Origins And Purpose Of Consciousness
Consciousness (in this section using the word in its most general sense), needless to say did not spring into existence overnight, any more than the mammalian brain itself, but is the result of a long process of elaboration of the neural apparatus that evolved to allow animals to respond speedily and appropriately to sets of circumstances in the outside world. From that perspective, the advanced social consciousness of a modern human is not different in kind from the chemical reaction that caused an amoeba to turn away from the light 5 billion years ago.
Amoebas which did not turn away from the light shrivelled and died; and modern humans who through sickness or disability are incapable of accurate social functioning may be preserved intact by modern medicine for a period of time but are less likely to reproduce.
As with every characteristic of humans, or any other animal, there is an evolutionary reason for the existence of consciousness in its variegated forms; the job of researchers working in the brain sciences is surely to identify that reason, and it hardly seems possible and certainly not useful to describe the workings of an aspect of the brain without at the same time having a notion of its purpose.
Heaven knows how many hundreds or even thousands of books have been written about consciousness or how many millions of hours have been spent in discussion of it with little or no consideration given to its purpose. A surprising number of current writers on the subject have nothing to say about the reason for which consciousness exists. For them it is either inscrutable, or perhaps it is simply too obvious to be worth mentioning. For centuries, while dualistic theories of consciousness ruled the roost, it was convenient to hide behind its God-given unknowability; and the habit seems to linger on even after the neural mechanisms that underpin consciousness have been identified, described and even quantified to a point at which no serious student of the phenomenon can suppose that its explanation lies anywhere but between our ears.
Starting from the proposition that there is a direct line of descent, or perhaps we should say ascent, from the light-sensitive amoeba to the human brain, a concept which is no longer questioned, Table One sketches a series of stages of neural and cognitive development. Of course there are multiple intermediate or parallel stages, but to support the integrity of the proposition of continuity of development, it just remains to demonstrate adaptive fitness at each stage, to give a reasoned account of the impact of the changes that took place, and to explain to an extent how and or why those particular changes took place when they did.
The last twenty years have seen major shifts in the generally accepted account of the phylogeny of early animals due to rapid advances in biochemical and genetic research techniques, and the succession of anatomical stages shown in Table One, once regarded as a seamless progression, is now better regarded as a series of snapshots of advancing animal evolution, with a possibly tortuous phylogenetic route linking the various stages.
In describing the neural apparatus of animals at the different stages of development, it also has to be remembered that it is current members of the species in question that are described. So, for instance, nobody can tell for sure when the jelly-fish, a member of the Cnidarians, actually evolved, or at which stage jelly-fish acquired particular sensory capabilities. But we do know that Cnidarians came before Bilateria (e.g. worms), had nerve nets, did not have ganglia (assemblages of neurons), had some sort of sensory apparatus and had motor capabilities.
As just about everyone knows, the jelly-fish has a nerve-net, a series of interconnected nerve cells but without ganglia (i.e. without a proto-brain); it also has nerve rings. Jelly-fish also have a sensory apparatus which can stimulate the nerve-net and at the other end, so to speak, muscles which can cause locomotion.
The jellyfish does not however qualify on even the lowest rung of the ladder of states of consciousness set up for the purposes of this book, 'somatic responsiveness' – the ability of an organism to assemble an integrated view of its bodily state from moment to moment on at least one sensory modality and behave appropriately in response to external and internal stimuli.
The ragworm (e.g. Platynereis dumerilii or Nereis succinea) is a Protostome, that is to say it has a body cavity and its mouth forms before its anus; they emerged for the first time about 600 million years ago. They also have a differentiated front section, but which cannot yet be called a head, usually with a mouth, something resembling an eye or eyes, a collection of neurons which can begin to be called a brain, a nerve-cord (originally probably ventral) with branches, and a primitive blood circulation system. Many researchers believe that an early bilaterian ancestor 'flipped over' at some stage so that the nerve cord became dorsal, which it has remained ever since (see, e.g. Telford, 2007).
Apart from its own direct connection to the brain, the last ganglion before the brain as such sends out circular nerves which travel around parts of the front of the animal before reaching the brain, which consists of two relatively large lobes. Four eyes are embedded directly in the brain. Detlev Arendt et al (2002) hypothesize, based on comparison of cell types, that the urbilaterian eye evolved from within the animal's brain. The reproductive cycle of ragworms is initiated by varying day length, perhaps perceived through the eyes, and mating results in the death of the female animal. Separate nerves from the other sense organs of the front section, including two types of antennae, chemical sensors and 'palps' (primarily intended to manipulate food, but having sensory receptors as well) also enter the brain. The segmental parapodia also have sensory receptors. Note that the ragworm's neural apparatus is already using synaptic neuron-to-neuron linkages, whereas the jellyfish uses 'in passing' neuron-to-neuron connections which are less flexible, slower and less informative than a synaptic mechanism.
Heuer and Loesel (2008) have studied a related ragworm called Nereis diversicolor, describing two major brain compartments, paired mushroom bodies and a central optic neural cluster. Mushroom bodies occur in all insect species, where they are taken to be involved in the olfactory pathway and have been associated (but not by all writers) with learning and memory functions. They also occur in all annelid worms where they are mostly assumed to be homologous with insect mushroom bodies. There is no clear agreement on the function of mushroom bodies in annelid worms; but it may be fair to say that they are involved in processing chemo-sensory input from the antennae, other chemical sensors and the palps, all being forerunners of the olfactory sense. There is little or no connection between the mushroom bodies and the optic centre.
Detlev Arendt has established that Platynereis has a type of cell in part of its brain that is very similar in molecular terms to the type of cell found in the vertebrate hypothalamus. Although Polynereis does have mechanisms to ensure homeostasis, it appears that these operate through chemical balancing and may not involve the nervous system in a significant way.
In a very approximate form, the precursors of the vertebrate tri-partite brain can therefore be observed in ragworms: the forebrain, with a primarily olfactory input and a role in implementing internal affective agendas and a primitive endocrine function; the mid-brain, with optic input; and the hind-brain (the brain-stem), responsible for implementing motor programs, although much of that function is distributed among the segmental ganglia.
It will be seen that by comparison with the jellyfish, the ragworm has a considerably more sophisticated system of motor control, to deal with the coordination of as many as 200 sets of segmental paddles, including control of the direction of locomotion in three dimensions, resulting from collaboration between the fore-brain and the segmental ganglia. Here can be seen the earliest beginnings of time-related behaviour: each pair of paddles must act in synchrony with its predecessor pair. In fact they act in a wave motion.
Although the jellyfish has an up and a down, its motor activity is limited to simplistic functions such as 'go away from this stimulus' and 'envelop this prey'. The ragworm on the other hand can burrow, purposively approach food, swim directionally and bend its body; for this, a nerve net with its generalized responses was not good enough, and evolution has developed a brain in which mappings exist between particular sets of sensory stimuli and particular motor outcomes. The worm also has the beginnings of a proprioceptive, afferent nervous system in which the brain (or perhaps the segmental ganglia) receives information from sensory receptors on the segmental paddles which can be understood topographically (in a somatic sense) and used in the control of continuing locomotion waves. It is perhaps also significant that there are parallel longtitudinal nerve fibres emerging directly from the brain and connecting with segmental processes, bypassing the segmental ganglia, which may suggest a feedback loop. It is speculative, but possibly the brain might control the speed and direction of locomotion waves via direct feedback from the paddle receptors and input from the animal's sensory equipment, while the segmental ganglia direct synchronized locomotion itself. Whether or not this is what happens, the structure of the ragworm's nervous system would allow such sophistication, which is arguably required by the patterns of the animal's life.
