A Brief History Of Brain Evolution

Striking points:

(1) Rudimentary versions of the brainstem, thalamus, basal nuclei, cerebellum, hippocampus, amygdala, and neocortex appeared between 600 and 420 million years ago. Most of these structures first appeared in the fishes.
(2) The brain initially evolved as a motor program system capable of generating more complex movements, then as a temporary memory system able to both "play back" and produce immediate fear-based reactions to certain situations, and finally as a permanent memory system that constructs a model of the world to make predictions about that world.
(3) Regarding the current functions of individual brain structures, the human brainstem generates arousal, reward, and stress necessary for memory formation and immediate survival of the individual, the thalamus mediates arousal and stimulates states of attention necessary for memory formation, the basal nuclei processes context thus ensuring that the most statistically suitable memories for a particular situation are converted into movements and cognitions, the cerebellum times memories to produce practiced, high-level movements and cognitions, the hippocampus encodes and consolidates novelty such that it can learn, store, recall, and transfer temporary memories of new experiences into more permanent storage in the neocortex, the amygdala generates and regenerates emotional states so as to predict the potential stress of an experience and enhance the ability to cope with that stress in the future, and the neocortex constructs an internal model of the world with which it retrieves memories to make predictions about that world which ultimately enhances the long-term survival of the individual.

Opening

This is an exposition on the human brain.

There are two facets to understanding any system (anything with interacting physical parts). First, you must know its structure (how it is arranged internally); if you understand a system´s structure deeply, you should be able to build another system like it. Second, you must know its function (how it interacts with the world); if you understand the system´s function deeply, you should be able to predict what it will do reasonably far into the future. The brain is often considered to be the most complex system in the known universe, yet perhaps much of this apparent complexity is illusory if one avoids getting mired in details; as Jeff Hawkins says, "what we need is a top down theory". I will focus on top-down explanations for the major brain structures, speculating at times.

We must journey back in time before we journey inward.

The Sponge Pinacocyte

We begin our discussion with the phylum Porifera, the sponges. These animals are among the first multicellular organisms in existence, dating back as far as 700 million years ago (Petranyi, 2002). Sponges are full of pores and channels that permit water to circulate within their bodies. However, since they lack true tissues and organs (Fieseler et al, 2004), they have no nervous system (a network consisting of specialized nerve cells, called neurons, that allows an animal to sense and respond to the world).

Although sponges do not possess neurons and thus do not have nervous systems, they still have a limited ability to sense and respond to things. They may be extremely slow at only 1-4 mm per day (Bond and Harris, 1988), but some sponges can crawl across the sea bed as a result of the movements of specialized cells called pinacocytes. These flat cells are located on the outer sponge layers and can expand and contract, allowing the sponge to either move or alter its size. Moreover, the pinacocytes can perform coordinated contractions to remove blockages in their channels, squeezing the water channels and thus expelling foreign substances. The sponge shows us that early animals could sense and respond to the environment prior to the evolution of nervous systems by using their specialized expanding and contracting pinacocytes, although their range of movements was limited.
Sponges are animals that consist mainly of pores and channels that enable water to circulate within their bodies. They have no nervous system.
Since they have no nervous system, sponges use specialized expanding and contracting cells called pinacocytes (yellow outer layer) to alter their size and shape.

The Jellyfish And Starfish Nerve Net

After the sponges appeared the phylums Cnidaria (jellyfish, corals, and sea anemones) and Echinodermata (starfish, sea urchins, and sand dollars). These animals potentially evolved as far back as 700 million years ago (Schwab and Sadun, 2007). The simplest form of nervous system, called a nerve net (a diffuse series of interconnected neurons), developed within both of these groups of animals (Miljkovic-Licina et al, 2004). In general, the neurons in a nerve net are spread far apart. Nerve nets are a feature of animals with radial symmetry - no right or left side.

Jellyfish, from the phylum Cnidaria, are freely swimming marine animals with an umbrella-shaped bell, used for locomotion, and tentacles, used for stinging prey. They swim by expanding and contracting their bell-shaped bodies to push water behind them (Singla, 1978). Along the outer edges of the bell, jellyfish have a loose network of neurons, or nerve net. The jellyfish nerve net is like a cobweb in structure. There are sensory cells and receptors that stimulate the nerve net, and muscles that contract in response to signals from the nerve net. The nerve net enables jellyfish to respond quickly to an external stimulus, but they cannot locate the identity or location of the stimulus, thus a jellyfish will produce the same motor response to something touching it regardless of what it was or where the jellyfish was touched (Schwab and Sadun, 2007).

