Primary Somatosensory Cortex of Some Species of the Muroidea (Superfamily)

Okajimas Folia Anat. Jpn., 58(4-6) : 443-452, March 1982

Cytoarchitectonic Variations of "Barrels" Organized in the Primary Somatosensory Cortex of Some Species of the Muroidea (Superfamily)

KOICHI TAKATSUJI, HIDEO MASAI and KIMIYUKI TSUCHIYA

Department of Anatomy, Osaka University Medical School, Osaka 530, Japan, and Department of Medical Zoology, Hokkaido Institute of Public Health, Sapporo 060, Japan

-Received of Publication, September 18, 1981-

Key words : "Barrel" structure, Brain weight, Vibrissae, Habitat, Meriones unguiculatus

Summary : In 18 species of the Muroidea, the cytoarchitecture of the barrel structures of the posteromedial barrel subfield (PMBSF) in the primary somatosensory cortex was studied comparatively by cresyl violet staining. All species examined revealed barrel structures. The barrel patterns were classified into three types, A, B and C, on the basis of the features of the "side", "septum" and "hollow" of each barrel. The type A barrel was the most clearly defined, the type C barrel was obscure in appearance, and the type B barrel was intermediate between types A and C. In general, the larger the brain, the less obvious were the barrels. However, Meriones unguiculatus had a type A barrel even though its brain was large. This situation is discussed in relation to the peculiar habitat, such as arid desert.

In layer IV of the primary somatosen- sence of certain interspecific differences sory face area of the cortex of rats and in the barrel patterns of five species of mice, there are specialized cell groups the Myomorpha. termed "barrels". Physiological experi- The purpose of the peesent study was to ments have shown that the barrels in assess the major trends of the cytoarchi- the posteromedial barrel subfield (PMBSF) tectonic variations of the barrels in the are the cortical correlate of contralateral PMBSF occurring within one taxa, the mystical vibrissae (Woolsey and Van der Muroidea (superfamily), by increasing the Loos '70). Woolsey et al. ('75a) described number of species examined. the occurrence of the barrels and their morphological variations in the brains of 27 species from seven mammalian orders. This comparative study suggsted the pre-

Footnotes : This study was supported by a Grant for Scientific Research from the Ministry of Education of Japan.

443 444 K. Takatsuji, H. Masai and K. Tsuchiya

Materials and Methods The area termed a "hollow" which was surrounded by this ring, exhibited a Eighteen species belonging to the lower cell density. Each barrel was Muroidea were collected in the field and separated by a clear area or "septum" obtained from other laboratories. The (Fig. 3). Although the septum was less scientific names given followed Corbet clearly seen in the PMBSF in coronal ('78). For classification of the , species, sections, each barrel structure was gene- Simpson's ('45) and Wood's systems ('55) rally visible as patches contrasting with were chosen as shown in Table 1. The adjacent homogeneous regions in layer habitat of each species was based on IV (Fig. 2). field observations by the present authors The average brain weight, the hollow and the descriptions of Walker ('68). size, the type of barrel structures and Following pentobarbital anesthesia, the habitat of each species are summarized animals were perfused intracardially with in Table 1. In measurements of the 10% formalin solution. The brains were barrel size, the hollow size was repre- removed from the skulls, postfixed in sented in practice by the average diame- the same fresh fixative for 4 weeks, and ters parallel and perpendicular to the then weighed. The brains were embed- row in fiver relevant barrels which were ded in celloidin. Serial sections of the selected at random in a few tangential brains were cut in two directions, i.e. at sections. Insofar as the hollow size was a thickness of 25 pm in the coronal plane concerned, no peculiar species were noted. and at 50 pm in the tangential plane to The larger brain had a relatively more the pial surface of the PMBSF. All enlarged hollow in tangential profile sections were stained with 0.1% cresyl (Table 1). violet. Measurement of the hollow sizes In tangential section, the barrel struc- (see Results) was carried out on photo- tures in the PMBSF could be classified graphs enlarged to an 80-fold magnifica- into three types, A, B and C, based on tion. the features of the "side", "hollow" and "septum" , as follows. Results Type A (Figs. 3 and 4) This type of barrel showed the basic pattern. The All the species of the Muroidea exami- side was clearly defined and seen distin- ned revealed "barrel" structures in layer guishably as a single cell layer. The hollow IV of what was histologically judged to contained cell bodies at less density. The be the somatosensory cortex (Figs. 1 and septum was a clearly visible and almost 2). Firstly, according to the definition acellular area. Type A barrels were of Woolsey and Van der Loos ('70), the prominent, and seen in Mus boodga, basic plan of each barrel in the PMBSF Micromys minutus (Fig. 3) and Meriones must be described in relevant sections unguiculatus (Fig. 4). The septa were cut tangentially to the pial surface. In wider in Meriones unguiculatus than those the species examined except for Meriones in Mus boodga and Micromys minutus. unguiculatus, the barrels in the PMBSF Type B (Fig. 5) In the type B barrel, were arranged in five rows. In Meriones the septum was wider and contained unguiculatus there were seven rows of more cells than that in the type A barrel. barrels. The shape of the barrels was The border of the side and septum was circular or elliptical. Each barrel revealed less clearly recognizable than that in type a ring of nerve cell bodies called a "side". A. The cell density was less in the Table 1. Classification of barrel types of muroidea rodents examined. Each species was arranged in order of its brain weight.

