Evolutionary trends in nervous systems and behaviour

As we ascend the evolutionary scale from simple unicellular organisms to vertebrates, the organisation and complexity of sensory and motor responses, and, in multicellular animals, nervous systems, change in two major ways: first towards greater differentiation, and second towards greater centralisation (see Guthrie 1980).

3.1.2.1 Unicellular organisms

Even in unicellular organisms, without any nervous system at all, there can be spatial differentiation between sensory and motor functions. Paramecium, for example, is an aquatic protozoan covered with motile cilia (hair-like processes) that propel it in a helical fashion through the water. When Paramecium collides with an obstacle, a mechanoreceptor at the anterior end is stimulated, causing the direction of beating of the cilia to be reversed and the organism to back away and move off in a different direction (Fig. 3.3a). If it is hit from the rear, a posterior mechanoreceptor triggers a forward thrust. But how do the mechanoreceptors manage to communicate information to the cilia in the absence of nerve fibres? The answer seems to be by causing changes in the electrical potential of the cell membrane, which are then picked up by each of the cilia in turn. In short, the entire organism acts like a single nerve cell. As in a neuron, there is a negative resting potential across the membrane. When the anterior mechanoreceptor fires, it causes a drop in the potential which spreads over the whole cell and is detected by voltage-sensitive channels around each of the cilia (Fig. 3.3b). The channels open to allow calcium to flow into the cell down its concentration gradient. The calcium then interacts with the cilia to reverse their beat before being pumped out of the cell again. Stimulation of the rear receptor increases potassium permeability, which raises the membrane potential and increases the rate of beating of the cilia and thus forward propulsion. Thus the location of the mechano-receptors determines the sign of the change in the membrane potential and, through that, the direction of beating of the cilia and the subsequent movement of the organism.

3.1.2.2 Nervous systems and behaviour in invertebrates

Although Paramecium can respond in a directed way to stimuli from its environment, control is limited because the means of linking receptors to effectors is relatively unrefined. In multicellular animals, this role is taken over by the axons and dendrites of neurons and the various synapses between them. In an advanced nervous system, there are five major components linking stimulus perception and motor response: (a) a cell or group of cells acting as a sensory receptor, (b) an afferent or sensory neuron carrying impulses from the sense cells, (c) an efferent or motor neuron carrying impulses to effector cells, (d) an internuncial neuron or interneuron linking sensory and motor neurons, and (e) an effector organ (that performs the motor task).

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Nerve nets

Examples of this link-up system at its simplest are found in the nerve nets of cnidarians (sea anemones, jellyfish and their relatives) and echinoderms (starfish, sea urchins, etc.).

The simplest kind of net is the type found in the sedentary freshwater cnidarian Hydra (Fig. 3.4a), which lies just under the epidermis and consists of a series of synaptically linked bipolar and tripolar (two and three connections respectively) cells. Transmission is slow because impulses have to traverse large numbers of synapses and lack directionality, thus dissipating in several different directions. Trends in other cnidarians, which still pos-sess nerve nets, are towards the differentiation of nerve cells into fast-conduction tracts (e.g. Fig. 3.4b), mainly through the lengthening and thickening of individual axons.

Impulses can then be channelled in particular directions to bring effector organs into play more rapidly. The rapid withdrawal reaction of anemones such as Actinia and Metridium is a good example.

The behaviour of animals relying on nerve nets is characteristically stereotyped (unvarying). Most exhibit simple reflexes (see 3.1.3.2), stereotyped motor sequences and rhythmic locomotory activities. Even more elaborate behaviour patterns, such as shell-climbing in epizooic (living on other animals) anemones, consist of only three or four elements. There is relatively poor stimulus discrimination, and such learning as exists consists of habituation (6.2.1.1) and reflex (3.1.3.2) facilitation rather than any Figure 3.3 The avoidance response of Paramecium. (a) After colliding with an object, Paramecium reverses its direction of locomotion and backs away. (b) Forward and reverse movements are driven by different changes in membrane potential (curves show responses to three different stimulus intensities). See text. After Collett (1983) and Randall et al. (1997).

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Figure 3.4 (a) The nerve net of Hydra; (b) the concentration of neural tissue into nerve rings in a hydroid medusa;

(c) the CNS of a turbellarian flatworm; (d) and (e) the segmental arrangement of ganglia and nerves in the CNS of an oligochaete worm (Lumbricus terrestris) and a cockroach (Periplaneta americana). After Chapman & Barker (1966) and Barnes (1968).

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form of associative learning (6.2.1.2). However, these simple responses function well in the animals’ relatively stable aquatic environment with its ample food supply and opportunities for passive dispersal.

