The Protocerebrum

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The ground structure of the protocerebrum suggests its ancestral affinities with segmental ganglia. In the protocerebrum, as in postoral ganglia, ascending sensory interneuron tracts enter it ventrally, whereas premotor interganglionic interneurons exit dorsally. Afferents (here the optic lobe output neurons; see later) distribute to local interneurons in a manner reminiscent of sensory afferents within postoral ganglia.

Despite its basic similarities with segmental ganglia, the protocerebrum contains neuropils that are not normally found in other segments and appear to have no counterparts in other ganglia, unless generated ectopically by genetic manipulation. Unique protocerebral neuropils comprise: (1) the central complex and (2) the mushroom bodies and some satellite neuropils belonging to both of these. A midline indentation between the two protocerebral lobes, called the pars intercerebralis, with its accompanying populations of neuromodulatory neurons, may also be unique to the protocerebrum. But without the relevant developmental studies on thoracic ganglia, it is not clear whether any of the unique clusters of neurons at their dorsal midlines are segmental counterparts of neurons at the pars intercerebralis.

The structure of the protocerebrum is best approached by understanding the basic organization of major axon tracts that extend between its two halves. Studies of Drosophila embryos show that major cerebral tracts appear early in development and pioneer the trajectories of interneurons linking later developing neuropil regions. Again, research by Boyan and colleagues on the development of locust embryos provides important insights into early brain development and demonstrates that neurons developmentally ascribed to the protocerebrum can actually end up distant from it in the adult. For example, studies of engrailed expression show that in locusts the first episode of neuroblast generation in the protocerebrum includes three neuroblasts that migrate caudally to lie beside the glomerular antennal lobes, which are structures usually ascribed to the deutocerebrum. The segmental origin of these three neuroblasts, which contribute neurons to the antennal lobe system, cautions against uncritically ascribing segmental identities to neurons in the adult brain.

Nevertheless, many of the tracts and neuropils described from the adult have been both ascribed to one of its segments and named, even though only a few are yet understood at a functional and developmental level. The reader is referred to two brain atlases, one by Strausfeld and the other an electronic publication, FLYBRAIN (, both of which focus on the adult structure of dipteran brains (the housefly Musca domestica and the fruit fly D. melanogaster). The basic divisions of the Drosophila brain are shown in Figs. 1—6. The following neuropils, or neuropil groups, comprise the salient regions of the adult protocerebrum.

The Central Complex

Insect and crustacean protocerebra contain unique midline neuropils and, in more advanced taxa, satellite neuropils associated with them. These structures and their interrelationships have been described by several authors, one cardinal study being by L. Williams in 1975. This and other studies summarized here are described in some detail in a recent article by Strausfeld published in 1999.

The midline component of the central complex, called the central body, is similar to a unique midline neuropil in the brains of chilopods, branchiopod crustaceans, and archaeog-nathan insects. Comparative studies suggest that these neuropils have become elaborated through time. In the flightless Zygentoma (e.g., "silverfish") as well as in the Palaeoptera (e.g., mayflies and dragonflies), several paired satellite neuropils are reciprocally connected to two midline neuropils: the columnar ellipsoid body and, above it with respect to the brain's neuraxis, the fan-shaped body, which is usually recognized by its scalloped profile. Further elaboration has occurred in the Neoptera, in which a distinct stratum called the superior arch is attached to the fan-shaped body anteriorly. A bridge of neuropils, called the protocerebral bridge, connects the two protocerebral lobes and provides axons that extend into the fan-shaped body and to the ellipsoid body behind it. In many taxa (e.g., locusts, flies, wasps) the protocerebral bridge is divided into 16 discrete modules, 8 each side of the midline. These connect to the 16 modules of the fan-shaped body and ellipsoid body. The most lateral module on one side of the bridge is linked to the most medial module of the other side. The next most lateral module is linked to the next most medial one, and so on. These connections provide an elaborate pattern of chiasmata between the bridge and the fan-shaped and ellipsoid bodies. Some of these neurons also extend to a pair of ball-like structures, called the noduli, situated caudally with respect to the fan-shaped and ellipsoid bodies. Two synaptic zones in the noduli, a core and an outer layer, receive connections from the fan-shaped body such that one-half is represented in the core of the contralateral nodulus, whereas the other half is represented in the outer layer of the ipsilateral nodulus. A recent account by Renn and colleagues (see FLYBRAIN database) uses genetic markers to dissect these various components and trace their development.

