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J Neurophysiol (February 1, 2003). 10.1152/jn.00799.2002
Submitted on Submitted 30 May 2002; accepted in final form 8 October 2002
Department of Anatomy and Neurosciences and Marine Biomedical Institute, The University of Texas Medical Branch, Galveston, Texas 77555-1069
Neugebauer, Volker and
Weidong Li.
Differential Sensitization of Amygdala Neurons to Afferent
Inputs in a Model of Arthritic Pain. J. Neurophysiol. 89: 716-727, 2003. Pain is associated with negative
affect such as anxiety and depression. The amygdala plays a key role in
emotionality and has been shown to undergo neuroplastic changes in
models of affective disorders. Many neurons in the central nucleus of
the amygdala (CeA) are driven by nociceptive inputs, but the role of
the amygdala in persistent pain states is not known. This study is the
first to address nociceptive processing by CeA neurons in a model of prolonged pain. Extracellular single-unit recordings were made from 41 CeA neurons in anesthetized rats. Each neuron's responses to brief
mechanical stimulation of joints, muscles, and skin and to cutaneous
thermal stimuli were recorded. Background activity, receptive field
size, and threshold were mapped, and stimulus-response functions were
constructed. These parameters were measured repeatedly before and after
induction of arthritis in one knee by intraarticular injections of
kaolin and carrageenan. Multireceptive (MR) amygdala neurons
(n = 20) with excitatory input from the knee joint
responded more strongly to noxious than to innocuous mechanical stimuli of deep tissue (n = 20) and skin (n = 11). After induction of arthritis, 18 of 20 MR neurons developed
enhanced responses to mechanical stimuli and expansion of receptive
field size. These changes occurred with a biphasic time course (early
peak: 1-1.5 h; persistent plateau phase: after 3-4 h). Responses to
thermal stimuli did not change (7 of 7 neurons), but background
activity (16 of 18 neurons) and electrically evoked orthodromic
activity (11 of 12 neurons) increased in the arthritic state.
Nociceptive-specific (NS) neurons (n = 13) showed no
changes of their responses to mechanical, thermal, and electrical
stimulation after induction of arthritis. A third group of neurons did
not respond to somesthetic stimuli under control conditions (noSOM
neurons; n = 8) but developed prolonged responses to
mechanical, but not thermal, stimuli in arthritis (5 of 8 neurons).
These data suggest that prolonged pain is accompanied by enhanced
responsiveness of a subset of CeA neurons. Their sensitization to
mechanical, but not thermal, stimuli argues against a nonspecific state
of hyperexcitability. MR neurons could serve to integrate and evaluate
information in the context of prolonged pain. Recruitment of noSOM
neurons increases the gain of amygdala processing. NS neurons preserve
the distinction between nociceptive and nonnociceptive inputs.
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