Apparently, in order to chase down prey purposively, the ragworm's brain would in addition have to be able to maintain some sort of topographical information about its own position in relation to that of its prey. At this stage of development, however, this is probably not to be thought of as any kind of map, and less still as autobiographical memory – it is more likely to be a series of moment-to-moment judgements of a kind such as: 'chemical receptors say food is at 8 cm on heading 5 degrees left; instruct segmental ganglia to increase speed to eight waves per second and change heading to 5 degrees left on level path'. It's not clear whether the ragworm would be capable of estimating the speed of its prey, which would allow a faster approach to it; this would seem to require the integration of a series of mappings over a defined time-base. The point could possibly be resolved by observing the approach of a ragworm to a moving but unaware food source: if the direction of interception is a straight line, then the ragworm has in some sense an awareness of time; if the direction is a curve, then time is probably not involved.
It is not clear whether, in the ragworm's brain, motor commands result from a simplistic 'if A then B' process, or whether, as is the case in mammalian brains, the process is more along the lines of: 'if A then B unless C'. That's to say that almost all mammalian activity seems to be the result of those drives or action decisions which are not inhibited, whereas in the jellyfish, there is a straightforward stimulus-response linkage. It might be supposed that the 'act if not inhibited' model must have been set up fairly early on in the development of the brain, but it is not clear whether the re-entrant loops that make this mechanism possible have begun to exist in the brain of the early Protostome. Even if they exist today in the brains of Protostomes, which is itself unclear, that does not of course prove they existed in Protostome brains 600 million years ago.
The ragworm appears to exhibit no social behaviours other than reproduction. The reproductive cycle is influenced by the moon. The worms reproduce sexually through the mingling of clouds of male and female gametes. Male worms are attracted to females by pheronomes, which cause movement towards greater concentrations of pheronome, culminating in the release of gametes when concentration reaches a critical level. It appears that the female dies after producing her oocytes; neither female nor male plays any part in the development of young worms. In fact this behaviour can scarcely be called 'social', since it is entirely driven by outside influences (light, or its absence, and chemicals), and does not seem to involve even the slightest idea of an 'other' or even recognition of a conspecific.
Neural characteristics of the original Protostome which was our direct ancestor and which can be described as having 'somatic responsiveness' are as follows:
Although the goal which drives this neural activity may be as vague as a general imperative that causes the animal to react to the nearby presence of a food source, it can't be ruled out in the current state of knowledge that the mechanism is indirect, ie that the ragworm has the beginnings of an affective (hedonic) system which is activated by chemical imbalances.
Between the ragworm, which clearly has somatic responsiveness but not categorizing responsiveness, and the shark, which probably has categorizing responsiveness, an intermediate animal, the hagfish, still an invertebrate, will illustrate the ongoing development of the brain.
The hagfish (Myxine glutinosa), which is supposed to be something like our final pre-vertebrate ancestor, is thought to have originated about 530 million years ago, and to have changed relatively little over that period. The only fossil found, about 330 million years old, is surprisingly similar to modern hagfish.
It should be said, however, that the phylogeny of the hagfish is disputed. One theory holds that it is a member of the Cyclostomata (jawless fishes) along with the lamprey, while another theory has the lamprey (which is vertebrate) as being closer to Gnathostomes (jawed, vertebrate fishes). See e.g. Heimberg (2010). It is even possible that the hagfish as we now see it diverged from the main line of Cyclostomata development, since it has some features that are not present in lampreys or Gnathostomes. At all events, for the purpose of studying neural development, it provides a useful halfway house.
However, motor commands are seemingly still communicated directly by the EPS to the brainstem, rather than through a feedback loop via the thalamus to the cortex (Loonen and Ivanova, 2015). Researchers say that the hagfish has either no cerebellum (involved in the fine control of movement) or only a very primitive precursor region.
A number of neurotransmitters characteristic of vertebrate brains already exist in the hagfish brain (Donald, Toop and Evans, 1999).
Not very much is known about the mating behaviour of the hagfish. It is apparently variably hermaphrodite, male or female depending on conditions and age (Powell, Kavanaugh and Sower, 2005). The mating or reproduction cycle is seasonal. Powell et al hypothesize that there is an active neuro-endocrine axis in the reproductive cycle of the hagfish, i.e. that production of gametes is stimulated by gonadotropins produced by the pituitary gland. Fertilization of oocytes takes place in water after release of male and female gametes.
The hagfish has only very primitive visual and auditory senses, but has a well developed system of sense organs on the skin which may be haptic or may even have a proprioceptive function and are connected to the brain stem (Braun, 1998). The eye is lensless, and covered by skin; perhaps it is primarily concerned with the timing of the reproductive cycle. The dominance of the olfactory sense is what might be expected for a bottom-dweller, like the hagfish. It is supposed, but the evidence is unclear, that the animal has only very limited ability to integrate sensory inputs.
The hagfish has some sophisticated motor abilities, though, including the capacity to tie its eel-like body into knots and ease the knot up or down its length, assisted by its slimy surface. This behaviour is said to be useful in prey-acquisition (tie yourself to a convenient post and reel in your meat) and in self-cleaning after escaping from a predator through the use of slime production. Hmmm. The hagfish swims by using a paddle-like tail, by gliding or by using "figure eight" or worm-like propulsion. Slime production, the other feature for which the hagfish is so remarkable, takes place in response to threats or supposed threats to the animal's well-being.
Sophisticated motor abilities in more evolved vertebrate forms involve a hippocampus, with the development of short term spatial memory, and an associated topographically organized body map. The hagfish has an area of its fore-brain which is considered likely to be homologous with the medial pallium of fishes (what later became the hippocampus), which is referred to as the 'primordium hippocampi' by some authors, and which receives sensory input from the olfactory lobe and also has substantial input from the thalamus (Wicht and Northcutt, 1998).
Clearly it is tempting to imagine that the hagfish, primitive as it is (or was) may have the beginnings of a motor control system with rudimentary short term spatial memory and a sensory mapping of its body in relation to its surroundings. Writers use words such as 'upset' or 'angry' in describing the animal's state when it becomes agitated enough to produce slime, and while there may be some anthropomorphism here, it is not unlikely that the hagfish has the beginnings of an amygdala-like affective (hedonic) system.
The shark is a jawed, vertebrate, cartilagenous fish (chondrichthian). While the olfactory sense is obviously of major importance to the shark – it can famously detect the most minute concentrations of blood and other important chemicals in water, it has very well developed vision and a highly sensitive 'mid-line' vibration detector which is supposed to assist in detecting vulnerable prey but may simply or also be a range-finding mechanism which works in conjunction with the olfactory sense. The shark has an auditory sense and, in addition to what would become a mammal's normal range of senses, an electrical sense through the 'Ampullae of Lorenzini' which is thought to give it information about nearby bio-electrical activity. The shark also has the ability to maintain parts of its body, and specifically the brain, at a higher temperature (as much as 14°C more) than that of the surrounding water; this energetically expensive behaviour is 'switched on' when needed, particularly during predation, allowing faster motor control.
The shark's brain has sensory input from well-developed eyes, from the 'mid-line' vibration detector, and from auditory and electrical senses. The brains of most sharks are mostly hollow — perforated by a series of irregular, interconnected chambers (ventricles) — and filled with a complex fluid (cerebrospinal fluid) that probably helps regulate the brain chemically. These ventricles are particularly large in the Great White shark, resulting in a brain composed of an unusually thin 'shell' of nerve tissue.