The protocerebral bridge receives a system of elongated fibers from the medial protocerebrum, which is itself supplied by terminals of ascending interganglionic interneurons that originate in thoracic ganglia. These elongated protocerebral fibers extend through dendritic trees that contribute to the modules across the bridge and are assumed to provide inputs to their dendrites, although this awaits confirmation.

The superior arch appears to be distinct from protocerebral bridge inputs and is connected heterolaterally to neuropils of the protocerebral lobes, themselves receiving terminals from the median bundle, a midline tract originating from the subesophageal ganglion and ventral cord and ascending along the midline of the ventral surface of the protocerebrum. The superior arch shares local interneurons with the fan-shaped body and ellipsoid body.

The fan-shaped body and ellipsoid body each receive fanlike terminals from axons that originate at dendritic trees in various lateral neuropils of the protocerebrum. Both the ellipsoid and the fan-shaped bodies supply outputs that extend to lateral protocerebral neuropils, particularly a ventrocaudal region called the ventral bodies, known also as the lateral accessory lobes. These lobes are invaded by the dendritic collaterals of many of the descending neurons leaving the brain for thoracic and abdominal ganglia.

The central complex is strictly a higher center that is distant from sensory inputs. Dye fills fail to demonstrate any sensory interneuron inputs to central complex neuropils nor do the antennal lobes or optic lobes provide direct connections to the central complex. The central complex has no direct connections with the mushroom bodies. Instead, various regions of the protocerebrum that are connected to the central complex are also connected to the mushroom bodies and to higher level sensory neuropils, such as the lobula of the optic lobes and antennal and vertical lobes of the deutocerebrum (see later).

As described in Nassel's 1993 review, the central complex is richly supplied by peptidergic neurons that originate from the pars intercerebralis. The pars also provides a wealth of peptidergic neurons whose axons leave the brain for the retro-

cerebral complex (the corpora allata and corpora cardiaca) via the corpora cardiaca nerve NCC1. Other neurosecretory cells sending axons out of the brain lie lateral and rostral with respect to the protocerebrum (NCC2) and in the lateral tritocerebrum (NCC3). An exquisitely detailed enhancer trap analysis of these systems has been published by Siegmund and Korbe. The central complex is implicated in the control of motor actions, although exactly what it controls is not yet known. Studies of motor-coordination-defective Drosophila show that certain behavioral mutants have midline lesions of their protocerebral bridge or the fan-shaped bodies. Roland Strauss, at the University of Würzburg, has shown that these mutant flies are incapable of adjusting step length during turning. A similar disruption across the midline occurs in nature: certain rowing Heteroptera, such as the water strider Gerris, have split protocerebral bridges, minute noduli, and reduced modules in their fan-shaped and ellipsoid bodies. In contrast, insects that show sophisticated asymmetric but highly coordinated limb actions, such as are employed in grooming, object manipulation, or cell construction, possess elaborately modular central complexes and complete protocerebral bridges.

Prominent connections between the fan-shaped and the ellipsoid bodies with the lateral accessory lobes of the protocerebrum are of functional interest. The lateral accessory lobes are visited by dendritic collaterals from many of the interganglionic descending interneurons that send axons from lateral protocerebral regions to neuropils of the thoracic and abdominal ganglia. One interpretation of this organization is that the central complex plays a role in gating outgoing information from the brain.

The central complex is richly supplied from protocerebral regions involved in sensory discrimination. This organization, with the elaborate arrangement of repeat units (modules and chiasmata) within and between the protocerebral bridge and midline neuropils, might suggest that the central complex assesses the context and occurrence of sensory stimuli around the animal and that this plays a crucial role in modifying descending information to motor circuits.