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g, C J1 446 K. Takatsuji, H. Masai and K. Tsuchiya hollow than in the "wall" (Woolsey and septum of each barrel. Of these varia- Van der Loos '70) which consists of the tions, barrels of type A were clearly sides of two adjoining barrels and the defined and distinguishable from type intervening septum. Thus, the hollow B and C barrels. In type B and C remained clearly defined. Type B barrels barrels, the septum which forms the wall occurred in Mus musculus, Eothenomys, together with the sides, became less kageus, Clethrionomys rutilus mikado, obvious. In addition, the transition of Mus platythrix, Apodemus agrarius, Pero- the side to the hollow was mostly con- myscus leucopus (Fig. 5), Cricetulus ba- tinuous in type C barrels, and this type rabensis griceus, Clethrionomys bedfordiae of barrel was obscure as a whole. The and Microtus montebelli. pattern of the type B barrel is considered Type C (Fig. 6) In addition to the as intermediate between those of type obscure septum as recognized in the type A and type C. The barrel features of B barrel, the hollow in type C barrels Mus musulus (type B) and Rattus rattus was filled with small cell bodies. In (typeC) were similar to those described by this type of barrel, the packing den- Welker and Woolsey (74), and Woolsey sity of the cell bodies did not change et al. (75a). abruptly between the hollow and wall, The barrel patterns in the species and the barrels were very poorly identi- whose brain weights were large, belonged fied (Fig. 6). Type C barrels occurred to types B and C; that is, the larger the in Apodemes speciosus ainu (Fig. 6) and brain, the less obvious were the barrels, Rattus rattus. as noted in some species throughout In Vandeleuria oleracea and Apodemus rodent suborders (Woolsey et al. 75a). argenteus, each barrel was of type A or In the mouse, which has a type B type B. The barrel patterns in Apodemus barrel on our classification, the cell peninsulae giliacus and Millardia meltada located in the septa send dendrites to belonged to type B or C. more than one barrel, while the cells Among all the species except Meriones lying in the sides and hollows had unguiculatus, type A (i. e. clearly visible) processes confined to a single barrel barrels tended to occur in extremely (Woolsey et al. 75b). Based on such reduced brains, while type C (i. e. obscure) features of dendritic branching, it can be barrels tended to appear in larger brains. expected that most of the neurons contained in the sides and hollows are stron- Discussion gly influenced by one group of specific thalamocortical afferents corresponding It was found that "barrel" structures to one barrel. In contrast to this, the occurred in layer IV of the primary neurons located in the septa are likely somatosensory cortex of all species ex- to be contacted by more than two ad- amined in the superfamily Muroidea. As jacent thalamocortical afferents groups, for the hollow size, it appeared that and to receive amiguous signals (Woolsey larger brains had relatively enlarged et al. 75b, Harris and Woolsey 81). In hollows. There were no barrels whose this connection, it should be noted that size was disproportionate to the brain in type A barrels, the septum contains weight. few cells receiving ambiguous signals, Three types of variations were recog- and most cells are located in the side nized among the barrel patterns in terms and hollow, so that each barrel is more of the features of the side, hollow and or less presented with a distinguishable Variations of "Barrels" in Muroidea 447 input from one corresponding vibrissa. following postnatal vibrissa follicle This probably leads to clear analysis of damage. J. Comp. Neurol., 196: 357- inputs from vibrissae which may function 376, 1981. as a kind of exploror. 3) Simpson, G. G.: The principles of classi- In marked contrast to the trends in fication and a classification of mammals. Bull. Amer. Mus. Nat. Hist., 85: 1-350, barrel types and brain weights mentioned 1945. above, Meriones unguiculatus possessed 4) Suthers, R. A.: Sensory ecology of type A barrels even though its brain mammals. In : M. A. Ali. (ed.) Sensory weight was large. The barrel pattern Ecology, Review and Perspectives. 253- of Meriones resembled that of Gerbillus 287. Plenum Press, New York, 1978. as described by Woolsey et al. (75a). 5) Walker, E. P.: Mammals of the World. Both species live in a similar habitat, 2nd ed. vol. II. The Johns Hopkins i. e. arid desert, which differs sharply Press, Baltimore, 1968. from the habitats of the other species, 6) Welker, C. and Woolsey, T. A.: Struc- ture of layer IV in the somatosensory such as mountain wooded areas, fields, neocortex of the rat : Description and etc. (Walker 68). It is of interest that comparison with the mouse. J. Comp. both these species of desert rodents Neurol., 158 : 437-454, 1974. whose ears are sensitive to low frequen- 7) Wood, A. E.: A revised classification cy sounds (Suthers 78), possess type A of the rodents. J. Mammal., 36: 165- barrels which are considered able to 187, 1955. analyze distinguishably the inputs from 8) Woolsey, T. A. and Van der Loos, H.: The vibrissae. structural organization of layer IV in the Based on the present study, although somatosensory region (SI) of the mouse it is difficult to draw any conclusions cerebral cortex : the description of a cortical field composed of discrete cyto- concerning the evolution of barrel struc- architectonic units. Brain Res., 17: 205- tures, it can be said that the features of 242, 1970. the barrels do not depend upon the 9) Woolsey, T. A., Welker, C. and Schwarz, taxa, such as family and subfamily, but R. H.: Comparative anatomical studies on the brain weight or on the habitat in of the Sm I face cortex with special some species. reference to the occurrence of "barrel" in layer IV. J. Comp. Neurol., 164: 79- 94, 1975a. References 10) Woolsey, T. A., Dierker, M. L. and Wann, 1) Corbet, G. B.: The mammals of the D. F.: Mouse Sm I cortex : Qualitative palaearctic region, a taxonomic review. and quantitative classification of Golgi- Cornell Univ. Press,- London/Ithaca, 1978. impregnated barrel neurons. Proc. Nat. 2) Harris, R. M. and Woolsey, T. A. : Acad. Sci. U. S. A. 72 : 2165-2169, 1975b. Dendritic plasticity in mouse barrel cortex 448 K. Takatsuji, H. Masai and K. Tsuchiya

