Organization of somatosensory cortex in monotremes: in search of the prototypical plan.
The present investigation was designed to determine the number and internal organization of somatosensory fields in monotremes. Microelectrode mapping methods were used in conjunction with cytochrome oxidase and myelin staining to reveal subdivisions and topography of somatosensory cortex in the platypus and the short-billed echidna. The neocortices of both monotremes were found to contain four representations of the body surface. A large area that contained neurons predominantly responsive to cutaneous stimulation of the contralateral body surface was identified as the primary somatosensory area (SI). Although the overall organization of SI was similar in both mammals, the platypus had a relatively larger representation of the bill. Furthermore, some of the neurons in the bill representation of SI were also responsive to low amplitude electrical stimulation. These neurons were spatially segregated from neurons responsive to pure mechanosensory stimulation. Another somatosensory field (R) was identified immediately rostral to SI. The topographic organization of R was similar to that found in SI; however, neurons in R responded most often to light pressure and taps to peripheral body parts. Neurons in cortex rostral to R were responsive to manipulation of joints and hard taps to the body. We termed this field the manipulation field (M). The mediolateral sequence of representation in M was similar to that of both SI and R, but was topographically less precise. Another somatosensory field, caudal to SI, was adjacent to SI laterally at the representation of the face, but medially was separated from SI by auditory cortex. Its position relative to SI and auditory cortex, and its topographic organization led us to hypothesize that this caudal field may be homologous to the parietal ventral area (PV) as described in other mammals. The evidence for the existence of four separate representations in somatosensory cortex in the two species of monotremes indicates that cortical organization is more complex in these mammals than was previously thought. Because the two monotreme families have been separate for at least 55 million years (Richardson, B.J. [1987] Aust. Mammal. 11:71-73), the present results suggest either that the original differentiation of fields occurred very early in mammalian evolution or that the potential for differentiation of somatosensory cortex into multiple fields is highly constrained in evolution, so that both species arrived at the same solution independently.
Krubitzer
L
L
Department of Physiology and Pharmacology, University of Queensland, Australia.
Manger
P
P
Pettigrew
J
J
Calford
M
M
D000818:Animals; D001303:Auditory Cortex / Q000033:anatomy & histology / Q000502:physiology; D004558:Electric Stimulation; D008839:Microelectrodes; D008959:Models, Neurological; D010296:Parietal Lobe / Q000033:anatomy & histology / Q000502:physiology; D010812:Physical Stimulation; D010987:Platypus / Q000033:anatomy & histology*; D011984:Sensory Receptor Cells / Q000502:physiology; D013003:Somatosensory Cortex / Q000033:anatomy & histology* / Q000502:physiology; D004442:Tachyglossidae / Q000033:anatomy & histology*; D014793:Visual Cortex / Q000033:anatomy & histology / Q000502:physiology