Olfactory information is far from having a dominant role in the fore-brain of the shark; input from the olfactory lobes is restricted to only one section of the pallium, while other sections receive input from all the other senses (Hoffman, 1999). It seems more than likely that there is a degree of sensory integration in the pallium, with resulting control over motor behaviour according to affective (hedonic) agendas driven by the amygdala.
The shark has a well-developed cerebellum, which sits alongside the tectum, a region of the mid-brain at the top of the brain-stem. Both the cerebellum, and even more so the tectum receive input from many different parts of the brain. The internal organization of the tectum is essentially similar to that in other vertebrates. Fibres originating in the retina forms a majority of input to the tectum, which is probably the region in which external objects are mapped in relation to the animal – the formation of a sensory image of the outside world. The cerebellum is strongly connected with the brain-stem, as would be expected, and receives efferent motor commands (Hoffman); its role in the shark, as in all vertebrates, is that of fine tuning of the animal's motor behaviour.
Sharks have sophisticated predation strategies involving a wide range of complex motor behaviours and appear to be able to predict the location of a fast-moving prey animal some seconds into the future; studies in the wild also indicate that sharks can improve their predation techniques through accumulated experience (Martin, Hammerschlag, Collier and Fallows, 2005) . Motor behaviour would therefore result from an interaction between the pallium and the tectum, with the cerebellum involved in detailed implementation. The pallium would seem to be the obvious candidate for the location of the combinatorial abilities that would be involved in the complex motor sequences needed in, for instance, predation.
There is plentiful anecdotal evidence for quite sophisticated social behaviour on the part of sharks. Apart from the predatory and mating behaviours described above, they are variously described as engaging in play, cooperating as a group to move the carcass of a partially beached dead whale to deeper water where they could feed on it, communicating with each other, exploring strange objects such as a boat or a diver in a non-predatory way, and learning to ignore a non-food, non-threatening object such as a boat.
R. Aidan Martin, who was the Director of the ReefQuest Centre for Shark Research, a Research Associate of the Zoology Department of the University of British Columbia, and an Adjunct Professor of the Oceanographic Center of Nova Southeastern University had plenty to say on his web-sites about the sophistication of the shark's mental apparatus:
Perhaps it's going too far to suggest that sharks have 'a developed sense of self and non-self', or indeed that they are conscious in the generally accepted sense of the term; but various aspects of these behaviours surely constitute categorization? Male conspecifics, female conspecifics, prey objects, non-prey objects, are some obvious categories which the shark employs, and can apparently access in relation to individual objects. It is of the essence of groupish behaviour that a group member recognizes other members of the group; it is hard indeed to imagine how group behaviour could exist at all in the absence of categorization of others (not necessarily, but usually) as group members. The evidence does not however go so far as to prove that the shark recognizes or identifies individual conspecifics. Brown and Gruber (2004) investigated dominance behaviour among lemon sharks, concluding that dominance was strictly correlated with size in almost all cases – but there was one instance when two sharks exchanged rankings (one got larger, the other smaller) without affecting their previous places in the hierarchy. That is difficult to account for unless there is a degree of individual characterization; but the evidence is inconclusive at this point. Other categories utilized by the shark would therefore appear to include dominance, inferiority, and species identity.
The seat in the shark of what Edelman (see Chapter Two) would call global mappings, if they exist, cannot be other than the pallium – a global mapping being a stored set of categorized spatial and sensory phenomena, possibly with affective linkages, which can be recalled on a future occasion when it is relevant. It's important however to distinguish this type of memory from continuous short-term (autobiographical) memory, which probably did not emerge until the amphibians developed a hippocampal memory.
Aidan Martin, who probably knew more about sharks than any other researcher, chose to call them conscious. That word has been banned in this book except in connection with self-consciousness, but it must surely be allowed that the shark has categorizing responsiveness?
As ever, of course, the caveat must be entered that what is true of today's sharks may not have been true of the original, ancestral chondrichthian. It is much easier and more secure to make the statement that the shark does not have a differentiated hippocampus, therefore neither did the ancestral precursor animal, than to assert that because the modern shark has a cerebellum, therefore so also did the precursor animal. Researchers approach that problem from a biochemical, cytological perspective. If the modern shark's cerebellum has a set of differentiated neural cell types that closely matches the comparable set in a mammal (and it does) then parsimony dictates that they had a common origin. There certainly are cases of parallel evolution, but at a much grosser level, and they typically use different chemical approaches even if they are functionally equivalent. Thus, the precursor animal almost certainly had a pallium which could store global mappings (because the necessary biochemical apparatus available in the mammalian cortex is matched in the shark pallium), probably did have a central-line vibration analysis sense (since a similar sense exists in amphibians, although it does not occur in mammals), but plausibly did not have a magnetic field detection sense (no mammalian cell-type has any apparent relationship with the shark's 'Ampullae of Lorenzini').
Approximately 430 million years ago, the lobe-finned fish (Sarcopterygians) evolved; these bony fish, with lobed, paired fins, are just about universally accepted as the ancestors of all tetrapods, i.e. four-limbed animals, which of course includes us humans, and their modern representatives, including the lung-fish and the famous coelacanth, which are thought to have conserved their original features to an unusual extent. The Sarcopterians have rather small brains, but they exhibit all the features described above for the shark, and there is (disputed) evidence that the hippocampus has become differentiated.
It is therefore probably not fanciful to suggest that the development of the hippocampus is linked to the emergence of amphibians onto dry land, something that happened about 380 million years ago. The sea is after all far more featureless than the land (although the sea bottom is not) and motor activity is much the same whenever and wherever an animal practises it. That all changes when an animal has to function on dry land, which presents innumerable topographical challenges. Clearly it would be adaptive for an organism to be able to record and 'play back' learned sequences of motor activity relevant to the territory it inhabits without involving the scarce resource of the cortex, which was very small at first. Thus it is that the hippocampus needs to remember events over short time-scales; without such a functional ability, memory and the awareness of the flow of time which we call consciousness could never have developed.
It is unclear whether the original amphibian would have had a hippocampus as such; perhaps at first there was simply a differentiated region of the pallium which carried out an equivalent function.
The cerebellum, on the other hand, which already existed in at least more advanced species of fish, underwent great expansion when amphibians grew legs on dry land, requiring far more sophisticated control of balance and movement.
Among extant amphibians, it is generally supposed that the salamander is phylogenetically closest (but not very close) to the original amphibian animal which was the common ancestor of reptiles (our own ancestors) and modern amphibians. The salamander has a well defined amygdala and a hippocampus which have plentiful links to other regions of the fore-brain and mid-brain, which would appear to permit interaction between emotional agendas, sensory states and motor activity (Laberge, Muhlenbrock, Grunwald and Roth, 2006).
In amphibians, sensory input from the eyes goes chiefly to the tectum, the thalamus and the hypothalamus. It is thought that the tectum, which is organized topographically in relation to the images perceived by the retina, is involved in prey recognition. Frogs and toads, which do not have saccadic eye movements and cannot track objects moving across the visual field, must decide on whether an external object is prey or non-prey before moving, and having once started a motor sequence towards prey must complete it even if the prey disappears (Ewert, 1974). In fact, it appears that frogs do not make use of the information in their visual field other by noticing that an object (typically, a fly) is crossing it. If the fly is motionless, they will not see it (Lettvin, Maturana, McCullough and Pitts, 1968). Mating behaviour is supposed to be guided much more by olfactory and auditory input than by visual input.
Afferent (incoming) sensory information in toads and frogs also includes input from pain, touch and temperature receptors, as in all later vertebrates. Motor responses to touch seem to be mediated by an area close to but distinct from the tectum.
