2015; Nieuwenhuys and Puelles, 2016; Ruiz-Reig et al., 2018).

• It would be a lot simpler if everyone stayed in their radial lane, but alas, that is not the case..

Amygdala

A consensus model gradually emerged, which described in mammals a phylogenetically primitive central nuclear complex surrounded by supposedly new amygdalar nuclei; a medial nuclear group located in the medial wall of the temporal pole; a basolateral nuclear group (lateral, basal, and accessory basal, later called basomedial) deep to the corticoid structures; and various superficial corticoid masses (anterior, posterolateral, posteromedial). These nuclei were named with regard to their apparent topographical disposition in coronal sections, attending to Nissl staining and chemoarchitectural/immunohistochemical profile

This was historically an unnoticed consequence of disregarding the easily observable fact (in sagittal sections) that most amygdalar nuclei lie rostral to their correlative ventricular surface. There is an obliquity of 45 degrees between the natural (histogenetic) amygdalar radial dimension and the standard coronal sections (widely assumed to be orthogonal to an ideal, non-molecularly defined forebrain axis ending in the telencephalon; Herrick, 1910; Swanson, 2012).

• The amygdala is skewed at a 45 degree angle..

In this sense, the main amygdalar subdivisions distinguished were the basal-ganglia-like (or striatum-like) structures, meaning the classic medial and central amygdala with the intercalated nuclei and the extended amygdala added, and the cortex-like structures, which would encompass the BL and associated corticoid masses. For example, Swanson and Petrovich (1998) emphasized in an influential review the separation of striatum-like and cortex-like moieties of the amygdala based on the predominance of GABAergic vs. glutamatergic cell populations, respectively (notably, this agrees with the developmental distinction of subpallial and pallial moieties).

The mouse amygdala is a droopy mess! From Garcia-Calero et al., 2020;

In summary, neurogenetic data consistently support the existence of an allocortical ring external to the pallial amygdala, which includes the APir as a singular olfactory subarea only present next to the amygdalar border of the allocortical ring. These cortical areas uniformly show an inside-out neurogenetic pattern that contrasts with the uniform amygdalar outside-in stratification pattern of timed birthdates. The results also point to APir and caudal Pir as the most precociously born structures in the allocortical ring.

The present radial model of the pallial amygdala contemplates five main radial units, or macrounits, with a total of nine subdivisions, each displaying (with one exception) periventricular, intermediate and superficial strata, thus representing 27 distinct spatial amygdalar loci believed to have different neuronal populations, all of them differentiable neurogenetically from all bordering allocortical domains.

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MorenoGonzalez07

Moreno, N., & González, A. (2007). Evolution of the amygdaloid complex in vertebrates, with special reference to the anamnio-amniotic transition. Journal of Anatomy, 211(2), 151–163. https://doi.org/10.1111/j.1469-7580.2007.00780.x

Note: probably the best comparative review.

Key term: hodological -> based on pathways of connectivity

The current view of the AC in tetrapods considers pallial and subpallial components. Thus, the ‘pallial amygdala’ comprises derivatives of the lateral and ventral pallium, whereas the ‘subpallial amygdala’ consists of derivatives of the lateral and medial ganglionic eminences (Puelles et al. 2000; Martínez-García et al. 2002; Moreno & González, 2006). This dual origin makes the AC a histogenetic com- plex area, with the morphogenetic and migratory process during development being extremely intense, which increases the complexity of the adult structure in all tetrapods (Puelles et al. 2000). In mammals, the pallial amygdala is composed of a superficial group of nuclei that shows a laminar organization and is called ‘cortical amygdala’ and a deep group of nuclei that form the ‘basolateral amygdala’. In turn, the subpallial amygdala is formed by a striatal component, the central amygdala, and subpallial component, the medial amygdala, which most likely also contains pallial elements (Martínez-García et al. 2002; Medina et al. 2004).

The existence of an AC with components that share embryological origin in all tetrapods has a major implication in the interpretation of the evolution of this structure in that the precursors of the amygdaloid nuclei are already present from anamniotes. In the following sections we will deal with the major characteristics that are now accepted as being shared in the organization of the AC in tetrapods. In addition, we will comment on the recent data from fish suggesting that the AC is recognizable in teleosts, reinforcing the idea that its crucial functional role has been conserved through evolution.

The olfactory system and in particular the olfactory bulbs are extremely conserved in vertebrate evolution in terms of embryological origin, neurochemistry, connectivity and function. In all tetrapods the olfactory bulbs are pallial structures that incorporate subpallial components (Puelles et al. 2000). In particular, the olfactory neurons projecting outside the bulbs are pallial cells, like all projection neurons in the cortex, whereas the interneurons originate in the subpallium. This situation has also been confirmed in anurans, in which the mitral neurons express pallial markers (Moreno et al. 2003), while the interneurons express subpallial markers and are thought to reach the bulbs probably following a migratory process similar to that of amniotes (Smeets & González, 2000; Boyd & Delaney, 2002; Brox et al. 2003) (Fig. 2).