Starfish, from the phylum Echinodermata, consist of a central disc with five arms. Using the suckers on their tube feet, starfish can move faster than sponges, though many cannot exceed 76 cm per minute (Mueller et al, 2011). Still pretty slow. The starfish nerve net is organized into a nerve ring around the mouth along with radial nerves that run down each arm. The nerve ring and radial nerves have sensory and motor components. The sensory component receives rudimentary sensory information regarding touch, light, temperature, orientation, and odour. The motor component controls the tube feet and muscles. The radial nerve net in starfish is a touch more complicated than the diffuse nerve net of jellyfish, suited to controlling more complex movements within each arm.
Jellyfish have an umbrella-shaped bell and tentacles with which they are able to freely move. They possess a rudimentary nervous system, called a nerve net.
Starfish have a central disc with five arms with which they can crawl along the sea floor. They also possess a nerve net.
Though still limited, the nerve nets of cnidarians and echinoderms permit them to have a greater range of movements than sponges.

The Ragworm Brainstem

Ragworms, marine animals from the phylum Annelida, evolved 600 million years ago (Tomer et al, 2010). They are one of the first animals with bilateral symmetry - a right and left side. Ragworms have a head with a collection of neurons called a brain (the coordinating center of the nervous system), with four primitive eyespots embedded within it. Some people postulate that the eye evolved first and stimulated brain evolution by providing vast amounts of visual data (Schwab and Sadun, 2007).

The ragworm brain is the precursor to our tripartite brain (Tomer et al, 2010); it has a hindbrain, midbrain, and forebrain. All vertebrates display these three stages during embryological development. The hindbrain is a rudimentary medulla, one of the major components of the brainstem. In the ragworm, this rudimentary brainstem probably executed motor programs. As animal brains developed and later brain structures appeared, the rudimentary brainstem changed little (Northcutt, 2002); for example, an ancient component of the brainstem called the reticular formation contains the same number of nuclei in all jawed vertebrates (Cruce et al, 1999). Thus, the rudimentary brainstem's motor programs remained confined to executing protective reflexes as well as eye and body movements, though as the eye developed the brainstem started creating topographic maps. Later, as the other brain structures evolved, the brainstem became critical for generating states of arousal, reward, and stress.
Ragworms have a head with a rudimentary medulla, or brainstem. It is still hard to tell which end is the head.
The human brainstem is sandwiched between the spinal cord and the rest of the brain. It has four components - reticular formation, midbrain, pons, and medulla; the reticular formation is not shown here.

The Hagfish Thalamus

Hagfish, appearing 530 million years ago, have a skull but no vertebral column and are often considered to be the final ancestor to precede the vertebrates of phylum Chordata (Kuratani and Ota, 2008). They have eel-like bodies and literally tie themselves up in knots to get enough leverage to tear flesh from carcasses (Wallace, 2007).

Hagfish possess a rudimentary thalamus (Wicht and Northcutt, 1998) with which they integrate sensory information. Since the world often stimulates more than one sense, the evolution of a structure that could combine sensory information from multiple sources would have been extremely beneficial, providing a multimodal sensory experience of the world. In addition, perhaps the rudimentary thalamus aided the rudimentary brainstem in storing and producing simple motor programs, resulting in more complex behaviours such as the ability of the hagfish to tie its body into knots. However, as the thalamus continued to evolve in reptiles, birds, and mammals, its functions changed as the hippocampus and neocortex developed alongside it. Being entwined with these two structures, the thalamus now helps the brainstem to generate various states of arousal needed for optimal memory formation by the hippocampus and neocortex, and it also stimulates the neocortex into highly activated attention states.
The hagfish, the only known animal with a skull but no vertebral column, possesses a rudimentary thalamus.
The human thalamus is a bilobed walnut-shaped structure that consists of a mass of nuclei, the most prominent of which are the relay and intralaminar nuclei; the thalamic nuclei form extensive circuits with the neocortex.

