Neural substrates for tone-conditioned bradycardia demonstrated with 2-deoxyglucose. I. Activation of auditory nuclei.

The 2-deoxyglucose (2-DG) autoradiographic method was used to map the metabolic activity of auditory nuclei before, during and after conditioning. The experiment involved freely behaving rats in a Pavlovian conditioning paradigm in which a 4-5 kHz frequency modulated tone (CS) was paired with aversive electrical stimulation of the midbrain reticular formation (US). The unconditioned response was a rapid decrease in heart rate evoked by the US. Eight groups of rats were subjected to: (1) the tone CS before conditioning; (2) the US alone; (3) the paired CS-US (acquisition); (4) the tone CS after conditioning (extinction); (5) the US prior to the CS (sensitization); (6) the unpaired CS-US (pseudoconditioning); (7) the CS after pseudoconditioning; and (8) no stimulation. The major finding was the differential effect produced by the same tone before and after conditioning. The results showed that: (a) reticular mechanisms interact with incoming acoustic stimuli and modulate the response of auditory nuclei; (b) within each auditory nucleus the region of overlap of the spatial representations of CS and US developed an enhanced metabolic response during conditioning; and (c) the CS representation within the neuronal space of the tonotopic maps in all auditory nuclei, with the exception of the medial geniculate, reflected the learned behavioral value of the CS. The changes revealed by the 2-DG method represent the first anatomical demonstration of the activating effects of reticular sensitization and conditioning on a sensory system. The observations support the conclusion that auditory responses are dependent on the physical as well as on the behavioral parameters of a stimulus.