A major part of the amygdala is an integral component of the olfactory and vomeronasal systems of the brain (Swanson & Petrovich, 1998; Halpern & Martínez-Marcos, 2003; Moreno & González, 2006), receiving large olfactory and vomeronasal projections in all tetrapods (Swanson & Petrovich, 1998; Moreno et al. 2005). In fact, the amygdala includes the main secondary vomeronasal and olfactory centres in the brain (Swanson & Petrovich, 1998). Thus, the organization of the main sensory inputs of the amygdala (vomeronasal and olfactory) is extremely conserved, at least in tetrapods, which is striking in view of the evolutionary distance between species.

• Note: vomeronasal = liquid, pheromone chemosensation. Basically, olfaction is the most ancient and important sensory modality, and amygdala evolved as a secondary processing area on top of this basic sensory pathway.

In their review of the organization of the AC of mammals into functional systems, Swanson & Petrovich (1998) proposed the existence of two distinct multisensorial systems: the frontotemporal amygdaloid system and a main olfactory amygdaloid system. However, in other vertebrates such a subdivision has not been recognized and it seems more appropriate to consider only one ‘multisensorial amygdala’, which certainly receives major olfactory information but also thalamic and brainstem inputs (Moreno & González, 2006).

In mammals, taken together, the olfactory/multimodal amygdaloid system consists of distinct cortical and deep amygdaloid areas. The cortical areas include the anterior cortical amygdala (CoAa), the posterolateral cortical amygdala (CoApl) and the cortex–amygdala transition area (CxA). In turn, the deep pallial areas (named, as a whole, the basolateral amygdala) include the basolateral (BL), basomedial (BM) and lateral (LA) nuclei (Swanson & Petrovich, 1998). Notably, the lateral nucleus, included in the frontotemporal functional system (Swanson & Petrovich, 1998), is the major sensory receptive area (LeDoux et al. 1990; Savander et al. 1997) and conveys sensory informa- tion to other amygdaloid nuclei for further processing (Pitkänen et al. 1995) and, thus, it is a very important component of the multimodal amygdala strongly implicated in the emotional behaviour (LeDoux, 2000).

• Anurans = frogs

Autonomic amygdala = CeA:

This component of the amygdala, the central amygdala (CeA), constitutes the main integrative centre in the AC. In all tetrapods studied it receives a wide range of sensory information from other amygdaloid regions and ascending thalamic and brainstem inputs. All this information will modulate the behavioural responses that could be the sum of the stimuli from other amygdaloid nuclei.

The identification in all tetrapods of an autonomic amygdala is relatively easy and it seems that homologous components to the mammalian CeA represent a conserved evolutionary entity (Fig. 4). The CeA constitutes a striatal component (in origin) that is an integrative area and possesses long descending projections to autonomic centres (Moreno & González, 2006). In addition, in the different tetrapods it has been involved in mediating many autonomic, somatic, endocrine and behavioural responses. The conservation of this system in evolution is of important significance in that the autonomic amygdala constitutes the link between the environmental stimuli received by the animal and the correct behavioural response based on previous experiences, association of apparently unrelated stimuli, learned behaviours, etc.

Abundant physiological evidence in amniotes indicates that the amygdala profoundly influences a variety of visceromotor responses, as well as the expression of instinctive and conditioned behaviours with a motivational and/or emotional component that could be mediated, at least in part, by projections from the amygdala to the hypothalamus and lower brainstem (Price et al. 1987; LeDoux, 1992; McDonald, 1998; Swanson & Petrovich, 1998). In addition, the strong amygdalo-hypothalamic connections through the stria terminalis constitute one of the impor- tant features of the organization of the amygdaloid system in all tetrapods (Risold et al. 1997; Lanuza et al. 1997, 1998; Martínez-Marcos et al. 1999; Moreno & González, 2005b, 2006). Given its importance, studies regarding the connectivity of the AC in different vertebrates used the analysis of the amygdalo-hypothalamic projections to establish putative homologies among amygdaloid territo- ries. In addition, the precise mode in which the amygdala connects with the hypothalamus is of particular interest in evolutionary studies as it seems to be extremely conserved across tetrapods (Bruce & Neary, 1995; Lanuza et al. 1997, 1998; Martínez-Marcos et al. 1999; Moreno & González, 2005b).

Is there an amygdaloid complex in fish?