Frogs and toads have well-developed ears, along with a set of very programmed vocal calls, whose purposes include at least mating, territorial marking, release, warning, rain, and distress (Bogert, 1960). Auditory input (as in all vertebrates) arrives in the mid-brain, but eventually climbs via the thalamus to the pallium (Feng, 1990). Hoke, Ryan and Wilczynski (2007) found that calls related to mating resulted in activity in multiple regions of the brain, whereas calls with aggressive intent involved fewer regions. Mating behaviour in most amphibians is indeed complex; Gillette, Jaeger and Peterson (2000), describe social monogamy (which doesn't necessarily result in mating) among a population of salamanders. Deception is observed in frogs: small individuals sometimes make deeper calls in order to present themselves as larger than in fact they are (Bee, Perrill and Owen, 2000).
All of the frog's calls in fact probably have a social purpose (Kanamadi, Schneider, Hiremath and Jirankali, 1993). The 'release' call is used when a male frog mounts another male, presumably in error, and possibly to avoid waste of sperm. Tropical frogs make 'rain' calls when humidity indicates that rain is imminent, but it is not clear whether the call has a territorial or a sexual purpose. 'Defense' calls are used in territorial disputes, usually between males. 'Distress' calls are made when a frog is in danger, and may serve to warn conspecifics.
Jaeger, Gillette and Cooper (2002) showed that male salamanders were significantly more aggressive towards and stayed farther away from female partners that were socially polyandrous relative to those that were socially monogamous, during both the summer noncourtship season and autumn courtship season. 'We infer that males attempted to manipulate female partners into social monogamy by increasing aggression towards socially polyandrous partners', said the researchers. This suggests that salamanders must not only be able to distinguish and remember the identity of conspecifics in their locality (group?) but also can retain and access memories of their past behaviour in future social situations.
Frogs often migrate in groups to reproduce in or at a body of water. After the collective calling behaviour for which frogs are so well known, frogs reproduce through physical contact between males and females, although eggs and sperm meet outside the body in most species. There are many examples of parental care among frogs (Crump, 1996): some species guard spawn until it hatches; others carry the spawn on their backs or legs until it hatches; Darwin's Frog (Rhinoderma darwinii) from Chile keeps tadpoles in its vocal sac while they develop.
Groups of salamanders occupy ranges of territory in which individuals mark out their own individual territories. They are then highly territorial, and defend their territories against intruders (Mathis, Schmidt and Medley, 2000). The territories of males and females can overlap.
All in all, as would be expected from the lack of cortical development, it cannot be said that the amphibian's behaviour stems from an integrated cognitive understanding of its state. Individual behaviours result from coordination of just those parts of the brain that are necessary, with reproductive behaviour seemingly the most complex, and employing the greatest degree of coordination of sensory information with emotional agendas. However, the amphibian does have a map of its external surroundings, sets of 'global mappings' in its pallium, and, thanks to the presence of a hippocampus, it probably has the beginnings of a 'remembered present', allowing it to construct sequences of behaviour which are informed by internal and external events within the last few seconds. Thus the amphibian can be said to have categorizing responsiveness, on the scale of awareness employed in this book, and displays the beginnings of social responsiveness.
Sauropsids constitute a phylum which includes among its living representatives turtles, snakes, lizards and birds. They are of course verterbrates (jellyfish and worms are invertebrates). It is not too clear what our original Sauropsid ancestor may have looked like, but it is a good guess that it appeared about 300 million years ago. Among extant Sauropsids, turtles are often said to be closest to the original ancestor, while snakes are rather remote. Sauropsids and all their descendants are amniotes, that is to say they have eggs with impermeable skins, an evolutionary innovation that became necessary when animals no longer had access to water in which to reproduce.
Sauropsid brains already exhibit most of the structural features of mammalian brains, including a cortex with differentiated regions (known as the pallium and including the striatum in the basal ganglia), the amygdala, cerebellum, hippocampus, thalamus, reticular formation and so on. This may and arguably does mean that Sauropsids have emotional states which can influence behaviour (amygdala), have automatic control over the fluidity and timing of movement (cerebellum), have the ability to lay down memories, particularly ones associated with spatial data (hippocampus), and control motor behaviour by using re-entrant loops linked to affective (hedonic) systems via the thalamus (basal ganglia), ie a snake may not bite you if it knows you, something that wouldn't work with a ragworm or a jellyfish.
Major changes that took place in the evolution of the Sauropsid brain from the amphibian brain include greater size, much increased structural differentiation in the mid-brain and developing forebrain, and much stronger neural connections between the olfactory bulbs, the corpus striatum, and several other subcortical structures, most of which were subsequently conserved in the evolution of mammals. The connectivity of the telencephalon (hippocampal-striatal-amygdala complex), already much increased in the amphibians, and even more in Sauropsids, provides capacity for interaction and synthesis between internal hedonic (affective) agendas (drives) and sensory representations which are crucial to the development of categorizing responsiveness in more advanced amniote vertebrates. These changes are seen as being necessary for the mediation of predation and mating, and also provided the basis for social behaviors including cooperation and aggression.
Reiner, Yamamoto and Karten (2005) state that in birds, the basal ganglia occupy no more of the telencephalon than is typically the case in mammals, and that they play a role in motor control and motor learning as in mammals. They say that the vast majority of the telencephalon in birds is pallial in nature and, as is true of the cerebral cortex in mammals, provides the substrate for the substantial perceptual and cognitive abilities evident among birds. They consider it most likely that the avian pallium and the mammalian cerebral cortex, and their respective thalamic connections, had a common origin in an ancestral Sauropsid amniote.
Biochemical studies of turtle brains (eg Powers and Reiner, 1993) have also confirmed the common origin of mammal and Sauropsid brain organization, as well as pinpointing what appears to be the crucial site (the cortical edge of the pallium) where a biochemical difference emerged leading to the lamination of cortical layers so characteristic of the mammalian brain (Bernier, Bar, Pieau, De Rouvroit and Goffinet, 1999).
Although snakes have travelled far in evolutionary terms from their original Sauropsid ancestor, they have a standard Sauropsid sensory apparatus, including eyes, a sense of smell (through the tongue), a sense of taste, an auditory sense (probably based on skeletal vibration), cutaneous organs sensitive to pain, temperature, pressure, and stretching of the skin. There are proprioceptive receptors associated with muscles, tendons, ligaments, and joints. This set of sensory receptors is of course essentially identical in all vertebrates descended from Sauropsids, although the anatomical form taken by a given sense varies widely across species. In addition, most snakes have infra-red receptors via facial 'pits' in the mouth and nose region.
Snakes use their visual sense to locate and approach prey, probably assisted by vibration sensors (descended from the lateral line organ of fishes), and a chemoreceptive sense known as Jacobsen's organ usually located in the upper mouth; but at close quarters or in darkness they rely at least as much on their infra-red sensors (Jones, Lynn and Stone, 2001). Input from the facial pits arrives at the brain stem and is relayed to the optic tectum where it joins input from visual, motor, proprioceptive and auditory senses. In many snakes, infra-red perception is stereoscopic. The snake's visual and infrared maps of the outside world are overlaid in the optic tectum; the combined information is relayed to the fore-brain (Hartline, Kass and Loop, 1978).
Snakes have rapid and effective learning capabilities, coupled with retentive memories, for tasks which match the characteristics of their natural environments. Research conducted by Holtzman, Harris, Aranguren and Bostock (1999) confirms that sight is the primary sense employed by snakes for everyday daytime behaviour, and that the animals can quickly learn to escape from a brightly lighted environment (which they dislike), using remembered visual cues to escape much more quickly on repeated trials.