Nerve tracts and centralisation

In the Cnidaria, through-conduction tracts are little more than local channels in an otherwise diffuse net. In relatively more advanced invertebrates, such as flatworms (Platyhelminthes), the tracts become more pronounced and the nervous system begins to show signs of the second major evolutionary trend, centralisation (Fig. 3.4c). Even within the Cnidaria there is a trend towards more deeply seated nerve rings (Fig. 3.4b) and tracts in more mobile species, but flatworms are the first level of life to possess a recognisable central nervous system (CNS). They are also the first to show the early stages of cephalisation, the concentration of nervous tissue in the head region into an anterior ganglion or simple brain. In bilaterally symmetrical organisms (those with distinct ‘head’ and ‘tail’ ends), incoming information arrives mainly at the front as the organism moves forward through its environment. Consequently there is an obvious advantage in concentrating sensory and integration centres at the anterior end. Two nerve cords, linked by nerves in a ladder-like arrangement (Fig. 3.4c), extend down the body from the anterior ganglion.

Nerve fibres extend from the cords to all regions of the body in a network arrangement, constituting the peripheral nervous system. The division into a central and peripheral nervous system is common to most invertebrates and all vertebrates, but is seen in its simplest form in the flatworms. In general, the CNS houses most of the motor nerve cell bodies, while the peripheral nervous system contains the sensory receptors.

Sensory cells in the head region of flatworms such as Planaria respond to various stimuli, including temperature, touch and chemical changes in the water. Changes in light intensity can also be registered by a pair of eyespots (clusters of photoreceptor cells). Impulses from the various sensory receptors are routed to the anterior ganglion and from there to the appropriate muscles. The nerve cords allow much more rapid transmission of impulses than nerve nets, with a consequent enhancement in the speed and variety of behavioural responses to different environmental stimuli. The increased differentiation and centralisation of the nervous system in flatworms is also associated with a degree of learning ability, for example learning which way to turn in a T-maze to avoid a noxious mechanical stimulus, and with relatively sophisticated mechanisms of assessment during mate choice (Vreys & Michiels 1997; see Chapter 10).

Nerve cords and ganglia

In the higher invertebrates, which include the metamerically segmented (animals with a serially segmented body plan) annelids (earthworms, ragworms, etc.) and arthropods (crustaceans, insects, spiders, etc.), and the non-metamerically segmented (it is generally assumed) molluscs, the nervous system has become differentiated into a series of ganglia linked by nerve cords lying near the ventral surface of the body (Fig. 3.3c–e). This increasing centralisation has produced a kind of neural ‘switchboard’. Afferent fibres from sensory receptors plug into the central switchboard where a mass of interneurons is ready to connect them with a variety of motor neurons. Depending on the type of input from a sensory receptor, different motor neurons are brought into play so that the animal can respond appropriately.

Ganglia (other than cerebral ganglia) in the CNS may contain anything from 400 cells (in leeches) to over 1500 (in the mollusc Aplysia). Well-defined tracts and glomeruli

(aggregations of neuron terminals) can also be distinguished, especially in the cerebral ganglia which may form an elaborate brain-like structure. The primary function of each ganglion is the regulation of local reflex arcs, providing for a degree of local con-trol of movement impossible with a diffuse nerve net. Ganglia also exercise longer-range control via long interneurons extending along the nerve cords, thus facilitating the coordinated operation of different parts of the body. A number of behavioural advances are associated with these developments. In particular, elaboration of appendages and musculature, aided by the emergence of a fluid-filled body cavity (the coelom), makes subtle movements and complex, manipulative tasks possible, as, for example, in the web-building activities of spiders and the elaborate courtship songs and ornamented nest constructions of some insect species. Stimulus discrimination and learning also show advances over species with less structured nervous systems. However, learned responses are seldom retained for long, probably because of the small capacity of the cerebral ganglia, itself perhaps a reflection of the short-generation life cycles of many invertebrate species – where there is little time for sophisticated learning, simple pre-programmed responses may be more economical (see Chapter 5).

Among the invertebrates, there is a trend towards enlargement of the ‘brain’ by amalgamation of somatic ganglia, and an increase in the brain’s control over regional centres. Despite the increasing importance of the brain, however, the somatic ganglia still retain considerable independence of control. Earthworms, for instance, can crawl normally, feed, copulate and burrow after removal of the cerebral ganglia, though they are hyperactive and their movements phrenetic. Nereid species (ragworms) are able to learn certain tasks, or persist with previously learned tasks, after disconnection of the cerebral ganglia from the rest of the CNS. The cerebral ganglia thus appear to be just one of several memory storage sites.

