ISSN 0013-8738, Entomological Review, 2013, Vol. 93, No. 6, pp. 703–713. © Pleiades Publishing, Inc., 2013. Original Russian Text © A.A. Makarova, A.A. Polilov, 2013, published in Zoologicheskii Zhurnal, 2013, Vol. 92, No. 5, pp. 523–533.
Peculiarities of the Brain Organization and Fine Structure in Small Insects Related to Miniaturization. 1. The Smallest Coleoptera (Ptiliidae) A. A. Makarova and A. A. Polilov Faculty of Biology, Lomonosov Moscow State University, Moscow, 119991 Russia e-mail:
[email protected] Received January 27, 2011 Emended December 14, 2012
Abstract—This paper describes for the first time the organization and fine structure of the brain in the smallest free-living insects Acrotrichis grandicollis, Micado sp., and Nanosella sp. (Ptiliidae, Coleoptera), which were studied using serial histological sections as well as TEM and computer-assisted 3D reconstructions. Some specific structural features related to miniaturization were revealed; the relative size of the brain regions and localization of its structures were analyzed. In spite of the extremely small body size, the brain retains the structure and fine structure typical of larger representatives of related groups, illustrating high conservatism of the brain morphology. Data on the number and size of neurons in the brain of Ptiliidae were obtained. The results obtained confirm and supplement the hypothesis about the factors limiting miniaturization of insects. [The next papers will describe the brain organization in Mymaridae and Trichogrammatidae (Hymenoptera), Corylophidae (Coleoptera), Thripidae (Thysanoptera), and Liposcelidae (Psocoptera).] DOI: 10.1134/S0013873813060043
Miniaturization is one of the principal directions of the evolution of insects (Chetverikov, 1915), as the result of which many insects become comparable in size to protozoa. An extremely small body size is an important characteristic of an insect which largely determines the morphology, physiology, and biology of a particular species (Schmidt-Nielsen, 1987). Although miniaturization affects all the organs, of the greatest interest are the nervous and reproductive systems since changes in these systems limit further decrease in the body size of insects (Polilov, 2005, 2007, 2008). First publications on the structure of the insect nervous system appeared as early as in the XIV–XVI centuries. The classical neuromorphological works of S. Ramón y Cajal and C. Golgi, the Nobel Prize winners of 1906, marked a breakthrough in the studies of the nervous systems. Research into the comparative neuroanatomy of arthropods was pioneered by J. Flögel who started detailed studies of the insect mushroom bodies (Strausfeld and Seyfarth, 2008). At present, the structure of the insect nervous system has been studied in sufficient detail and summarized in numerous reviews and monographs (Dujardin, 1850; Zavarzin, 1941; Bullock and Horridge, 1965; Tsvilin-
eva, 1970; Williams, 1975; Strausfeld, 1976; Plotnikova, 1979; Sviderskii, 1980; Tyshchenko, 1986; Gupta, 1987; Homberg, 1994; Breidbach and Kutsch, 1995; Burrows, 1996; Strausfeld and Meinertzhagen, 1998; Chaika, 2010). However, the application of new methods and the use of extensive material still allow the researchers to obtain radically new data on the functional and evolutionary morphology of the nervous system (Strausfeld, 2009; Rybak et al., 2010). The structure of the nervous system of the smallest insects is poorly studied; there are only general data on the ground plan of this system in Ptiliidae (Polilov, 2005, 2008; Polilov and Beutel, 2009), Corylophidae (Polilov and Beutel, 2010), Mymaridae (Polilov, 2007), and Strepsiptera (Beutel et al., 2005). According to these data, a decrease in the body size is accompanied by strong oligomerization and concentration of ganglia in the central nervous system, whereas both the size and the number of neurons also decrease. However, despite the extremely small size and a small number of neurons, the central nervous system of feather-winged beetles occupies a relatively large part of the body volume, the relative size of the CNS increasing with miniaturization. The fine structure of the nervous system of the smallest insects has not been
