Emotional and Behavioral Correlates of Mediodorsal Thalamic Neurons during Associative Learning in Rats

Neuronal activity was recorded from the mediodorsal thalamic nucleus (MD) of behaving rats that were trained to lick a protruding spout just after a conditioned stimulus to obtain reward or to avoid shock. Conditioned stimuli included both elemental (auditory or visual stimuli) and configural (simultaneous presentation of auditory and visual stimuli predicting reward outcome opposite that predicted by each stimulus presented alone) stimuli. Of 122 MD neurons responding during the task, the activity of 13 increased just before licking only during the task, but not before spontaneous licking during the intertrial interval (conditioned behavior related). These conditioned behavior-related neurons were located mainly in the lateral MD, which has intimate anatomical connections with motor-related areas such as anterior cingulate and striatum. The activity of the other 109 neurons was related to conditioned stimulation (conditioned stimulus related). Most of these neurons responded differentially to both elemental and configural stimuli in terms of reward contingency, and also changed their responses during extinction and relearning trials. Conditioned stimulus-related neurons with latencies <300 msec were located mainly in the rostromedial MD, which receives afferents from the basolateral nucleus of the amygdala in which sensory information from various sources converge. Furthermore, most differential neurons that were tested responded during the delay period in a reward task in which a delay was imposed between the conditioned stimulus and reward delivery. The present results, along with previous anatomical studies, suggest the existence of two limbic circuits: anterior cingulate–striatum–lateral MD (motor) and amygdala–medial MD–orbital prefrontal cortex (short-term memory/emotion).