Early sensory pathways for detection of fearful conditioned stimuli: tectal and thalamic relays

Sensory stimuli acquire significance through learning. A neutral sensory stimulus can become a fearful conditioned stimulus (CS) through conditioning. Here we report that the sensory pathways used to detect the CS depend on the conditioning paradigm. Animals trained to detect an electrical somatosensory stimulus delivered to the whisker pad in an active avoidance task were able to detect this CS and perform the task when a reversible or irreversible lesion was placed in either the somatosensory thalamus or the superior colliculus contralateral to the CS. However, simultaneous lesions of the somatosensory thalamus and superior colliculus contralateral to the CS blocked performance in the active avoidance task. In contrast, a lesion only of the somatosensory thalamus contralateral to the same CS, but not of the superior colliculus, blocked performance in a pavlovian fear conditioning task. In conclusion, during pavlovian fear conditioning, which is a situation in which the aversive outcome is not contingent on the behavior of the animal, the sensory thalamus is a critical relay for the detection of the CS. During active avoidance conditioning, a situation in which the aversive outcome is contingent on the behavior of the animal (i.e., the animal can avoid the aversive event), the sensory thalamus and the superior colliculus function as alternative routes for CS detection. Thus, even from early stages of sensory processing, the neural signals representing a CS are highly distributed in parallel and redundant sensory circuits, each of which can accomplish CS detection effectively depending on the conditioned behavior.