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studied; such insects are of great interest from the point of view of neurobiology since, despite the extremely small size and transformations of their nervous systems, they still retain all the forms of behavior typical of the larger representatives of related groups. The part of the central nervous system located in the head capsule is usually referred to as the brain. In insects, the brain is represented by two structures: the supraoesophageal and suboesophageal ganglia connected by circumoesophageal connectives. In the interpretation of most neuromorphologists, only the supraoesophageal ganglion should be called the brain (Jawlowski, 1948; Goossen, 1949; Schwanwitsch, 1949; Bullock and Horridge, 1965; Howse, 1975; Strausfeld, 1976; Tyshchenko, 1986; Chaika, 2010). The aim of this work was to study the organization and fine structure of the brain in the smallest beetles and to characterize the factors limiting the size of their nervous system. MATERIALS AND METHODS The nervous system of feather-winged beetles was studied in adults of Acrotrichis grandicollis (Mannerheim, 1844; body length 0.8 mm) collected in Moscow Province in July–August 2008; Micado sp. and Nanosella sp. (body length 0.5 and 0.4 mm, respectively) collected in Vietnam in May 2009. For comparison, we also studied larger representatives of the superfamily Staphylinoidea: the rove beetles Aleochara sp. (Staphylinidae) (body length 8 mm), collected in Moscow Province in June 2009. For histological examination, the material was fixed in formalin-ethanol-acetic acid mixture; for electron microscopy, the material was fixed in 2% glutaraldehyde in cacodylate buffer and postfixed in 1% buffered osmium tetroxide. The material was then dehydrated in a graded ethanol series and in acetone and embedded in Araldite M for light histology and in Epon 812 for transmission electron microscopy. Cross-sections and longitudinal serial sections 1 μm thick were obtained from Araldite-embedded specimens on a Leica 2225 Microtome. The sections were impregnated with silver by the modified technique of Scott (1979) and stained with toluidine blue by the following method: The slides with sections were placed in 4% formalin solution for 10–20 min, rinsed twice in distilled water, dried on a hot plate (60°C), and treated with solution of ammoniacal silver for 40–60 s. The slides were then
rinsed again in two volumes of distilled water and placed in 4% formalin solution for 5–10 min. The procedures with ammoniacal silver and 4% formalin were repeated 2–4 times, until the sections turned yellow-brown. The staining was fixed in 5% sodium thiosulfate solution for 5 min, after which the slides were rinsed in distilled water. Then the slides on a hot plate (60°C) were treated with solution of toluidine blue (0.8%) and pyronin (0.4%) for 1–2 min, rinsed twice in distilled water, dried for 2 h at 60°C, and mounted in Pertex. The permanent preparations were examined in Zeiss Axioscop 40 equipped with an Axiocam digital camera. The brain fine structure was studied in ultrathin sections, which were obtained on an LKB Ultratome, stained with lead citrate, and examined using a Jeol JEM-1011 transmission electron microscope. The aligned image stacks representing complete series of cross-sections were loaded into the Bitplane Imaris software, in which all the relevant details were manually contoured and the 3D reconstruction was created. The 3D vector models were imported into Autodesk Maya, in which the dithering and rendering functions were applied. The volume of individual organs and the entire body (without legs, wings, antennae, and palps) was calculated from the 3D models, using the Imaris statistical functions. In order to determine the number of cells in the brain, the mean linear size of the cell body was calculated in the Reconstruct software based on the mean area occupied by a cell in histological sections; then the number of cells was calculated from the volume of the cortical layer and the mean cell body volume. None of the presently available methods allows the neurons and glial cells to be counted separately. The number of neurons cannot be determined based on the neuron-to-glia ratio, either, since this ratio varies greatly between insect species and between different parts of the brain (Chaika, 2010). Therefore, in this communication we considered the total number of cells in the brain. It should be noted that all the published estimates of the number of neurons in insects are also based on calculation of the total number of cells in the CNS. RESULTS We have studied the brain organization in adult feather-winged beetles of three species: Acrotrichis grandicollis (Acrotrichinae), Micado sp., and Nanosella sp. (Nanosellinae). Although these species ENTOMOLOGICAL REVIEW Vol. 93 No. 6 2013
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Fig. 1. Morphology of cephalic ganglia of Acrotrichis grandicollis: cross-sections impregnated with silver and stained with toluidine blue, at the level of the antennal lobes (A), the base of mandibles (B), the suboesophageal ganglion and the beginning of prothoracic segment (C), and the base of maxillae (D). al, antennal lobes; ant, antenna; cb, central body; lbl, lobulus; lg, lamina; lob, lobula; lp, lateral protocerebrum; mb, mushroom bodies; mbα, α-lobe of pedunculus; mbβ, β-lobe of pedunculus; md, mandible; med, medulla; oc, compound eye; ph, pharynx; sog, suboesophageal ganglion; trtc, tritocerebrum.