Mushroom Bodies

The mushroom bodies, discovered by Félix Dujardin in 1850, were the first brain centers to be recognized as distinct entities. Dujardin's suggestion that mushroom bodies supported intelligent actions was with reference to social insects, in which mushroom bodies are largest and most elaborate. Since his 1850 paper, the mushroom bodies have been considered to be centers crucial to learning and memory.

The mushroom bodies are paired lobed neuropils. Comparative studies by Strausfeld, Ito, and others have identified mushroom bodies in all groups of insects except the archaeognathan. In zygentoman and palaeopteran insects, mushroom bodies comprise two sets of lobes, one set extending medially toward the midline (medial lobes), the

FIGURE 7 Neuraxis. Many descriptions in the literature rarely make the point that the brain's orientation is not that of the body. During postembryonic development, the brain undergoes morphogenic movements, tilting upward and back. This brings the dorsal surface of the brain to face caudally with respect to the body's axis. The front of the brain is its ventral side according to the neuraxis. The top part of the brain is rostral. Likewise, the antennal lobes are ventral, not frontal.

FIGURE 7 Neuraxis. Many descriptions in the literature rarely make the point that the brain's orientation is not that of the body. During postembryonic development, the brain undergoes morphogenic movements, tilting upward and back. This brings the dorsal surface of the brain to face caudally with respect to the body's axis. The front of the brain is its ventral side according to the neuraxis. The top part of the brain is rostral. Likewise, the antennal lobes are ventral, not frontal.

other extending ventrally, with respect to the neuraxis. However, because most brains are tilted upward (Fig. 7), these lobes can point forward or even upward. They are thus collectively referred to as the vertical lobes.

The mushroom body lobes comprise many thousands of approximately parallel-running processes. These originate from clusters of minute globuli cells situated dorsorostrally in the protocerebrum's cell body rind. In neopteran insects, these neurons have distal dendritic trees that contribute to rostral neuropils called the calyces. Each mushroom body has a pair of calyces, each of which is divided into two halves. A crucial study by Kei Ito and colleagues demonstrated that each half is generated by one of a quartet of embryonic neuroblasts. The four half-calyces are supplied by four lineages of globuli cells, all of which provide dendrites in the calyces and long axon-like processes in the lobes. These "intrinsic neurons" of the mushroom bodies are known as Kenyon cells, named after their discoverer. Lineage analysis of the Drosophila mushroom bodies has shown that each of the four neuroblasts generates the same sequence of Kenyon cells, certain types of which differentiate before others. Different types of Kenyon cells contribute to different and discrete subdivisions of the lobes. Farris's studies on the mushroom bodies of the cockroach Periplaneta americana and the worker honey bee Apis mellifera have shown that the sequence of Kenyon cell production and segregation to subdivisions is similar to that in Drosophila described by Lee et al. in 2001.

Observations of the cockroach and honey bee calyces show these neuropils as organized into nested zones, each of which is defined by the types of afferents supplying it. The most up-to-date study on the honey bee demonstrates that an outer region called the lip comprises three zones, each of which receives axon collaterals from neurons that project from glomeruli of the antennal lobes (see later) to regions of the lateral protocerebrum. A second region of the calyx, which comprises the collar, is further divided into discrete zones, each of which is defined by visual and other afferent endings, such as from gustatory neuropils of the subeso-phageal ganglion. However, in many other insect orders, the calyces receive sparse inputs, if any, from the visual system. A central region of the calyx called the basal ring is similarly divided into modality-specific zones.

Kenyon cells having dendrites in one of these zones send their axon-like processes into a specific stratum that extends all the way through the vertical and medial lobes. Each stratum thus represents a zone of the calyces. However, a special class of Kenyon cells that is generated earliest in development supplies axon-like processes to a separate division of the mushroom bodies, called the gamma lobe. Depending on the taxon, this lobe lies parallel to the medial (flies), vertical (honey bees), or both (cockroach) lobes. Important studies by Zars and Heisenberg on gene expression in different parts of the mushroom body of Drosophila have implicated the gamma lobe in supporting short-term memory.