The Lamprey Basal Nuclei

Lampreys also appeared around the time of the hagfish and since they have a vertebral column may be the earliest vertebrates. They parasitize living fish by attaching themselves with their sucker-shaped mouths and cutting through the skin with their teeth to suck away body fluids (Wallace, 2007).

Lampreys possess a rudimentary basal nuclei (Stephenson-Jones et al, 2011), a brain structure that evolved to help perform movements. As animals developed a larger repertoire of motor movements, there were more options to choose from, and the rudimentary basal nuclei probably evolved to ensure that only the single best movement was performed at any given time. Interestingly, the organization and function of the basal nuclei has been conserved during vertebrate evolution, all the way from lampreys to humans (Stephenson-Jones et al, 2011), although the basal nuclei did expand significantly in size along the way. The size increase is probably best explained by the greater variety of new and different landscapes encountered as amphibians and later reptiles, birds, and mammals explored dry land. Dry land presented a variety of new and different terrain types which would have stimulated an expansion in the repertoire of available movements, which in turn would have driven an increase in basal nuclei size to ensure that the single best movement was chosen from this expanded repertoire. Despite the increase in size, the basal nuclei still performs its original function, processing contextual sensory information so as to ensure that the most statistically suitable memories for a particular situation are converted into movements and cognitions.
Lampreys have a vertebral column and lots of teeth made of keratin. They also possess a rudimentary basal nuclei.
The human basal nuclei is a collection of subcortical gray matter deep within the brain that consists of several groups of neurons called the striatum (caudate nucleus, putamen, and nucleus accumbens), pallidum (internal and external pallidum), substantia nigra (pars compacta and pars reticulata), and subthalamic nucleus; the basal nuclei exists within circuits that include the thalamus and neocortex.

The Shark Cerebellum

Jawed cartilagenous fish, such as the shark, are vertebrates that appeared over 450 million years ago (Haines et al, 2005). In addition to the senses we are most familiar with, including a supremely developed sense of smell enabling it to detect tiny concentrations of blood in the water, the shark possesses a lateral line system capable of detecting vibrations in the water, and they are able to detect tiny electromagnetic fields produced by other animals (Fields, 2007). As everyone knows, sharks are predators.

Sharks were among the first animals to evolve a rudimentary cerebellum, a brain structure involved in motor control that is notably absent in hagfish and lampreys (Northcutt, 2002). Sharks have sophisticated predation strategies requiring a wide variety of complex motor behaviours. To simply perform a sequence of behaviours does not require critical timing, but to perform them with skill - so as to catch fast-moving prey, for example - does require critical timing; one poorly timed behaviour and the intended prey escapes. The rudimentary cerebellum allowed motor programs generated by other brain structures to be executed in a temporally controlled fashion, resulting in skillfully timed movements. The structural organization of the cerebellum has changed very little from sharks to mammals (Northcutt, 2002), and hence its role as a memory timer has also changed very little; however, as the neocortex expanded in size and complexity, so did the cerebellum such that it now produces not only practiced, high-level movements but practiced, high-level cognitions as well.
The shark is a predatory fish with a supremely developed array of sensory abilities and a highly developed cerebellum.
The human cerebellum is attached to the bottom of the brain and contains more neurons than all of the other brain structures put together. It forms prominent circuits with these other structures, especially the neocortex.

The Goldfish Hippocampus And Amygdala

Moving along brings us to the goldfish, a type of ray-finned fish, a subclass of bony fish that appeared as far back as 420 million years ago (Jastroch et al, 2005). There are many species of ray-finned fish, such as eels, salmon, and cod, but goldfish are particularly well-known as a result of their domestication in China over one thousand years ago.

Ray-finned fish have a medial pallium. The medial pallium aids in spatial navigation - there is ample experimental evidence of a spatial memory system in goldfish (Portavella et al, 2004) - and the formation of new memories. The medial pallium probably developed further in amphibians when they moved to dry land 380 million years ago (Yeo and Drage, 2006); moving in the sea is not that difficult, as swimming movements are similar regardless of location or depth, but on land the topography constantly changes. Along with a few other brain structures, the medial pallium evolved as part of a memory system that could learn and ¨play back¨ movement sequences that had been successful in a particular situation experienced earlier. The memories of these movement sequences were helpful whenever the animal encountered a situation similar to that which originally produced the memory. This memory system became more established in reptiles, even more so in birds, and with the appearance of mammals the medial pallium had differentiated into a structure called the hippocampus. The human hippocampus is the structure that encodes and consolidates novel sensory information.