belong to two different subfamilies and differ considerably in size, their brain morphology proved to be similar, differing only in some quantitative parameters. The general structure of the cephalic ganglia in the studied feather-winged beetles corresponds to the insect ground plan. The neuron bodies lie on the periphery whereas the central part is occupied by the neuropil (Figs. 1A–1D). The cortical layer of the brain reveals nuclei of the neurons, the cytoplasm being barely noticeable. The supraoesophageal ganglion is situated in the posterior half of the head. A considerENTOMOLOGICAL REVIEW Vol. 93 No. 6 2013
able portion of the suboesophageal ganglion is shifted into the prothorax and fused with the prothoracic ganglion. In Nanosella, a small part of the supraoesophageal ganglion also extends into the prothorax and reveals noticeable asymmetry: in particular, the posterior part of the ganglion has an asymmetrical left distal outgrowth (Fig. 2). The brain sheaths have the structure typical of the insect ganglionic sheath (Fig. 3A). The sheath consists of two layers: the outer non-cellular neurilemma and the inner planocellular perineurium. In the studied representatives of the smallest beetles, the neurilemma
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Fig. 2. Morphology of cephalic ganglia of Nanosella sp. in front (A, C) and dorsal (B, D) view. pm, protocerebral bridge; other designations as in Fig. 1.
is 0.06–0.14 μm deep, whereas the thickness of the perineurium varies within a greater range, from 0.03 to 0.3 μm.
cerned in the processes where they are longitudinally arranged.
The medullary and cortical layers reveal welldeveloped neuroglia closely adjoining the bodies (the cortical glia) and processes of the neurons. Neuroglia also envelopes the glomeruli of the mushroom bodies and forms the perineural layer of the brain sheath (Figs. 3A, 3D, 3F).
Both gap junctions and chemical synapses can be found in the neuropil of Acrotrichis grandicollis (Fig. 3C). The gap junctions are represented by the longitudinal and transversal types. The synaptic contacts are either divergent or shaped as terminal buds (Fig. 3C). Electron-dense neurosecretory granules are present in the presynaptic zone of the axoplasm.
The neuron cytoplasm includes mitochondria, rough ER, the Golgi apparatus, and vacuoles with inclusions (Fig. 3B). The neuropil contains distinct axons with their axolemma, mitochondria, microtubules, and neurofibrils (Fig. 3C). The neurofibrils run in various directions in the neuron bodies and can be easily dis-
The protocerebrum includes the most important associative centers: the central complex (the central body and the protocerebral bridge) and the mushroom bodies (Figs. 1, 2, 4). The oval-shaped central body is situated medially above the oesophagus and between the pedunculi of the mushroom bodies; it conENTOMOLOGICAL REVIEW Vol. 93 No. 6 2013
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Fig. 3. Fine structure of the brain of Acrotrichis grandicollis, TEM: brain sheaths (A), neurons (B), neuropil (C), and glomeruli in the calices of the mushroom bodies (D–F). cut, cuticle; ga, Golgi apparatus; gl, neuroglia; glm, glomeruli; gr, rough ER; ls, lysosomes and residual bodies; mf, microfilaments; mt, mitochondria; nc, nucleus of a neuron; nl, neurilemma; np, neuropil; pn, perineurium; syn, synaptic contacts. ENTOMOLOGICAL REVIEW Vol. 93 No. 6 2013
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Fig. 4. Morphology of cephalic ganglia of Acrotrichis grandicollis in front (A, C) and dorsal (B, D) view. For designations, see Figs. 1, 2.
