Five Topographically Organized Fields in the Somatosensory Cortex of the Flying Fox: Microelectrode Maps, Myeloarchitecture, and Cortical Modules

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Five Topographically Organized Fields in the Somatosensory Cortex of the Flying Fox: Microelectrode Maps, Myeloarchitecture, and Cortical Modules THE JOURNAL OF COMPARATIVE NEUROLOGY 317:1-30 (1992) Five Topographically Organized Fields in the Somatosensory Cortex of the Flying Fox: Microelectrode Maps, Myeloarchitecture, and Cortical Modules LEAH A. KRUBITZER AND MIKE B. CALFORD Vision, Touch and Hearing Research Centre, Department of Physiology and Pharmacology, The University of Queensland, Queensland, Australia 4072 ABSTRACT Five somatosensory fields were defined in the grey-headed flying fox by using microelec- trode mapping procedures. These fields are: the primary somatosensory area, SI or area 3b; a field caudal to area 3b, area 1/2; the second somatosensory area, SII; the parietal ventral area, PV; and the ventral somatosensory area, VS. A large number of closely spaced electrode penetrations recording multiunit activity revealed that each of these fields had a complete somatotopic representation. Microelectrode maps of somatosensory fields were related to architecture in cortex that had been flattened, cut parallel to the cortical surface, and stained for myelin. Receptive field size and some neural properties of individual fields were directly compared. Area 3b was the largest field identified and its topography was similar to that described in many other mammals. Neurons in 3b were highly responsive to cutaneous stimulation of peripheral body parts and had relatively small receptive fields. The myeloarchi- tecture revealed patches of dense myelination surrounded by thin zones of lightly myelinated cortex. Microelectrode recordings showed that myelin-dense and sparse zones in 3b were related to neurons that responded consistently or habituated to repetitive stimulation respectively. In cortex caudal to 3b, and protruding into 3b, a complete representation of the body surface adjacent to much of the caudal boundary of 3b was defined. Neurons in this area habituated rapidly to repetitive stimulation. We termed this caudal field area 1/2because it had properties of both area 1 and area 2 of primates. In cortex caudolateral to 3b and lateral to area 1/2 (cortex traditionally defined as SII) we describe three separate representations of the body surface coextensive with distinct myeloar- chitectonic appearances. The second somatosensory area, SII, shared a congruent border with 3b at the representation of the nose. In SII, the overall orientation of the body representation was erect. The lips were represented rostrolaterally, the digits were represented laterally, and the toes were caudolateral to the digits. The trunk was represented caudally and the head was represented medially. A second complete representation, PV, had an inverted body representa- tion with respect to SII and bordered SII at the representation of the distal limbs. The proximal body parts were represented rostrolaterally in PV. Finally, caudal to both SII and PV, an additional representation, VS, shared a congruent border with the distal hindlimb representa- tion of both SII and PV. VS had a crude topography, and receptive fields of neurons in VS were relatively large. Many neurons in VS responded to both somatosensory and auditory stimula- tion. Key words: SI, SII, parietal ventral area, ventral somatosensory area, area 1, area 2, electrophysiology, architecture By using microelectrode mapping procedures and myeloar- chitecture, we have delineated five topographically orga- Accepted September 20,1991. in Of nized cutaneous the cerebral the grey- Address reprint requests to Leah Krubitzer, VTHRC, Dept. of Physiology headed flying fox, pteropus ~ozioce~hazusand the little red and Pharmacology, The University of Queensland, Queensland 4072, Austra- flying fox, Pteropus scapulatus. Since no clear distinction in lia. o 1992 WILEY-LISS, INC. 2 L.A. KRUBITZER AND M.B. CALFORD somatosensory cortical organization was noted between these species, they were considered together throughout this investigation. We chose these bats for several reasons. First, in an earlier investigation in the flying fox (Calford et al., '85) that described the organization of the primary somatosensory area, SI or 3b, limited recordings outside of 3b suggested a highly developed somatosensory cortex. The present investigation extends this earlier study by describ- ing the detailed somatotopy for a number of fields, in addition to 3b, in parietal cortex. Second, because the flying fox has a smooth neocortex with a very shallow lateral sulcus, all of these somatosensory areas are readily accessi- ble on the surface of cortex (Fig. 1).Another reason we chose the flying fox is that relatively little is known about the organization of its somatosensory neocortex. Compara- tive