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 Previous Article
Journal of Neuroscience, Vol 14, 3969-3984, Copyright © 1994 by Society for Neuroscience
Responses of tonically active neurons in the primate's striatum undergo systematic changes during behavioral sensorimotor conditioning
T Aosaki, H Tsubokawa, A Ishida, K Watanabe, AM Graybiel and M Kimura
Jichi Medical School, Department of Physiology, Tochigi, Japan.
The basal ganglia have been implicated in motor planning and motor
learning. In the study reported here, we directly tested for response
plasticity in striatal neurons of macaque monkeys undergoing Pavlovian
conditioning. To focus the study, we recorded from the tonically active
neurons (TANs) of the striatum, which are known to respond to conditioned
sensory stimuli that signal reward delivery and elicit behavioral
reactions. The activities of 858 TANs were recorded extracellularly from
the striatum in alert behaving macaque monkeys before, during, and after
the acquisition of a classical conditioning task. Two monkeys were trained
to lick reward juice delivered on a spoon simultaneously with the
presentation of a click. Almost no licks were triggered by the cues at the
start of training, but by the fifth day more than 90% of licks were
triggered, and values were near 100% for the remainder of the 3 week
training period. In the striatum, only a small number of TANs responded to
the clicks at the start before conditioning (about 17%). During training,
the numbers of responding TANs gradually increased, so that by the end of
training more than 50- 70% of the TANs recorded (51.3-73.5%) became
responsive to the clicks. The responses consisted of a pause in firing that
occurred approximately 90 msec after the click and that was in some cells
preceded by a brief activation and in most cells was followed by a rebound
excitation. Prolonged recordings from single TANs (n = 6) showed that
individual TANs can acquire a conditioned response within at least as short
a time as 10 min. TANs retained such responsiveness after overtraining, and
also after a 4 week intermission in training. When the monkey was trained
to receive rewards in relation to a new conditioning stimulus, TANs were
capable of switching their sensory response to the new stimulus.
Histological reconstruction showed that the TANs that became responsive
were broadly distributed in the region of striatum explored, which included
the dorsal half to two-thirds of the caudate nucleus and putamen over a
large anteroposterior span. We conclude that, during the acquisition of a
sensorimotor association, TANs widely distributed through the striatum
become responsive to sensory stimuli that induce conditioned behavior. This
distributed change in activity could serve to modulate the activity of
surrounding projection neurons in the striatum engaged in mediating learned
behavior.
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