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Structure of the brain areas in the American cockroach (Periplaneta americana)



Ryuichi Okada (University of Hyogo)


General feature of the brain

The American cockroach brain is developmentally divided into the protocerebrum, duetocerebrum, and triotocerebrum. Each of these is further divided into smaller areas, but there is no clear definition, rule, or nomenclature system for such divisions; therefore, the boundaries of these areas and their names often differ among researchers. At present, the most comprehensive anatomical map of the American cockroach brain is that presented by Okada et al., (2003). Okada et al. used brain neuropils and neural tracts to anatomically divide the brain into 14 different areas. These 14 areas include those with clear boundaries, such as the mushroom body and central complex, and others without clear boundaries, such as the superior lateral protocerebrum. Because not all 14 areas have been functionally or anatomically well characterized, here, we concentrate on areas that are well understood. 


Anatomical terms

Anatomical terms are sometimes complex and difficult to understand. For example, when describing a positional relationship of two areas, it is expressed in different manners depending on whether the description is based on the body axis or the neural axis. To help understand the photographs, positional relationships are described based on the body axis in this section. Therefore, ventral and dorsal in the text correspond to the lower and upper sides in a photograph, respectively, or vice versa.





Fig. Microscope photograph of the cockroach brain: Shown are the anterior (A), medial (B), and posterior (C) sides. As noted above, some abbreviations in this figure are different from those used in this section. The upper side of the photograph is the dorsal side, and the lower side is the ventral side. α: alpha lobe of the mushroom body; β: beta lobe of the mushroom body; ant lob: antennal lobe; cc: central complex; deut: duetocerebrum; d lob: dorsal lobe; d pr: posterior slope; l ca: lateral calyx of the mushroom body; ped: peduncle of the mushroom body; pr: protocerebrum; p-v l ho: a part of lateral horn. Scale: 200 μm (adapted from Okada et al., 2003).


The protocerebrum

This area occupies the majority of the brain. It is developmentally derived from the 1st segment of the neural tube. The optic lobes are the visual center for compound eyes. In addition, there are areas important for animal behavior, such as the mushroom body, the central complex, the lateral horn, ventral body, and posterior slope.


The optic lobes

The optic lobes are the visual center for the compound eyes, connecting them to the brain. In the optic lobes of the American cockroach, the visual information is transmitted from the retina of the compound eyes to the medulla via the lamina, and finally to lobula. These areas have a beautiful layered structure. Similar to research findings in flies and butterflies, the lamina is considered to be involved in light–dark contrast detection and edge detection; the medulla in pattern recognition, color vision, and movement detection; and the lobula in detecting movement direction.


The mushroom bodies

The mushroom body is a paired neuropil eahc on the left and right sides of the brain, and an American cockroach mushroom body comprises calyx, pedunculus, α lobe, and β lobe. In the American cockroach, the mushroom body is a double calyx type, with 2 calyxes in each hemisphere. The parts extending from the 2 calyxes merge to form the pedunculus, which bifurcate into the alpha and beta lobes. A large number of afferent neurons terminates in the calyx; therefore, with some exceptions, it is considered to be the input part of the mushroom body. The mushroom body receives various types of sensory information including, at least, olfactory, visual, taste (gustatory), and tactile (mechanical) information. Different types of sensory information have been shown to be delivered to separate parts of the calyx (Nishikawa et al., 1998; Nishino et al., 2012). Inputs from inhibitory neurons with the GABA transmitter have also been confirmed in the calyx (Nishino et al., 1998). The α lobe, β lobe, and pedunculus are made up of layers of 16 light and dark pairs (Mizunami et al., 1998a), and positional relationships of individual layers are conserved among the three parts. Each layer in the mushroom body is presumed to be a functional unit, similar to the functional column in mammals, but the details remain unknown.

The mushroom body in the American cockroach is involved in not only integration of sensory information but also motor control, and learning and memory. Correlation analysis of the neural activity of the mushroom body and behavior of the insect revealed units that begin firing before starting locomotion and unit that exhibit different activity patterns depending on the direction of movement (Mizunami et al., 1998c; Okada et al., 1999). When mushroom bodies on both sides are destroyed, visual learning cannot be formed (Mizunami et al., 1998d). As clearly shown in other insects such as Drosophila, honey bees, and crickets, there is no doubt that the mushroom bodies are also involved in olfactory learning in the American cockroach.