tains the commissural fibers linking the left and right halves of the brain. The central body consists of three parts. The upper part includes the dorsal arc and the divided fan-shaped body. The lower part is the ellipsoid body, which fits into the valley of the arched upper part. The third part of the central body includes the noduli, which are small globular neuropils. The protocerebral bridge is a paired bundle of commissural fibers situated above the central body. The mushroom bodies lie on either side of the central body in the distal area of the protocerebrum. They have a neuropilar structure and are differentiated into the pedunculus and the calyx area. The calices are single and do not have the typical cup-like shape. A similar structure of the mushroom bodies was described for Chauliognathus lecontei (Cantharidae) (Strausfeld, 2009): the calyx is a uniform structure
surrounded by the glomeruli that consist of Kenyon cell processes. The Kenyon cells are situated on the dorsal surface of the protocerebrum and can be distinguished by their sharper contrast against the background of the cortical brain layer (Fig. 1D). The glomeruli have a dense neuropilar structure and surround the calyx area in a single layer (Figs. 1D, 3E, 3F); their diameter does not exceed 4 μm. The pedunculus is subdivided into α- and β-lobes (Figs. 2, 4). The mushroom bodies of Acrotrichis grandicollis and Nanosella sp. differ in the length of the pedunculus. The mushroom bodies of Nanosella sp. are more compact than those of A. grandicollis. The optic lobes consist of three zones: lamina ganglionaris, medulla externa, and medulla interna (Figs. 2, 4). The medulla interna (lobula) of AcrotriENTOMOLOGICAL REVIEW Vol. 93 No. 6 2013
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chis grandicollis is additionally subdivided into the rounded lobula and the elongate lobulus. All the three optic zones are situated close together. In Nanosella sp. the third zone does not appear to be subdivided, whereas the second one (medulla externa) is more extensively developed; it is the largest of the three zones, and narrows towards the posterior part of the brain. The medulla interna is hemispherical, with its convex side facing outwards. The lateral protocerebrum lies between the mushroom bodies and the optic lobes (Figs. 2, 4) and consists of cell processes associated with the visual and olfactory centers. This structure has an approximately the same relative size in Acrotrichis grandicollis and Nanosella sp. Some other, smaller structures, such as the ventral bodies, tracts, chiasmata, etc., could not be reliably discerned due to insufficient resolution of the histological method. The spherical antennal lobes with glomerular neuropil can be distinguished in the deutocerebrum (Figs. 2, 4). The dense glomeruli of Acrotrichis grandicollis are 5–7 μm in diameter, whereas in most insects they reach 20 μm in diameter (Tyshchenko, 1986). The antennal lobes comprise approximately 230–300 glomeruli; the exact number is difficult to determine since the boundaries of many glomeruli are indistinct. The tritocerebrum is the smallest part of the supraoesophageal ganglion, represented by paired structures lying lateral to the gut (Fig. 1C). Its commissure passes below the gut (Fig. 1D). The connectives linking the tritocerebrum with the suboesophageal ganglion cannot be discerned due to the fusion of the supra- and suboesophageal ganglia. The brain cells in representatives of the family Ptiliidae are much smaller than in other insects: 2–4 μm (M = 3.8, n = 256) in Acrotrichis grandicollis, 0.8–2 μm (M = 1.5, n = 291) in Nanosella sp., and 1–2.4 μm (M = 2.3, n = 328) in Micado sp. For comparison, the size of the brain cells in large representatives of Staphylinoidea, such as Aleochara sp., is 4.6– 7.6 μm (M = 6.2, n = 549). The nucleus occupies 80 to 90% of the brain cell volume in Ptiliidae. The number of cells in the nervous system of feather-winged beetles is also considerably smaller than in larger insects. The brain of Acrotrichis grandicollis comprises about 20 000 cells, that of NanoENTOMOLOGICAL REVIEW Vol. 93 No. 6 2013