Crocodilians also have good, probably colour vision, and see well at night using vertical, cat-like pupils. They also have vibration-sensing pits, not just on the face, but in many species all over the body.
Those lizards thought to represent the earlier stages of Sauropsid evolution tend to be more reliant on the visual sense than later arrivals, notably the chameleons, famous for changing colour, although this is not so much to adopt protective coloration as to express emotion in a social context (Cooper and Greenberg, 1992). More advanced lizards such as the Varanidae (from whom it is possible that snakes are descended) put more reliance on chemosensory systems, sometimes in association with an active hunting style (Cooper, 2003)
Cutaneous sense organs are regularly present in Sauropsids, including receptors sensitive to pain, temperature, pressure, and stretching of the skin, very often all over the body. Sauropsids also typically have afferent proprioceptive nerves reporting on the position of muscles, tendons, ligaments, and joints.
Tool use has been observed in other bird species, including woodpecker finches (Cactospiza pallida), Egyptian vultures (Neophron percnopterus) and hyacinth macaws (Anodorhynchus hyacinthinus). There is no agreement at present as to the relative contributions of genetic predisposition and cultural (social) transmission to these behaviours, but in their more developed forms it cannot be denied that the birds are using a sophisticated amalgam of multi-sensory mapping, motor control, short-term and long-term memory to satisfy emotional agendas. 'Tool' or 'bent stick' is clearly a cognitive category for crows, and they can associate (and remember the associations) of that category to a variety of possible materials. This is a convincing demonstration of categorizing responsiveness. How far this statement can be generalized to all Sauropsids is a moot question. They all have basically the same brain structure, but in the 300 million years since it evolved there has been plenty of time for a vast range of different functionalities to have emerged. Crows with twigs put one in mind of Dr Johnson's impossibly sexist remark (recorded by Boswell): "Sir, a woman's preaching is like a dog's walking on his hind legs. It is not done well; but you are surprised to find it done at all."
Snakes have a variety of reproductive patterns, but the norm is for a male and female snake to copulate through penetration by the male; in some species of snake there are mating 'balls' in which many snakes, with a preponderance of males, share the mating process. Snakes display a variety of male-to-male dominance and courtship behaviours, including combat rituals between males, with chin-rubbing, body jerks, wave motions, pushing, biting and tail manoeuvres during courtship, with sometimes several of these happening at once (Carpenter, 1977). Suggestions from previous research that polygyny (multiple females for one male) is the dominant mating pattern among snakes have been contested by Rivas and Burghardt, 2005, who present evidence that the contrary is true, and that polyandry (multiple males for one female) is more common. They suggest that this accounts for the lack of territorial behaviour among snakes. Although pythons incubate their eggs, parental care is generally rare among snakes.
Turtles interact during feeding, courtship and basking, displaying agonistic, courtship and general social behaviours, the latter particularly between females. Gossip, already? Dominance displays among males sometimes involve two or more larger males 'bullying' smaller ones. (Davis, 2007)
Many types of Sauropsids have hearing, but snakes and some lizards lack an external ear. It is supposed that in those cases, vibration may be conducted through the skeleton to the middle and inner ears. Some researchers believe that such earless animals are deaf to the sounds they themselves make; but that seems improbable unless the sounds have no social function.
Social behaviours are particularly well developed among some species of birds; tool-use among crows (described above) may have a strong social element – young crows may learn about particular tool shapes by observing conspecifics forming or working with tools. Social acculturation plays a large part in the upbringing of crows: they live in extended family groups for at least the first year of life, foraging together (Bluff, Weir, Rutz, Wimpenny and Kacelnik, ibid).
Observation of crows in a Moscow suburb over a long period of time (Yarmoosh, 2008) has shown that they cooperate in small groups of five or six birds to fight off hawks which threaten smaller birds, although not the crows themselves. The area consists of an array of tower blocks divided by extensive recreational areas with belts of trees and shrubs and much open ground. Hawks live nearby in a forest and occasionally attempt to prey on the easy pickings of sparrows and titmice, birds which are often fed by local residents. The surreptitious approach of the hawk is usually spotted by pigeons, who seem particularly sensitive to the shape of the hawk in the air, and whose agitation alerts the crows, which immediately drive off the hawk. No direct physical encounter between crows and hawks has ever been seen, however: once the crows are onto the case, the hawk knows it has no choice but to return to the forest.
This tale is rich in conclusions about the cognitive behaviour of the various types of bird that are involved; but the most interesting by far is the apparent altruism displayed by the crows. They don't eat sparrows, are not eaten by hawks, and don't appear to face any territorial challenge from the hawks. So what is going on? Is it fanciful to suppose that some kind of multi-species mutually supportive bird group has developed? But then, what do the sparrows do for the crows? The smaller birds, which typically feed during the winter from small nut and seed dispensers fixed to the outside walls of upper floor balconies (inaccessible to larger birds) have been observed to use their beaks to kick out seeds and nuts to fall to the ground, possibly to reward the crows and pigeons. It seems too good to be true!
Ravens (corvids) and western scrub-jays (another intelligent bird species) display complex food-cacheing behaviour which involves close observation of conspecifics' behaviour and deceptive strategies (eg Clayton, Dally, Gilbert and Dickinson, 2005). Rooks, another highly social and intelligent species of corvid, spontaneously cooperate in solving problems, with two animals rapidly learning to pull simultaneously at two strings in order to reel in a food platform (Seed, Clayton and Emery, 2008). Noting that living in a large social group requires or encourages the evolution of enhanced cognitive abilities, Paz-y-Miño, Bond, Kamil and Balda (2004) demonstrated the ability of pinyon jays (Gymnorhinus cyanocephalus), a highly social bird which does indeed live in large groups, to reach inferential conclusions about their own social status through observation of the behaviour of other group members. Say the authors:
Some species of lizard are reported to use vocalizations in courtship or distress situations. Some lizards exercise parental care, with the female incubating eggs, and newly-hatched young remaining close to their mothers for some days. Hartdegen, Russell, Young and Reams (2001) reported that mothers in such situations exhibited defensive behaviour, including production of a 'distress' call, when a human intervened. Accompanying male lizards seemed indifferent to the provocation. Lizards are often collected in duos, sometimes in trios, with one male being accompanied by two females, causing Hartdegen et al to describe them as being quite social animals.
Many types of Sauropsid generate sounds, usually with a social purpose. Male alligators bellow; snakes hiss or growl or lash or rattle their tails. Birds are of course the stars of Sauropsid communication, and birdsong has been the subject of innumerable studies. Most conclude that birdsong has a predominantly social function, something that seems evident without any need for demonstration! As one example, a study (Robinson 1990) of the Superb Lyrebird (Menura novaehollandiae), a social bird which produces complex, long-lasting vocal displays, showed that they are made up of a mixture of specific calls (warning, aggression, courtship) interspersed with mimicry (known as phatic communication), seemingly purposeless stretches of song which the researcher in fact concludes have the result of strengthening social bonds through maintaining contact:
The term 'social consciousness' has been defined for the purposes of this book as the state of cognitive awareness that underpins social interaction, evidently including some or all of intentionality (the understanding of others as social actors), empathy (awareness of and sympathy with emotional states in others), . . . and self-consciousness (awareness of oneself, and the ability to introspect).
