Somatosensory and motor representations in cerebral cortex of a primitive mammal (Monodelphis domestica): a window into the early evolution of sensorimotor cortex.
To examine the potential early stages in the evolution of sensorimotor cortex, electrophysiological studies were conducted in the primitive South American marsupial opossum, Monodelphis domestica. Somatosensory maps derived from multiunit microelectrode recordings revealed a complete somatosensory representation of the contralateral body surface within a large region of midrostral cortex (primary somatosensory cortex, or S1). A large proportion ( approximately 51%) of S1 was devoted to representation of the glaborous snout, mystacial vibrissae, lower jaw, and oral cavity (the rostrum). A second representation, the second somatosensory area (or S2), was found adjacent and caudolateral to S1 as a mirror image reversed along the representation of the glabrous snout. A reversal of somatotopic order and an enlargement of receptive fields marked the transition from S1 to S2. Mapping of excitable cortex was conducted by using intracortical microstimulation (ICMS) techniques, as well as low-impedance depth stimulation and bipolar surface stimulation. In all three procedures, electrical stimulation resulted in movements confined strictly to the face. Specifically, at virtually all sites from which movements could be evoked, stimulation resulted in only vibrissae movement. ICMS-evoked vibrissae movements typically occurred at sites within S1 with receptive fields of the mystacial vibrissae, lower jaw, and glaborous snout. Results were similar using low-impedance depth stimulation and bipolar surface stimulation techniques except that the motor response maps were generally larger in area. There was no evidence of a motor representation rostral to S1. Examination of the cytoarchitecture in this cortical region (reminiscent of typical mammalian somatosensory cortex) and the high levels of stimulation needed for vibrissae movement suggest that the parietal neocortex of Monodelphis is representative of a primitive sensorimotor condition. It possesses a complete S1 representation with an incomplete motor component overlapping the S1 representation of the face. It contains no primary motor representation. Completion of the motor representations within S1 (trunk, limbs, tail) as well as the emergence of a primary motor cortex rostral to S1 may have occurred relatively late in mammalian phylogeny.
Frost
S B
SB
Department of Molecular and Integrative Physiology and Center on Aging, University of Kansas Medical Center, Kansas City, Kansas 66160, USA.
Milliken
G W
GW
Plautz
E J
EJ
Masterton
R B
RB
Nudo
R J
RJ
D000818:Animals; D005075:Biological Evolution; D001931:Brain Mapping; D004558:Electric Stimulation; D004594:Electrophysiology; D005260:Female; D008297:Male; D008839:Microelectrodes; D009044:Motor Cortex / Q000033:anatomy & histology* / Q000166:cytology / Q000502:physiology; D009893:Opossums / Q000033:anatomy & histology*; D013003:Somatosensory Cortex / Q000033:anatomy & histology* / Q000166:cytology / Q000502:physiology