The central complex

The central complex is located in the center of the brain and on the dorsal side of the mushroom body β lobe. It consists of an ellipsoid body, a fan-shaped body locating on the dorsal side of the ellipsoid body, an elongated structure lying posterior to the dorsal side of the fan-shaped body called the protocerebral bridge, and the nodulus, a small area adjacent to the ventral side of the ellipsoid body. The central complex has previously been referred to as the central body. Of the 4 areas of the central complex, the ellipsoid body and fan-shaped bodies are easily identifiable based on their size and position in the brain. 

In the American cockroach, the functions of the central complex and its role in behavior remain unknown. In another cockroach species (Blaberus discoidalis), the central complex has been reported to be involved in locomotor behavior (Bender et al., 2010). In crickets, grasshoppers, and some butterflies,  the central complex neurons respond to selectively specific e-vector orientations of the polarized light, which indicates that the central complex may be a center for processing information from polarized light (Homberg et al., 2011; Sakura et al, 2008). In grasshoppers, 16 functional units (columns) have been observed related to polarized light information (Homberg et al., 2011). It remains unknown whether the American cockroach can detect polarized light; therefore, it is unclear whether the central complex of the American cockroach has the same function as that in grasshoppers and crickets. Polarized light information in the sky is used for spatial recognition by navigating insects. In Drosophila, the central complex has been reported to be necessary for spatial learning through visual cues (Ofstad et al., 2011).


The lateral horns, or lateral protocerebral lobes

The lateral horns are located on the lateral side, not the central part, of the brain and beneath the mushroom body calyxes. It has no clear boundary, generally being defined as the main terminate area of the projection neurons from the antennal lobes. In honey bees, a similar area can be referred to as the lateral lobe of the protocerebrum (LLP) or the lateral porotocerebral lobe (LPL). Neurons in the lateral horn are rich in varieties of morphology and also in physiological characteristics, including not only neurons that respond to odor but also light-, mechanosensation-, humidity-, and temperature-responsive neurons. (Nishino et al., 2003). However, because the lateral horn is rich in are the terminals of the antennal lobe projection neurons, the lateral horn has been predominantly studied as the secondary center for olfaction. In particular, in Drosophila, where research on the lateral horn is advancing, it has been reported that the topography of the antennal lobe glomerulus is relatively conserved in the lateral horn (Jefferis et al., 2007).

Although there is no doubt that the lateral horn is a second-order olfactory center, several researchers believe that it has other important roles. However, because neurons responding to a diverse range of sensory modalities are existing together in the lateral horn, analyzing the information processing mechanisms and their role on behavior is difficult. Therefore, other functions of the lateral horn are not well understood. In terms of locomotion regulation, the absence of dendrites of descending neurons toward the thoracic ganglia in the lateral horns suggests that the lateral horn is not a direct control center for locomotory motion.  Instead, it is believed to indirectly control behavior and movement through regulation of some other areas (Okada et al., 2003). In addition, there are no ascending neuron terminals coming from the thorax and abdomen. Therefore, the lateral horns are likely to function as neither motor center nor sensory center, but as an association center for locomotion (Okada et al., 2003).


Ventral bodies, lateral accessory lobes

The ventral body is located, each on the left and right hemisphere, between the mushroom body β lobe and the antennal lobe. The ventral bodies are believed to function as a one of motor centers, but the function and neuronal configurations remain unknown. In silkworm moths, grasshoppers, and crickets, they are called lateral accessory lobes (LAL). In grasshoppers, neurons connecting the LAL and central complex are known to detect polarized light and are a part of polarized light information processing neural network (Homeberg et al., 2011). In silkworm moths, they are known to be a motor center during courtship. When a male silkworm moth detects the sex pheromone emitted from a female, he walks straight ahead, in a zigzag pattern, and then in large circles. Descending neurons that show neural activity corresponding to the zigzag walking pattern have been found in the LAL of the male silkworm moth. In addition, neurons connecting the left and right LAL are present. The two LALs are connected through these neurons. The zigzag walking pattern is believed to be caused by the LAL neurons on each side being suppressed in turn by GABA.