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sella sp., 11 000 cells, that of Micado sp., 12 000 cells, and that of Aleochara sp., 73 000 cells. A decrease in body size is accompanied by changes in the relative volume of certain parts of the brain, different structures showing different scaling. According to the data obtained, the size of the central body in Nanosella sp., Acrotrichis grandicollis, and Aleochara sp. changes isometrically while that of the other brain structures changes allometrically (Fig. 5). The relative volume of the mushroom bodies, lateral protocerebrum, antennal lobes, and optic lobes decreases with body size. The volume of the neuropil changes isometrically with respect to that of the brain as the body size decreases (Fig. 6). DISCUSSION The nervous system of the smallest beetles is subject to strong oligomerization and compactization. Their brain, however, show a very high degree of conservatism, completely retaining its organization and fine structure in spite of the manifold decrease in the body size. Their differences from the larger beetles are mostly observed in the relative size of certain brain areas and in the quantitative parameters. The relative volume of the central body complex in Nanosella sp., Acrotrichis grandicollis, and Aleochara sp. remains constant as the body size decreases, i.e., this structure changes isometrically. This complex is responsible for motor coordination of the appendages (Martin et al., 1999; Heinrich et al., 2001; Strausfeld, 2009). Since representatives of the family Ptiliidae retain an almost complete set of muscles (Polilov and Beutel, 2009), the functional load on the motor centers may be considered the same, regardless of the body size. The relative volume of the mushroom bodies in the smallest insects is reduced as compared to that in the larger representatives of related groups. The mushroom bodies of larger insects have to process a greater amount of information. The indistinct shaping of the calyx and reduction of the total relative volume of the mushroom bodies in the smallest beetles can be explained by a smaller number of sensory inputs. The relative volume of the optic lobes also decreases with body size. The number of ommatidia in the eyes of feather-winged beetles is reduced as the body size decreases, and the load on the sensory centers is reduced correspondingly. The smallest relative
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Fig. 5. The relative volume of certain brain structures of Staphylinoidea as related to body size: central body (A), protocerebral bridge (B), mushroom bodies (C), lateral protocerebrum (D), optic lobes (E), and antennal lobes (F).
volume of the optic lobes is observed in the smallest representative of the order. The relative volume of the lateral protocerebrum (with respect to the entire brain) decreases with body size. The lateral protocerebrum participates in perception and processing of olfactory stimuli (Plotnikova and Isavnina, 2006); therefore, its size changes in the same way as that of other sensory centers. The relative volume of the antennal lobes, like that of the lateral protocerebrum, changes allometrically.
A decrease in the number of the antennal chemosensory receptors reduces the load on the olfactory center, so that its relative volume can decrease. Thus, a decrease in the body size is accompanied by a decrease in the relative volume of the structures responsible for coordination and processing of sensory signals, such as visual and olfactory ones. As the number of analyzers decreases, the brain structure coordinating their activity is reduced in size. On the contrary, the central body complex, responsible for ENTOMOLOGICAL REVIEW Vol. 93 No. 6 2013
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Fig. 6. The relative size of the cephalic ganglia and neuropil of Staphylinoidea as related to body size: changes in the volume of the neuropil with respect to the volume of the brain (A), and changes in the volume of the brain with respect to the volume of the body (B).
coordination of the motor functions, does not change its relative volume in the course of miniaturization. Similar trends were described in the intraspecific variation of bees (Mares et al., 2005).
crease in the neuron size was observed in many small insects: Hydroscaphidiidae (Beutel and Haas, 1998), Corylophidae (Polilov, Beutel, 2010), Mymaridae (Polilov, 2007), and Strepsiptera (Beutel et al., 2005).
