Sensory representation abnormalities that parallel focal hand dystonia in a primate model.
In our hypothesis of focal dystonia, attended repetitive behaviors generate aberrant sensory representations. Those aberrant representations interfere with motor control. Abnormal motor control strengthens sensory abnormalities. The positive feedback loop reinforces the dystonic condition. Previous studies of primates with focal hand dystonia have demonstrated multi-digit or hairy-glabrous responses at single sites in area 3b, receptive fields that average ten times larger than normal, and high receptive field overlap as a function of horizontal distance. In this study, we strengthen and elaborate these findings. One animal was implanted with an array of microelectrodes that spanned the border between the face and digits. After the animal developed hand dystonia, responses in the initial hand representation increasingly responded to low threshold stimulation of the face in a columnar substitution. The hand-face border that is normally sharp became patchy and smeared over 1 mm of cortex within 6 weeks. Two more trained animals developed a focal hand dystonia variable in severity across the hand. Receptive field size, presence of multi-digit or hairy-glabrous receptive fields, and columnar overlap covaried with the animal's ability to use specific digits. A fourth animal performed the same behaviors without developing dystonia. Many of its physiological measures were similar to the dystonic animals, but receptive field overlap functions were minimally abnormal, and no sites shared response properties that are normally segregated such as hairy-glabrous combined fields, or multi-digit fields. Thalamic mapping demonstrated proportionate levels of abnormality in thalamic representations as were found in cortical representations.
Blake
David T
DT
Coleman Laboratory, Keck Center for Integrative Neuroscience, and Department of Otolaryngology-Head and Neck Surgery, University of California, San Francisco, USA. dblake@phy.ucs.edu
Byl
Nancy N
NN
Cheung
Steven
S
Bedenbaugh
Purvis
P
Nagarajan
Srikantan
S
Lamb
Michelle
M
Merzenich
Michael
M
D000818:Animals; D016645:Aotidae; D001931:Brain Mapping; D002540:Cerebral Cortex / Q000503:physiopathology*; D003216:Conditioning, Operant / Q000502:physiology; D004195:Disease Models, Animal; D020821:Dystonic Disorders / Q000503:physiopathology*; D005145:Face / Q000294:innervation; D007839:Functional Laterality / Q000502:physiology; D006225:Hand / Q000294:innervation*; D018737:Hand Strength / Q000502:physiology; D006801:Humans; D009046:Motor Neurons / Q000502:physiology; D009415:Nerve Net / Q000503:physiopathology; D013003:Somatosensory Cortex / Q000503:physiopathology; D013239:Stereotyped Behavior / Q000502:physiology; D013788:Thalamus / Q000503:physiopathology