Explanation of Figures

Plate I

Fig. 1. Frontal section of the cerebral cortex through the somatosensory region in Micromys minutus. Cresyl violet staining. The arrow shows the "barrel" region. ac : Anterior commissure. Scale : 1 mm.

Fig. 2. Barrel structure of Micromys minutus in a frontal section of the brain. Cresyl violet staining. Triangle : hollow, arrow : side and septum. Scale : 0.2 mm. 449 Plate I

K. Takatsuji, et al. 450 K. Takatsuji, H. Masai and K. Tsuchiya

Plate II

Fig. 3. Barrel structure of Micromys minutus in a tangential section of the brain. Cresyl violet staining. Triangle : hollow, arrow : septum between sides. Scale : 0.2 mm.

Fig. 4. Barrel structure of Meriones unguiculatus in a tangential section of the brain. Cresyl violet staining. Triangle : hollow, arrow : clear septum between sides. Scale : 0.2 mm.

Fig. 5. Barrel structure of Peromyscus leucopus in a tangential section of the brain. Cresyl violet staining. Triangle : hollow, arrow : septum and sides. Scale : 0.2 mm.

Fig. 6. Barrel structure of Apodemus speciosus ainu in a tangential section of the brain. Cresyl violet staining. Arrows show the wall of one barrel. Scale : 0.2 mm. 451 Plate II

K. Takatsuji, et al.