Research by Prior, Schwartz and Güntürkün (2008) shows that the European Magpie (Pica pica), a member of the corvid family, exhibits self-recognition, through use of the mirror test. In apes, self-directed behavior in response to a mirror has been taken as evidence of self-recognition. Say the authors:
There is no clear evidence in fact that self-recognition arose 'independently' in birds and primates. Maybe it did: it is arguable that self-recognition is an inevitable cognitive step that would appear in any species which adopts a social life-style, and that no organic evolutionary adaptation is necessary for it to take place once there is enough neural capacity in the brain; but it is also arguable that the specific neural adaptations that are required for self-recognition are present in all Sauropsids. There are no mirrors in Nature, unless you count a reflecting pool of water. The benefits of self-recognition on its own are therefore not entirely clear. What is required as part of social behaviour is that the animal should recognize conspecifics as different from other types of animal, and itself as one of the group, which is easy enough in most cases. The mirror stuff may just be a spandrel, although it turned out to have its uses when Helen of Troy came along. Humans made mirrors from at least BC 5,000, and they do seem to have been most popular with the ladies:
Writers on animal psychology are generally reluctant to impute such very 'human' characteristics as intentionality to animals, but there are honourable exceptions. Patricia Smith Churchland, writing in Brain-Wise – Studies In Neurophilosophy, allows that chimpanzees and dogs, for example, have at least some degree of intentionality:
Ability to deceive in a social setting has to be one of the major indicators of intentionality. On this test, intentionality has to be allowed to chimpanzees (indisputable) and dogs (very arguable), and it is difficult to see how some of the corvids described above should not pass the test as well. How far intentionality as reflected in the brain structure of corvids can be generalized to other Sauropsids is a difficult question. They all have the same basic brain structure; but we do not – cannot – know if the ancestral Sauropsid had the enlarged pallium (proto-cortex) and the quantity of re-entrant mid-brain and fore-brain circuits that appear to be necessary to support sociality.
As explained above, the presence of these features in many of the diverged branches of Sauropsids argues that they probably did exist in the ancestral Sauropsid, suggesting that at least primitive social consciousness should be allowed as a general Sauropsid feature.
Taking into account these various social behaviours, it is clear that in many Sauropsid species the telencephalon accommodates categorized 'global mappings' (in Edelman's sense) of the animal's internal state and external surroundings, that it has a long-term memory and a 'remembered present', and that it can synthesize these elements into complex behavioural patterns in the light of its affective (hedonic) agendas. This statement is more evidently true of birds, and less obviously true of reptiles.
Taylor (1998) says:
There was in fact no one point at which mammals evolved from a shared Sauropsid ancestor; over a period of 130 million years or more, mammal-like reptiles and reptile-like mammals came and went during a period of multiple extinctions. Something like 180 million years ago viviparous mammals diverged from oviparous (egg-laying) mammal-like reptiles (represented now by the platypus), and approximately 140 million years ago placental mammals (us!) diverged from marsupial mammals. And by the time that the great Cretaceous extinction of roughly 70 million years ago (caused by a meteorite, most people now agree) put paid to the dinosaurs' dominance, mammal-like reptiles had taken on a predominantly mammalian cast.
Whereas in the earliest stages of evolution it was hard to find living representatives of the stages in our direct ancestry, and by the time of the Sauropsids there were multiple types of quite well studied animals, with mammals there is a bewildering variety of possible animals to study, many of which have been the subject of intensive observation.
The skull of squirrels appears to have been highly conserved since the oldest-known squirrel (Protosciurus) appeared in the late Oligocene (approx. 30 million years ago). Squirrels are rodents; recently discovered fossils point to a common ancestor for rodents and lagomorphs (rabbits, hares, etc) in the mid- to late Paleocene (approx. 60 million years ago). This proto-rodent appeared not long after the Cretacean extinction, and may therefore not have been that different from the proto-mammal that survived the extinction.
Squirrels are well known for burying nuts to provide food supplies for the winter. This behaviour has been extensively studied, both on its own and in relation to the food-cacheing behaviour of corvids. Despite persistent reports that smell is involved in the recovery of cached nuts, careful studies seem to have demonstrated that cognitive abilities are more important. Squirrels are able to remember the locations of even hundreds of buried nuts, something that would be impossible for a normal human without external assistance. They appear to remember the location of each nut in relation to features of a large-scale map of the area in which burying takes place (Lavenex, Shiflett, Lee and Jacobs), but also use more than one mapping strategy in order to minimize the chances that seasonal landscape changes will undermine their memories (Gibbs, Lea and Jacobs, 2007).
Perhaps squirrels use smell to recover conspecifics' caches, while using memory to locate their own.
Research had shown that in comparable corvid behaviour, the size of the hippocampus (which plays a major part in laying down long-term spatial memories) grew at the times of year when food-cacheing takes place; but Lavenex, Steele and Jacobs found that there was no comparable change in the squirrel's hippocampus, although it is bigger in those species which bury nuts in many locations rather than centralizing their storage. It is possible that the squirrels' enlarged cortical resources play a greater role in the memorizing process than is the case for the birds.
An important aspect of the squirrels' cacheing behaviour is deception (as indeed is the case for corvids). Steele, Halkin, Smallwood, McKenna, Mitsopoulos and Beam (2008) have shown that free-living eastern grey squirrels (Sciurus carolinensis), when cacheing food in the presence of conspecifics perform behavioural deception by covering additional empty sites where nothing has been cached.
Anecdotally, squirrels have excellent memories, and are well able to get to know and remember individual conspecifics and humans, who often adopt them as pets. They conduct extended behavioural schemes of courtship, food gathering, food-cacheing and interaction with colony conspecifics, to which they will return if interrupted, even for extended periods of time. This suggests that squirrels have autobiographical memory.
Squirrels have excellent vision, even in dim light. They have well-developed senses of hearing and smell. Squirrels also have several sets of vibrissae, thick hairs or whiskers that are used as touch receptors to sense the environment. These are found above and below their eyes, on their chin and nose, and on each forearm.
Scent marking is used to communicate among squirrels. They also use a variety of sounds to communicate, including barks, chatters, distress screams, and high-pitched whines during mating. Squirrels will threaten one another by standing upright with their tail over their back and flicking it.
Due to their dependence on vision for many important tasks such as navigating in their environment, predator avoidance, and foraging for food, visual areas of the squirrel's brain (Lateral geniculate nucleus, V1, superior colliculus, and pulvinar) are prominent, and are thought to be reasonable models for research purposes of comparable aspects of the human brain (Van Hooser and Nelson, 2006).
As described above, the squirrels' olfactory sense has a role in cached nut recovery; it is also important in boundary marking, where various types of secretion may convey information about social status and reproductive readiness. Borgo, Conner and Conover (2006) showed that traces of the scent of various types of squirrel predator and of other squirrel species influence squirrels' choice of nesting sites.
Squirrels from most species are born in litters of between three and nine; the new-born squirrel is naked and blind. Fur begins to grow after about two weeks, and the eyes open after about 30 days, after which the young squirrels may begin to leave the nest for short periods. Mothers typically suckle their young for 50 to 70 days; the kittens are fully independent after about 100 days.
Squirrels are territorial and defend their feeding and nesting areas using complex vocalizations and tail displays. Richardson's Ground squirrel (Spermophilus richarsonii) lives on the American plains in elaborate colonies divided into many local areas, each one occupied by a self-contained group of squirrels (Douvris, 2001). The groups communicate one to another using gestures and calls. Lacey and Wieczorek (2001) studied the mating behaviour of arctic ground squirrels (Spermophilus parryii plesius). Although males occupy and defend territories, at least partly with a view to mating with a female that is also resident on their territory, agonistic encounters between males appeared to be influenced more by the identities of the interacting individuals than by the locations at which encounters occurred. Dominance hierarchies exist, with clearly defined pecking orders; males are not necessarily dominant to females. Dominance or subordination seems to be based on a combination of size and age. Access to females results from a complex interplay of dominance and occupation of territory. Females mate with numbers of males on the one day in a year that they are in oestrus, but usually first with the resident male, and most pregancies result from that first encounter. Significant is that the squirrels clearly know and characterize the other individuals in their group.