Ray-finned fish also possess a pallial amygdala. The pallial amygdala is involved in emotional processing - there is evidence that goldfish have an emotional memory system (Portavella et al, 2004) - which likely evolved to rapidly process fear-related information by creating memories of odours threatening the animal´s survival. The pallial amygdala prioritizes the expression of certain motor programs by producing fear, which surpasses all other considerations and allows the goldfish to react promptly to immediate danger. As vertebrates evolved from fish to mammals, the pallial amygdala developed into the more generalized amygdala, a structure that could process not only fear-related information but also information from other situations resulting in a spectrum of emotions. The generation of emotion allows the amygdala to predict the potential stress associated with an experience so that it may be engaged or avoided as necessary. The amygdala also regenerates emotions in slightly altered form during sleep which increase the ability of the individual to cope with stressful experiences more successfully.
The goldfish is a type of ray-finned fish that was domesticated in China over one thousand years ago. Ray-finned fish are named after their ray fins supported by bony or horny spines. The goldfish has both a medial pallium and pallial amygdala, precursors to the hippocampus and amygdala, respectively, of later vertebrates.
The human hippocampus is a seahorse-shaped structure that merges with the amygdala, an almond-shaped structure. The hippocampus is a small infolding of cerebral cortex that maintains strong interconnectivity with the neocortex. The amygdala is a tiny collection of nuclei that receives inputs from the thalamus, hippocampus, and neocortex and sends outputs to brain structures that produce excitatory neurotransmitters, most of which are in the brainstem.
In this front-on brain view we can see the relative positions of the hippocampus and amygdala, as well as the brainstem, thalamus, and basal nuclei.

The Neocortex From Opossums To Humans

Finally, marsupial and placental mammals appeared 125-190 million years ago (Ji et al, 2002; Lemos, 2007). The opossum is the oldest surviving mammal and can live in many diverse locations and conditions.

The opossum has a neocortex, a structure associated with the complex behaviours of mammals. The neocortex did not actually first appear in mammals - even the hagfish evolved a tiny bit of neocortex - but for a long time it was dedicated to olfaction (Northcutt, 2002). The neocortex remained an olfactory center in the fishes and amphibians, and while the reptiles and birds developed another possibly homologous structure called the dorsal ventricular ridge (Aboitiz, 1999), the neocortex changed little until the mammals. As a result of a striking increase in neocortical size, mammals developed brains that were ten times larger than those of reptiles of the same body size (Northcutt, 2002). The neocortex continued to evolve in size and complexity from early to later mammals. The opossum, being the oldest surviving mammal, has a thin layer of smooth neocortex that is small compared to other mammals, with no folds to give it extra surface area. The neocortex of cats is larger and has a few folds, and chimpanzees have even larger folded cortices. The neocortex of humans and cetaceans is relatively enormous (Northcutt, 2002) and the surface contains many folds, giving it a much larger surface area in the confined space of the skull. In humans, this massive expansion in neocortical size occurred in our human ancestors during the last two million years (Kaas, 2013), an exceedingly short period of evolutionary time, and it paralleled the evolution of sophisticated human behaviours such as the use of tools and the development of complex group social interactions. The neocortex was the final component of the memory system that began in the fishes, allowing mammals and especially humans to store many more memories of past experiences, culminating in an internal model of the world from which memories could be retrieved so as to make predictions about the world (Hawkins, 2004).
Opossums are the oldest surviving mammals. They are generalists and can survive in many different kinds of environments thanks in large part to their neocortex.
The opossum neocortex. Note the smooth thin outer layer and lack of folds.
The human neocortex is a 2-3 mm thick sheet of neurons that envelopes the rest of the brain. Note the extensive neocortical folding.

Human Brain Evolution

From the outline shown above, a reasonably coherent synopsis regarding the evolution of the brain and its various components can be presented.

The earliest animals such as sponges had no nervous systems, rather only a few semi-specialized cells with which they could sense and respond to the world. These cells enabled them to perform coordinated movements, but they remained largely sessile creatures with slow, limited behaviours. The jellyfish and starfish evolved a rudimentary nervous system called a nerve net. The nerve net allowed these animals to react quickly, but the range of movements was still limited.