One pervasive misconception is that the calyces are the "input region" of the mushroom bodies, whereas their lobes are their output regions. This view of the mushroom body does much to confuse and mislead theoretical considerations about how the mushroom bodies might work. Palaeopteran insects lack calyces supplied by sensory interneurons, yet their lobes both receive afferent endings from other protocerebral neuropils and provide efferents that extend back to protocerebral neuropils. In neopteran insects, the lobes likewise receive inputs and provide outputs, with the axon-like processes of Kenyon cells providing local circuits between them. However, in neopterans, Kenyon cells also supply calyces with dendrites that are visited by sensory interneurons. The role of the calyces is not fully understood. Possibly, afferents ending on Kenyon cell dendrites serve to modify the activity of local circuits in the lobes that are supplied by the processes of Kenyon cells, thereby providing sensory context dependence to computations that occur via Kenyon cell processes between inputs and outputs at the mushroom body lobes. It is also possible that inputs to the calyces provide persisting memory-like alterations of groups of Kenyon cells. Peptidergic and other modulatory neurons (e.g., octopaminergic, dopaminergic) associated with the mushroom bodies have been implicated in memory formation, and genetic disruption of vesicle recycling in a modulatory neuron of the Drosophila mushroom body shortens memory. It is still somewhat of a mystery why there are two sets of lobes, with most Kenyon cell processes dividing into each of them. However, as shown by Pascual and Preat, working at the CNRS in France, if the vertical lobes are absent, as in one type of Drosophila mutant, then long-term memory cannot be established. A role for the mushroom bodies in learning and memory has also been suggested by chemical ablation of the mushroom body neuroblasts, and a consequent lack of the mushroom body abolishes olfactory associative learning by the adult fly. However, such ablations also remove a set of local circuit neurons in the antennal lobes, complicating the interpretation of such experiments. A further complication in interpreting the mushroom body's role in memory acquisition is Dubnau's recent finding that synaptic transmission by mushroom body neurons is necessary only for memory retrieval and not for memory formation.

The Rostral Lateral Protocerebrum and Lateral Horn

The protocerebrum is composed of many discrete centers, most of which do not have obvious order and neat geometries, as in the mushroom bodies and central complex. Nevertheless, each protocerebral center is a unique entity and specific centers can be identified across different species. It is likely that studies of enhancer trap lines, as well as genetic labeling of clonally related neurons, developed by Liqun Luo and his colleagues, will in the near future reveal many new features of the cellular organization of the protocerebrum. But, so far, few studies have been done on these neuropils even though they together impart great complexity to the brain. This section focuses on just two neighboring regions, the lateral protocerebrum and lateral horn, which are now known to be second-order olfactory neuropils.

Antennal lobe projection neurons relay information from olfactory glomeruli to various areas of the brain, via three axon bundles called the inner, intermediate, and outer antennocerebral tracts. Axons of the inner antennocerebral tract provide axon collaterals to the mushroom body calyces. However, olfactory projection neurons providing input to the calyces do not terminate there but end in a region of the protocerebrum called the lateral horn and, caudally adjacent to it, the lateral protocerebrum. Axons of the intermediate and outer antennocerebral tracts also invade these neuropils, which therefore must be considered second-order olfactory processing centers of the brain. In honey bees, certain axons of the intermediate tract also target some neuropils that lie in front of and beneath the calyces as well as neuropils enwrapping the vertical lobes. Studies from Liqun Luo's laboratory at Stanford University have now shown that discrete fields of endings in the lateral horn and lateral protocerebral areas lying immediately caudal to it are supplied by specific groups of antennal lobe glomeruli, thus showing that the olfactory map that occurs among antennal lobe glomeruli is partially maintained within this lateral protocerebral area. With the exception of the calyces, neuropils targeted by antennal lobe projection neurons are second-order olfactory centers. These neuropils are not, however, unimodal olfactory centers as they also receive inputs from the optic lobes via large ascending fascicles.

The lateral horn and lateral protocerebrum give rise to systems of local interneurons as well as long-axoned interneurons, certain of which terminate in the mushroom body lobes. However, the relationship of the lateral protocerebrum with descending pathways is not yet known. A further area of ignorance is its relationship with the central complex.

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