Subordinate red squirrels are reported to behave as “floaters” (ie without a fixed territory) or settled on the edges of the ranges of dominant females (Wauters and Dhondt, 1992). This may be normal behaviour for squirrels in their first winter.
Although squirrels are evidently very familiar with their siblings and parents, there is some lack of clarity about the mechanism of their identification with a more extended kin-group. A study by Hare and Murie (1996) suggested that recognition and agonistic behaviour among Columbian ground squirrels (Spermophilus columbianus) owed far more to association during rearing than to relatedness as such, or put in other words, that group behaviour is a consequence of proximity rather than some pheronome or other chemical-based mechanism. Say the researchers:
Mass squirrel migrations in response to exceptional climatic conditions have often been reported, particularly in the USA. One such migration was described as follows:
are enthusiastic communicators, using both vocalization and body signals.
The squirrels' vocal frequency range is from 10Hz to 50,000Hz (humans:
20Hz to 20,000Hz); both vocal calls and tail flicks are used for the maintenance
of territory and hierarchy. Many different types of squirrel call have
been described including buzzing, moaning, squeaking, tooth-chattering,
lip-smacking, growling and a number of other sounds. Squirrels also have
a great variety of body language, often employing their tails. Ultra-high
frequency 'screams' which can be perceived by conspecifics but not by
predators such as hawks are used as alarm calls, and the exact pitch and
volume of the call is thought to include information about the precise
nature of the threat. Squirrels discriminate between reliable and unreliable
conspecifics as communicators: those who 'cry wolf' quickly acquire a
reputation for over-excitement, showing that squirrels
can form a concept of reliability which they can attach to their remembered
knowledge of individuals (Hare and
Many of the components of a high degree of cognitive development have been described above: squirrels have short-term and long-term memory; they have autobiographical memory – a 'remembered present'; they are aware of individuals, and not just among conspecifics; they can formulate and enact complex series of goal-directed behaviours involving deception. This all adds up to something that looks rather like intentionality. Squirrels are highly social and live group-centred lives; they appear to be capable of altruism. Clearly squirrels have social consciousness as it has been defined for this book. At the present stage of our knowledge of a squirrel's mental functioning, it is impossible to say however whether they have a degree of self-awareness – it can't be ruled in or ruled out.
The Mammalian Brain
The main features of the mammalian brain were already laid down at the Sauropsid stage of evolution, or even earlier, and the great enlargement of the mammalian cortex does not introduce a new principle of brain anatomical structure. The other major difference between sauropsid and mammalian brains is the proliferation of re-entrant loops.
The story of the evolution of the mammalian brain is partly one of centralization and partly one of specialization. The reptilian brain, with its three sections, is an historical patchwork in which origination and control of behaviours is spread about in different sections; in mammals it is the fore-brain with its far more highly developed cortex that controls almost all behaviours other than highly instinctive ones, which remain the responsibility of the brain-stem. To perform the controlling role, the cortex needs of course to receive sensory information, albeit in processed form, and the delivery of sensory input to the cortex has become the specialized responsibility of the thalamus. The thalamus is also the conduit towards the cortex of re-entrant loops, which have become a distinguishing feature of the mammalian brain. In many situations, the cortex works on a 'what if' principle, proposing actions which are reviewed by mid-brain structures in the light of hedonic agendas, memory and ongoing somatic representations, with the re-entrant feedback circuit acting to modify or inhibit the proposed action when appropriate.
Whereas in the reptilian brain the body image occupies part of the mid-brain, in mammals it resides in the motor cortex. Both are topographically organized, and in mammals the thalamus has matching topographical organization, so that re-entering motor signals return to the correct region of the motor cortex. Of course the decision-making cortex does not work in isolation: it makes its proposals in the light of the current sensory state of the animal and the animal's affective agenda.
In reptiles the body image used to generate motor commands and the equally topographical image representing the animal's sensory state in relation to the outside world share the same neural space in the mid-brain. In lower mammals such as the hedgehog this arrangement has been transferred relatively unaltered to the cortex, but in higher mammals the two maps sit alongside each other. The transfer to the cortex required two wholly new sections of the thalamus, known as the ventral lateral nucleus (for body image) and the ventral posterolateral nucleus (for sensory image), alongside other existing pathways, particularly those for non-topographical sensory (especially visual) and affective input (notably from the amygdala).
Output from the cortex resulting from the decision-making process based on incoming sensory information follows three main paths, each being an elaboration of a pathway that already existed in the reptilian brain but had partially different purposes.
Topographically organised motor commands travel to the basal ganglia (of which the striatum, heavily influenced by the amygdala, is the most prominent component) before returning via the thalamus to inhibit or permit the originating commands; the motor cortex, the basal ganglia and the cerebellum work together in a complex way before the cerebellum is, so to speak, finally permitted to release the motor command for execution. The circularity and complexity of the process is what allows humans and other advanced mammals to imagine and practise motor sequences before they take place in the physical world.
Memory is of course a crucial part of the planning, imagining and rehearsing sequence. The second main output path from the cortex is to the hippocampus, which governs the laying down of memories, something that is reinforced by constant repetition, whether real or imagined. The hippocampus, which in reptiles (see above) is responsible for the ordering of motor sequences at a gross level and is therefore a key player in the maintenance of short-term memory, is in mammals connected in turn (as ever, through the thalamus) with a new part of the cerebrum, the cingulate cortex, which runs parallel to those areas of the neo-cortex which house the body image and the sensory image. The cingulate cortex, which can be regarded as the seat, or at least the enabling apparatus, of long-term memory, works in close association with the neo-cortical body and sensory images, so that the process of envisioning a motor program can at its simplest be seen as a collaboration between the neo-cortex (the current state of things), the cingulate cortex (linked memories) and the hippocampus (articulating and continually reinforcing the links between current behaviour and related memories).
It is of course the frontal cortex which exercises the higher planning and goal-setting functions in mammals. The combination of the images and memories held in the cortex allows the animal to construct for itself a representation of space over time in which it can, so to speak, move around freely, predicting the spatial consequences of movement sequences. However a third major component of coherent and appropriate behaviour is goal-setting and planning. This is the role of the third main cortical output pathway, originally concerned with olfactory information. In the reptilian brain, the olfactory pathway strongly connects the reptilian dorsal ventricular ridge (DVR – possible precursor of the mammalian neo-cortex) with the amygdala (concerned with arousal, fear and anger) and the hypothalamus (concerned with hunger and sexual desire). In mammals this output route still exists, but reconnects back to the frontal neo-cortex via yet another new thalamic pathway.
Obviously, the most salient fact about advanced animals' brains is that they are much bigger in relation to body weight than is the case for animals at earlier stages of evolution. The relationship of brain weight to body weight matters more than absolute brain size, and within the brain, the relative size of the cortex (or pallium, in earlier types of animal) to that of the whole brain. In higher animals the cortex comes to make up a far higher proportion of total brain mass.
Table Two shows the progression of brain weight and of cortical volume through the course of evolution (in arriving at estimates of cortical volume for the earlier types of animal there are major problems of function and differentiation, so that the figures given are far from robust).