Initially, most of the brain structures evolved to process the execution of simple motor programs. The hindbrain, a rudimentary brainstem, evolved in annelids such as the ragworm and it generated these initial motor programs which allowed the animal to have a slightly greater repertoire of movements. In the earliest fish we see the evolution of the rudimentary thalamus, basal nuclei, and cerebellum. Multiple senses had now evolved and the rudimentary thalamus allowed the animal to integrate data from all of them; it may have also stored additional motor programs. With an increased repertoire of motor programs, some way was needed to ensure that the correct motor program was executed in response to a particular stimulus; the basal nuclei evolved to fulfill this need. The increased range of behaviours also meant that a greater variety of behaviours could be serially performed in a temporal sequence, resulting in a need for increasingly complex timing operations; the cerebellum evolved to fulfill this requirement. 

Although they became more elaborate, motor programs probably remained inflexible, which probably became a limitation as the variety of situations increased. To get around this, later fish developed a short-term memory system out of the precursors to the hippocampus and amygdala. The rudimentary hippocampus probably allowed the animal to temporarily learn simple memories and play them back, providing a way for experiences to be temporarily retained and used to predict events in future situations. The rudimentary amygdala evolved as a fear-based conditioning system, allowing the animal to rapidly respond to and remember stimuli that immediately threatened its existence. Although the rudimentary neocortex was around by now, it was dedicated to olfaction, and so this initial memory system probably relied largely upon temporary memory encoding and fear-based conditioning.

As amphibians moved to dry land and evolved into reptiles, birds, and mammals, most of the brain components above increased in size and changed or expanded in function. By now, the brainstem and thalamus were generating and mediating arousal by creating states of wakefulness and sleep optimal for memory encoding and consolidation, respectively; the brainstem was also guiding behaviour by generating physiological states of reward and stress, and the thalamus became important in stimulating states of attention important for memory formation by the hippocampus and neocortex. The hippocampus continued to play a central role in novelty encoding and consolidation, and the amygdala evolved further to produce numerous negative and positive emotional states other than fear with which it used to make predictions about potentially stressful experiences as well as cope with stressful experiences more successfully in the future. Finally and most notably, the neocortex evolved from an olfactory structure into a long-term storer and retriever of consolidated memories, thus enabling the animal to make long-term predictions about the world. Ultimately, the human brain has evolved into a memory system that constructs a model of the world to make predictions about that world.
The stages of human brain evolution, using a broad brush.
From the earliest fish to humans, all vertebrate brains go through the same precursor stages when developing as embryos. In humans, the hindbrain or rhomboencephalon gives rise to the pons and medulla of the brainstem, the midbrain or mesencephalon gives rise to the midbrain, and the forebrain or prosencephalon gives rise to the diencephalon (thalamus, hypothalamus, subthalamus, and epithalamus) and telencephalon (basal nuclei, amygdala, hippocampus, and neocortex).
Comparing the brains of sharks with humans illustrates the relative size increases of certain structures, particularly the forebrain telencephalon. In sharks, the telencephalon is no larger than any other structure. In humans, the telencephalon is massive and develops into multiple structures including the basal nuclei, hippocampus, amygdala, and neocortex.
The hominid brain has increased in size dramatically over the last three million years. In Australopithecus afarensis the skull volume was 400 to 550 mls. In modern Homo sapiens the skull volume is 1200 mls or more. Most of this is a result of neocortex expansion.

Closing

This is just an overview of the evolution of the main components of the human brain, and we will learn more about each of them in the chapters that follow. Placing the components of the human brain in an evolutionary context allows us to discern some of the reasons they evolved the way that they did. It should also be apparent that although the human brain is - currently - the final and most complex product of nervous system evolution, it is still only one point on the evolutionary continuum. Its structure and function are the final result of the many simpler precursor animal brains that preceded it. Thus, although the human brain may be complex, its evolution is ultimately grounded in simplicity and therefore it can be understood by using simple concepts that take evolution into account. Now that we have introduced the main components of the human brain and their respective places in evolutionary history, we are ready to take a hard look at the structural features of each, and how these features relate to function. 

We begin with the brainstem.
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