Independent control of behaviour by somatic ganglia is particularly well developed in arthropods. If still connected to its ganglion, the isolated leg of a cockroach (Periplaneta americana) will continue to show stepping movements when stimulated appropriately by pressing on the trochanter (articulating joint in the upper leg). Indeed, even if the ventral nerve cord is completely severed, coordinated walking can be elicited by stimulating a single leg. Movement of one leg exerts a traction force on the leg behind, stimulating specialised proprioceptors (cells sensitive to mechanical stimulation) called campaniform organs and eliciting a reflex response (Zill & Moran 1981). Even in cephalopods (squid and octopuses), where cephalisation has reached its peak within the invertebrates, many responses are still under the control of somatic ganglia. A constraint on the octopus’s (Octopus vulgaris) otherwise impressive object learning prowess is its inability to distinguish objects by weight. This is because the movements of each tentacle are regulated by local axial ganglia, so that information from proprioceptors in the tentacle are processed in the ganglia rather than being passed to the brain where it could become available for learning.

Evolutionary trends in invertebrate brains

The brains of invertebrates vary considerably in structure and complexity. At the lower end of the scale, flatworms brains contain some 2000 cells. Insect brains are intermediate, with around 340 000, whereas those of cephalopods contain up to 170 million, almost a tenth of the number found in the human brain. Despite its outwardly advanced appearance, however, the anatomy of the cephalopod brain reveals its derivation from amalgamated somatic ganglia. The cephalopod CNS contrasts sharply with the loose string of ganglia (comprising fewer than 50 000 cells in total) found in the slower moving gastropod (slugs, 3.1 ⁿ Nervous systems and behaviour x ₁₀₃ AB_C03.qxd 9/17/07 8:05 PM Page 103

snails) and lamellibranch (bivalve) molluscs. There are separate visual and tactile learning centres within the lobes of the brain, and centres for the integration of visual information from the high-resolution eye, and tactile information from the mobile tentacles.

Among arthropods, brain structure is remarkably conservative. In common with annelids, it develops as three main regions: (1) the protocerebrum, the main components in arthropods being the paired optic lobes, the median body and the corpora pedunculata, each functioning in the integration of information from the anterior sense organs and the control of subsequent behaviour; (2) the deuterocerebrum, containing association centres for the first antennae; and (3) the tritocerebrum, nerves from which extend to the upper alimentary canal, second antennae (where they exist) and the upper ‘lip’.

The same functional zones can be recognised throughout most of the phylum and are derived from homologous zones in the polychaete annelids (ragworms). Within broad taxonomic groups, the relative size of different centres in the brain reflects differences in predominant sensory modalities and lifestyle (see 3.1.3).

The gross plan of the CNS in arthropods, with its central nerve cord and ganglia in each segment, is broadly similar to that in annelids. The segmental arrangement is clearly discernible in primitive arthropods, but is obscured in advanced forms by extens-ive fusion of ganglia (Fig. 3.5a), a development that also characterises more advanced nervous systems in molluscs (Fig. 3.5b). The general tendency towards fusion of ganglia in invertebrate nervous systems goes hand in hand with the evolution of more sophisticated sensory systems and behaviour.

3.1.2.3 Nervous systems and behaviour in vertebrates

In vertebrates, the nervous system develops from dorsal tissue and as a tube rather than as a solid structure. Nevertheless, traces of the ancestral segmental pattern remain in the dis-tribution of sensory and motor zones within the system. Centralisation, cephalisation and the functional differentiation of the nervous system reach their peak in the vertebrates.

Indeed, while structural centralisation occurs at various levels of the evolutionary scale, true centralisation of function is the exclusive property of the vertebrate nervous system.

Figure 3.5 The trend towards fusion of ganglia in the CNS of higher invertebrates: (a) the house fly (Musca domestica) and (b) the Roman snail (Helix pomatia). After Chapman (1971) and Barnes (1968).

Structure and function in the CNS

The vertebrate CNS consists more clearly than that of invertebrates of two principal components: the brain and the spinal cord. The spinal cord comprises an outer region of mostly myelinated tracts (so-called ‘white matter’) connecting the brain with spinal control centres, and an inner region of neuron cell bodies (‘grey matter’). The dorsal horns of the inner region accept afferent, sensory neurons entering the CNS, while the ventral horns send out efferent motor fibres. The arrangement of axon and cell body material in the vertebrate spinal cord is the opposite of that in the invertebrate CNS, where the open circulatory system requires cell bodies to be exposed in the haemocoel (body cavity).