Multiple sources include: Cnotka et al (2008), Falk, Evolution of the Primate Brain (2005), Trends in Neurosciences (1995); Handbook of Palaeoanthropology, Vol. 2: Primate Evolution and Human Origins; Rilling, 2006; Platel (1976), Changizi and Shimojo (2005)
NB The numbers in columns 2 to 4 do not allow for differences in absolute body size; scales which do this are called allometric, and attempt to compensate for differences in body weight. The great ape is not so much smaller than a human, so the figures in the Table are roughly comparable; but the cat is thirty times smaller than a human; its allometrically adjusted brain weight as compared to a human would be several times lower than shown in the Table. Allometrically adjusted brain capacities are known as encephalization quotients, and are shown for some animals in column 5. It should be noted that crows have much larger brains than most types of bird, and that most of the extra encephalization is represented by the pallium (cortex equivalent).
Why did evolution deem it necessary to create such an energetically expensive organ as the neo-cortex of the mammalian brain? The degree of motor activity demonstrated by an animal is often quoted as a driver of comparative brain size, and this is indisputably a factor; but it seems inadequate to explain the difference in brain sizes between, say, a frog and a squirrel.
The irresistible conclusion is that increased brain size and cortical dominance is associated with increasing sociality; and this view has increasingly come to have general acceptance during the last hundred and fifty years. The necessary concomitant of increased sociality is an increased ability to behave appropriately towards conspecifics, and an increased awareness on the part of individual actors in a social dialogue that they are indeed taking part in a meaningful interplay, leading by degrees and inevitably to some kind of awareness of self – what is usually called self-consciousness.
Self-Awareness In Mammals
This chapter has concentrated on the gross anatomical and behavioural characteristics of an assortment of animals, and it has shown the close association between sociality and cognitive achievement. In the squirrel it has brought us to the edge of sentience, the beginnings of self-awareness. The next chapter will focus rather on the neural mechanisms that give expression to sociality and 'groupishness', before in Chapter Three all the components of behaviour, brain functioning and sociality are brought together in Homo sapiens to enable self-awareness and meta-cognition.
Arendt, D, Tessmar, K, de Campos-Baptista, M I, Dorresteijn, A and Wittbrodt, J (2002) Development of Pigment-Cup Eyes in the Polychaete Platynereis Dumerilii and Evolutionary Conservation of Larval Eyes in Bilateria, Development 129(5), pp 143-154
Bernier, B, Bar, I, Pieau, C, De Rouvroit, C L and Goffinet, A M (1999) Reelin mRNA Expression During Embryonic Brain Development in the Turtle Emys Orbicularis, The Journal of Comparative Neurology, 413(3), pp 463-479
Bogert, C M (1960) The Influence of Sound on the Behavior of Amphibians and Reptiles, in Animal Sounds and Communication, Ed. Lanyon, W E and Tavolga, W N, American Institute of Biological Sciences, Washington DC
Brown, L and Gruber, S H (2004) The Social Behaviour of Sharks, at http://www6.miami.edu/sharklab/research_socialbehavior.html, Manchester Metropolitan University, England
Clayton, N S, Dally, J M, Gilbert, J D and Dickinson, A (2005) Food Caching by Western Scrub-Jays (Aphelocoma Californica): A Case of Prospective Cognition? Journal of Experimental Psychology: Animal Behavioural Processes, 13, pp 115-124
Cooper, W E Jr. and Greenberg, N (1992) Reptilian Coloration and Behavior, in Hormones, Brain, and Behavior: Biology of the Reptilia, volume 18, Physiology, ed. Gans, C and Crews, D, pp 298-422, University of Chicago Press, Chicago
Douvris, C (2001) A Practicum Submitted to the Faculty of Graduate Studies in Partial Fulfillment of the Requirements for the Degree of Master of Landscape Architecture, Department of Landscape Architecture, University of Manitoba, Winnipeg
Hare, J F and Murie, J O (1996) Ground Squirrel Sociality and the Quest for the "Holy Grail": Does Kinship Influence Behavioral Discrimination by Juvenile Columbian Ground Squirrels? Behavioral Ecology, 7(1), pp 76-81
Hartdegen, R W, Russell, M J, Young, B and Reams, R D (2001) Vocalization of the Crocodile Skink, Tribolonotus Gracilis (de Rooy, 1909) and Evidence of Parental Care, Contemporary Herpetology, 2, pp 1094-2246
Heimberg, A M, Cowper-Sallari, R, Sémonc, M, Donoghue, P C J and Peterson, K J (2010) MicroRNAs Reveal the Interrelationships of Hagfish, Lampreys, and Gnathostomes and the Nature of the Ancestral Vertebrate, PNAS vol. 107 no. 45, pp 19379–19383, doi: 10.1073/pnas.1010350107
Lavenex, P, Shiflett, M W, Lee, R K and Jacobs, L F (1998) Spatial Versus Nonspatial Relational Learning in Free-Ranging Fox Squirrels (Sciurus Niger), Journal of Comparative Psychology, 112(2), pp 127-136
Lettvin, J Y, Maturana, H R, McCulloch, W S and Pitts, W H (1968) What the Frog's Eye Tells the Frog's Brain, Reprinted from: The Mind: Biological Approaches to its Functions, ed. Corning, W C and Balaban, M, pp 233-258
Loonen, A J M and Ivanova, S A (2015) Circuits Regulating Pleasure and Happiness: the Evolution of Reward-Seeking and Misery-Fleeing Behavioral Mechanisms in Vertebrates, Front Neurosci. 2015; 9: 394. Published online 2015 Oct 23. doi: 10.3389/fnins.2015.00394 PMCID: PMC4615821
R A, Hammerschlag, N, Collier, R S and Fallows, C (2005) The Predatory
Behaviour of White Sharks
Mathis, A, Schmidt, D W and Medley, K A (2000) The Influence of Residency Status on Agonistic Behavior of Male and Female Ozark Zigzag Salamanders, Plethodon Angusticlavius, The American Midland Naturalist 143, pp 245-249
R (1976) Comparative Volumetric Analysis of the Main Subdivisions
of the Brain in Saurian Reptiles, J Hirnforsch. 17(6),
Raikova, O I, Reuter, M, Jondelius, U and Gustafsson, M K S (2000) An Immunocytochemical and Ultrastructural Study of the Nervous and Muscular Systems of Xenoturbella Westbladi (Bilateria inc. sed.), Zoomorphology 120(2), pp 107-118
Ram, J L, Fei, X, Danaher, S M, Lu, S, Breithaupt, T and Hardege, J D (1999) Finding Females: Pheromone-Guided Reproductive Tracking Behavior by Male Nereis Succinea in the Marine Environment, The Journal of Comparative Neurology, 413(3), pp 463 – 479
Steele, M A, Halkin, S L, Smallwood, P D, McKenna, T J, Mitsopoulos, K and Beam, M (2008) Cache Protection Strategies of a Scatter-Hoarding Rodent: Do Tree Squirrels Engage in Behavioural Deception? Animal Behaviour, 75(2), pp 705-714
Tessmar-Raible, K, Raible, F, Christodoulou, F, Guy, K, Rembold, M, Hausen, H and Arendt, D (2007) Conserved Sensory-Neurosecretory Cell Types in Annelid and Fish Forebrain: Insights into Hypothalamus Evolution, Cell, 129(7), pp 1389-1400
Wicht, H and Northcutt, R G (1998) Telencephalic Connections in the Pacific Hagfish (Eptatretus stouti), with Special Reference to the Thalamopallial System, The Journal of Comparative Neurology, 395(2), pp 245-260
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