In a mathematical model proposed by Faisal and coauthors (2005), a decrease in the size of the axon increases the noise in the ion channels, negatively affecting propagation of the action potential. According to this model, axons with diameters smaller than 0.1 μm should be unable to transmit signals (Faisal et al., 2005). The parameters observed in our material confirm the estimation of the minimum axon diameter required for normal propagation of electric impulses. The axon diameter in representatives of the family Ptiliidae varies from 0.25 μm in free axons to 0.15 μm in complex fibers, i.e., it does not exceed the limits estimated by the cited authors. The diameter of the neuronal processes places a limit on the decrease of the neuropil volume; therefore, this parameter changes isometrically relative to the brain (Fig. 6).
Not only the size of the neurons but also their number decreases with miniaturization. The number of cells in the nervous system of feather-winged beetles is much smaller than in large insects. In particular, the brains of representatives of the family Ptiliidae contain from 11 000 to 20 000 cells, whereas the brain of Aleochara sp. contains 73 000 cells.
The considerable difference in the size of neurons between representatives of the family Ptiliidae and other insects deserves attention. The size of the brain cell bodies in the smallest insects is 1.5–4 μm, whereas in large representatives of Staphylinoidea, such as Aleochara sp., the neuron body size is 4.6–7.6 μm. The nucleus occupies from 80 to 90% of the neuron body volume in Ptiliidae, and about 60% in large representatives of related groups. At the cytological level, the decrease in the neuron size in feather-winged beetles as compared to their larger relatives occurs due to reduction of the cytoplasm volume, whereas the same process within the family Ptiliidae occurs due to an increase in the chromatin compaction level (Fig. 7). A considerable deENTOMOLOGICAL REVIEW Vol. 93 No. 6 2013
Despite a considerable decrease in the size and number of neurons, the relative volume of the brain in the smallest insects is several times that in the larger representatives of related beetle groups (Fig. 6B). Similar trends were observed in many small insects (Rensch, 1948; Beutel and Haas, 1998; Beutel et al., 2005; Polilov, 2005, 2007, 2008; Polilov and Beutel, 2009, 2010). Based on the data obtained, the following factors limiting miniaturization of the nervous system can be distinguished: conservatism of its morphology and ultrastructural organization, on the one hand, and the lower limit of the neuron size and the axon diameter, on the other. CONCLUSION Representatives of the family Ptiliidae are the smallest known beetles and the smallest non-parasitic insects. Their small size, comparable to that of unicellular organisms, has resulted in profound transformation of all the organ systems. Their nervous system undergoes strong oligomerization, with a considerable increase in its relative volume and compaction of certain structures. The brain shows a very high degree of
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Fig. 7. Fine structure of the neurons of Aleochara sp. (Staphylinidae) (A), Acrotrichis grandicollis (Ptiliidae) (B), and Nanosella sp. (Ptiliidae) (C), TEM.
conservatism, completely retaining its organization and fine structure despite the manifold decrease in the body size. Most brain parts change allometrically in the course of miniaturization; the relative size of the structures responsible for coordination and processing of sensory signals is reduced. The size of the nervous system is limited by its conservative morphology, the minimum possible size of the neurons and diameter of the axons, and acts as one of the factors limiting miniaturization in insects (Polilov, 2005, 2007, 2008; Polilov and Beutel, 2009). ACKNOWLEDGMENTS The work was financially supported by the Presidential Grants (MK-558.2010.4 and MK-375.2012.4) and the Russian Foundation for Basic Research (grant nos. 10-04-00457 and 11-04-00496). REFERENCES 1. Beutel, R.G. and Haas, A., “Larval Head Morphology of Hydroscapha natans LeConte 1874 (Coleoptera, Myxophaga, Hydroscaphidae) with Special Reference to Miniaturization,” Zoomorphology 18, 103–116 (1998).
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