The posterior slope

The posterior slope is situated in the posterior side of the brain and occupies a large area, including the almost the whole posterior part of the protocerebrum (excluding the mushroom bodies). It is believed to be the main area for efferent neural signals in the brain. Indeed, input sites (dendrites) of numerous descending neurons are found, but there are also terminals of lot of ascending neurons. The function and role of the posterior slope have not been well characterized at present.

The Ocellar tract neuropils

The American cockroach has a pair of simple eyes (ocelli) on the left and right side of the head, beside the base of the antennae. The thick ocellar tract neuropils run from the ocellar ganglia on the dorsal side near the midline of the protocerebrum, and information from the ocelli is sent to the brain.


The Duetocerebrum

Situated on the ventral side of the protocerebrum, it is developed from the second segment of neural tube. It contains olfactory and mechanosensory centers, the antennal lobes and the dorsal lobe, respectively.


The antennal lobe

The antennal lobe is a paired neuropil, each in the right and left brain hemispheres, and is the primary processing center of olfactory information. The primary olfactory sensory neurons in the antennae (olfactory receptor neurons) run through the antennal nerve and terminate at the antennal lobe, the primary olfactory center. There are at least 205 glomeruli in the antennal lobe of the American cockroach (Watanebe et al., 2010). As in other insect, in the American cockroach, the olfactory receptor neurons expressing the same olfactory receptors are strongly sure to project into the same glomeruli. Therefore, the glomerulus is believed to be a functional unit of sensory information processing. In addition to odor, the antennal lobe has neurons that respond to temperature and humidity, and their target glomeruli have been identified (Nishino et al., 2003). However, the aspect of the olfactory center has been emphasized, and considerable research on them has been targeted on their role as the primary center for olfaction. The male antennal lobe contains the macro-glomerulus that is clearly bigger than other glomeruli (Nishino et al., 2009). They are specialized for processing information from the sex pheromones emitted by the females. When it is necessary to distinguish the macro-glomerulus, the remaining are called ordinary glomeruli. In the antennal lobes, there are second-order olfaction neurons (projection neurons) that project to the mushroom bodies and lateral horns receive synaptic inputs from olfactory sensory cells. In the antennal lobe, the projection neurons also make synapses in a complex manner with the local interneurons, which connect the glomeruli in the antennal lobe and never leave the antennal lobe. The projection neurons are classified in detail on the basis of their morphology. A projection neuron that receives an input from a single glomerulus is a uniglomerular projection neuron; those that receive an input from multiple glomeruli are multiglomerular projection neurons. Projection neurons are also classified on the basis of the neural pathways running in the brain. The olfactory receptor neurons and projection neurons generally show excitatory responses to 2 or more different odors. They are classified into two groups: neurons that respond to relatively limited kinds of substances (experts) and neurons that respond to wide-ranged kinds of odors (generalists). In contrast, local interneurons usually show the generalist pattern, and many of them have an inhibitory function. During an odor stimulus, the various glomeruli in the antennal lobe respond with different temporal patterns due to the complex connection between projection neurons and local interneurons connecting projection neurons (Watanabe et al., 2012). Because this pattern differs depending on the odor stimuli, it is believed that the odor information is represented by the spatio-temporal pattern of the glomerulus activity. 


The dorsal lobes

The dorsal lobe is located in the left and right hemisphere in the brain and occupy an area posterior to the antennal lobes. It is an information processing center for the antennal mechanosensation. When the antenna in the American cockroach is stimulated by being directly touched, the cockroach turns away toward the direction opposite to the stimulated side. This area contains the dendrites of the descending neurons for this antennal touch escape behavior (Burdohan and Comer, 1996).


The triotocerebrum

This is located on the ventral side of the dorsal lobe, near the  esophagus. Developmentally, it is emerged from the 3rd neural segment. It is believed to be the mechanosensation center for the antennae. It is also believed to control the movement of the antennae, but anatomical knowledge is sparse, and extremely few functional analysis have been performed.



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