The telencephalon of teleosts has a characteristic appear- ance, with solid paired telencephalic lobes separated by a single median and dorsal telencephalic ventricle covered by a dorsal choroid tela.

The amygdaloid area implicated in emotional memory, which seems crucial for survival, most probably evolved before the ancestral amphibians. The existence of an emotional amygdaloid area derived from the latero- ventral pallial areas in fish strongly supports the hypothesis of the current view of the amygdaloid evolution based on recent data in anurans (Moreno & González, 2006) in which the ventral pallial amygdala has been postulated as the multisensorial amygdala implicated in this emotional labelling of stimuli; however, further functional data are needed, at least in anurans.

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YamamotoVernier11

Yamamoto, K., & Vernier, P. (2011). The Evolution of Dopamine Systems in Chordates. Frontiers in Neuroanatomy, 5. https://www.frontiersin.org/articles/10.3389/fnana.2011.00021

• A9 = SNC A10 = VTA,

A11: Similarly, DA cells located in the periventricular gray matter extending from the mesencephalon to p3 are found in many vertebrates, and they may correspond to the A11 group (reviewed in Smeets and González, 2000). In zebrafish, several diencephalic DA cell groups (located in p3 and hypothalamus), have been proposed to be similar to the mammalian A11 cells (DA groups 2, 4, 5, 6; Ryu et al., 2007; reviewed in Schweitzer and Driever, 2009). These posterior tubercular/hypothalamic DA cells in zebrafish require the transcription factor Orthopedia (Otp) as well as Nkx2.1 for their specification, as it is the case for the mouse A11 (Ryu et al., 2007; Löhr et al., 2009). Furthermore, mammalian A11 is characterized by distal projections to the spinal cord, and cells in the periventricular nucleus of posterior tuberculum (TPp) project to the spinal cord in zebrafish (Becker et al., 1997; Tay et al., 2011). These data indicate that these DA cells of zebrafish posterior tuberculum may be equivalent to the A11 of mammals. A11-like catecholaminergic projections to the spinal cord are found in amphibians as well, and the cell bodies are located in p3 and hypothalamic areas (Sanchez-Camacho et al., 2001), similar to the case in zebrafish. The diencephalo-spinal DA projections are also found in lampreys, but these cells are CSF-contacting neurons, unlike in jawed vertebrates. Thus, although diencephalo-spinal DA systems are commonly found throughout the vertebrates, the homology is currently unclear.

The A12 and A14 DA cells (which are respectively located in the arcuate nucleus and periventricular hypothalamic nucleus in rodents) are well studied and known to regulate prolactin, growth hormone (GH) or gonadotrophins, luteinizing hormone (LH), and follicle stimulating hormone (FSH) in the pituitary (Ben-Jonathan and Hnasko, 2001; Thiery et al., 2002; Dufour et al., 2005; Garcia-Tornadu et al., 2010; Zohar et al., 2010).

Not much is known about the function A15 cell populations.

In mammals, a majority of the DA cells of A9 (substantia nigra pars compacta, SNc) are located in the midbrain, as well as a large part of the A10 neurons (ventral tegmental area, VTA). The A8 group corresponds to the retrorubral component of the DA neurons. Similar cell populations are present in reptilian species (Smeets, 1994; Smeets and Reiner, 1994), and as in mammals they extend from the mesencephalon up to the basal part of the two first prosomeres, at least. In amphibians as well, similar nigro-striatal and meso-limbic pathways are identified, but unlike amniotes, the DAergic cells of amphibians are shifted more rostrally, many of them being located in the diencephalic territories. Then, the neurons giving rise to the two main projection fibers are intermingled rather than segregated (Marin et al., 1997). Midbrain DA cells with extension into the diencephalic posterior tuberculum are also found in cartilaginous fishes with two different populations. One, named the tegmental area is located just anterior to the interpeduncular nucleus, and the other, a putative substantia nigra, is scattered around the red nucleus (Stuesse et al., 1994).

In contrast, there is no midbrain DA cell in teleosts (Meek, 1994; Rink and Wullimann, 2001), or in lampreys (Pierre et al., 1997; Barreiro-Iglesias et al., 2008). In representatives of this very large group of species (more than 24,000 species), DA neurons are found at three main locations, the periventricular nucleus of the posterior tuberculum, the paraventricular organ, and the posterior tuberal nucleus, all located in the basal area of the third prosomere.

• OK, so it looks like the lamprey GPh -> LHb -> DA -> system may have been very specific to BG as its origin story?

Midbrain DA input to a proposed nucleus accumbens are found in amphibians, but the receptor distribution is not known.

Conclusion: As previously stated (Kapsimali et al., 2003), the basic role of DA systems has not significantly changed during vertebrate evolution, as far as the molecular and cellular mechanisms are concerned.