studies are inherently interesting, and if we are to appreciate how the brain changes or varies across species filling different ecological niches, and what features of organization are preserved in neocortical evolution, it is Fig. 1. Lateral view of Pteropus poliocephalus brain. Solid lines mark the location of somatosensory, auditory and visual areas of the important that we study many species to assess similarities neocortex.Arrow marks the shallow lateral sulcus. Primary visual area, or homologies accurately. For example, there is accumulat- 17; second visual area, 18; middle temporal visual area, MT; primary ing evidence that mammals in general may have more auditory area, AI;posterior parietal cortex, PP; primary somatosensory somatosensory areas in common than just the first (SI) and area, SI or 3b; caudal somatosensory field area 1/2; rostra1 somatosen- second (SII) somatosensory fields. Recently, another so- wry area, 3a; second somatosensoryarea, SII; parietal ventral area, PV; matosensory area, the parietal ventral area, PV, has been ventral somatosensory area, VS; parietal rhinal area, PR; lateral parietal area, LP;motor cortex, area 4; supplementary motor area, area identified in squirrels (Krubitzer et al., '86), New World 6; frontal ventral area, FV; pyriform cortex, PY; lateral sulcus, Is. primates (Krubitzer and Kaas, '90b) and rats (Fabri et al., '90). However, only by examining a variety of species can we confidently assign PV as a homologous cortical area in it would be beneficial to examine the cortical organization mammals. The final reason we chose the flying fox for these in an archontan, other than a primate, to see which experiments is the recent suggestion that megachiropteran features are shared by archontans, in general, and other bats may have a closer relationship to primates than other mammals. archontans (Pettigrew et al., '89). The Grandorder Ar- A second question we addressed in this study is what is chonta was first described by Gregory ('10) to include the organization of cortex caudolateral to 3b in the flying primates, megachiropteran and microchiropteran bats, Der- fox? This area corresponds to the lateral sulcus region in moptera (gliding lemurs), Scandentia (tree shrews), and primates, and the anterior ectosylvian sulcus region in cats. Macroscelididae (elephant shrews). Macroscelididae have In previous work on the grey squirrel, several fields lateral since been removed from the archontan group (McKenna, to SI were defined. These include the classically defined SII '75), and some investigators (Pettigrew and Cooper, '86) region, the parietal ventral area, PV, and the parietal rhinal consider only primates, Dermoptera, and megachiropterans area, PR (Krubitzer et al., '86). SII has been described in a to be archontans. The complex origins of the cortical number of mammals including rodents (Lende and Wool- organization of primates are presently poorly understood. sey, '56; Woolsey, '67; Welker and Sinha, '72; Nelson et al., Study of the cortical organization of a putative close sister '79; Pimentel-Souza et al., '80; Carve11 and Simons, '86; group, such as megachiropteran bats, could help illuminate Krubitzer et al., '861, carnivores (Haight, '72; Burton et al., the gap in understanding between primate and non- '82; Herron, '78; Clemo and Stein, '82), tree shrews (Sur et primate neocortical organization. al., '81),prosimian primates (Burton and Carlson, ,861, and We posed several questions in this study. First, how are simian primates (Whitsel et al., '69; Friedman et al., '80; the somatosensory representations in the anterior parietal Robinson and Burton, '80b; Pons et d.,'88; Cusick et al., cortex of the megachiropteran bat organized? In most New '89; Krubitzer and Kaas, '90b). However, there is little and Old World primates there is clear evidence for at least consensus on the organization of other somatosensory four topographically organized fields in the anterior pari- fields in addition to SII in cortex lateral to SI. Recently, PV etal cortex (Merzenich et al., '78; Kaas et al., '79; Nelson et has been defined in marmosets (Krubitzer and Kaas, '90b) al., '80; see Kaas and Pons, '88 for review). These fields and rats (Fabri et al., '90). In cats, a topographically include the primary somatosensory area 3b (SI proper), organized field adjacent to SII, termed SN (Clem0 and area 3a, area 1, and area 2. It has been proposed that this Stein, '82, '83; Burton and Kopf, '84) has been described, expansion of cortical fields in anterior parietal cortex in and in Old World primates the granular insular cortex, Ig, primates is a recent phenomenon found only in simian is in the relative location of PV. Although there are some primates (Krubitzer and Kaas, '90b). All other mammals features of SIV and Ig that are similar to PV described in examined have a primary somatosensory area, SI (see Kaas, squirrels and marmosets,
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