The brain develops as three major regions: the forebrain (prosencephalon), the mid-brain (mesencephalon) and the hindmid-brain (rhombencephalon) (Fig. 3.6). The foremid-brain is further divided into two parts: the anterior telencephalon, associated with olfaction and giving rise to the cerebral cortex, and the posterior diencephalon with its pathways connecting with the pituitary gland. The roof of the midbrain houses the optic lobes, or optic tecta in lower vertebrates, while a dorsal projection of the hindbrain, the cerebellum, acts a major coordination centre for movement by integrating messages from receptors in joints and muscles, though it also plays a role in higher brain functions and cognition in advanced vertebrates (Riva 2000). The hindbrain is also divided into two parts: the metencephalon, containing the anterior part of the medulla oblongata, the cerebellum and, in mammals, the pons and the myelencephalon, which contains the posterior medulla oblongata. The medulla oblongata is the centre of control for certain vital functions, including breathing and blood vessel tone. It contains a number of nuclei for the cranial nerves, including the vagus nerve, which is concerned with heart and gastro-intestinal reflexes, and large numbers of fibres pass through it on their way between the spinal cord and the forebrain cortex.

The relatively simple arrangement of ‘white’ and ‘grey matter’ in the spinal cord is extensively modified in the brain. Here it is the central regions surrounding the fluid-filled ventricles that originate in the outer regions of the spinal cord. The outer areas of the brain are specialised tissues consisting of dense masses of cell bodies homologous with the ‘grey matter’ of the spinal cord. The regions of the brain other than the cerebral cortex, and sometimes other dorsal lobes, are often referred to as the brain stem. The brain stem is the most primitive part of the brain. As well as acting as a conduit for information from the body flowing into the brain, various centres in the brain stem determine general alertness and regulate, as we have seen, the automatic maintenance processes of the body such as breathing and circulation.

3.1 ⁿ Nervous systems and behaviour x ₁₀₅ Figure 3.6 A generalised scheme of the

vertebrate brain, showing the major regions and pathways of sensory input (arrows).

After Guthrie (1980).

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Evolutionary trends in vertebrate brains

Vertebrate brains show two main evolutionary trends. The first, exemplified by the bony fish (Actinopterygii), is an elaboration of the midbrain in which the optic tectum becomes thickened and stratified and acts as a major integration centre for information from other parts of the brain. The diencephalon lies underneath it and differentiates into the central thalamus and the ventral hypothalamus and pituitary. The second trend, shown in mammals, involves the elaboration of the cerebral hemispheres of the forebrain, which now become the major association centres (Fig. 3.7a,b). The forebrain of the lower vertebrates remains in the form of the hippocampus and some other ventrolateral

Figure 3.7 Schematic diagram of the brain of (a) a teleost fish and (b) a mammal, showing developments of the major regions (see Fig. 3.6) and connecting pathways (arrows). Note the elaboration of the optic tectum in fish and the cerebral cortex in mammals (see text). After Guthrie (1980).

elements, but the cerebral hemispheres themselves consist of new material, the neocortex, which, in humans, has extended to cover the rest of the brain. A plot of the relationship between brain and body size in vertebrates emphasises the discontinuity caused by the elaboration of the forebrain cortex in higher vertebrates (Fig. 3.7c). In lower vertebrates, the brain accounts for less than 0.1% of the body mass, while in birds and mammals it often exceeds 0.5% with a high extreme of 2.1% in humans.

The neocortex has several externally visible divisions, many of which reflect different functional areas (Fig. 3.8a). In advanced mammals, voluntary motor control areas lie in front of those for somatic sensory functions and are separated from them by the deep central fissure. A proportion of the motor cortex cells communicate directly with the spinal cord via a large through-conduction pathway, the pyramidal tract (Fig. 3.7b). The two halves of the cortex are connected by another large tract, the corpus callosum.

Severance of the corpus callosum in humans has revealed pronounced differences in the functional dominance of the left and right hemispheres, for instance in the control of speech (usually a left hemisphere job) and verbal comprehension (right hemisphere).

Further motor control occurs subcortically in various centres, an important one being the corpus striatum. In birds, the corpus striatum is an association centre controlling the performance of stereotyped behaviour patterns. In mammals, it houses the basal ganglia which coordinate motor control by acting as ‘switches’ for impulses from different motor systems. Damage to the basal ganglia, or the cells immediately communicating with them (as in Parkinson’s disease) results in passive immobility as the nuclei can no longer send motor messages to the muscles. A second set of subcortical nuclei, the limbic system, 3.1 ⁿ Nervous systems and behaviour x ₁₀₇

Figure 3.7 (continued) (c) The relationship between brain and body mass (‘encephalisation quotient’) in extant higher and lower vertebrates. The plot shows minimum convex polygons

Figure 3.7 (continued) (c) The relationship between brain and body mass (‘encephalisation quotient’) in extant higher and lower vertebrates. The plot shows minimum convex polygons