Reverse effects of conditioning produced by two different unconditioned stimuli on thalamocortical transmission

Actions of cerebellothalamocortical (CTC) networks on the musculature can be modified by associative conditioning in adult animals. During conditioning, electrical stimulation of a CTC network involved in forearm flexion movements results in either flexion or extension responses, depending on the somatosensory information given by the unconditioned stimulus (UCS). In the present work we attempt to determine what kind of neurobiological changes induced in the CTC pathways as a consequence of distinct somesthetic messages could lead to different conditioned motor responses. Two conditioning procedures in which distinct UCSs were successively applied to awake cats in chronic preparation. The conditioned stimulus (CS) was an electrical subthreshold stimulation of an interpositus nucleus (IN) site at the origin of CTC circuits controlling forelimb flexion movements. It was first paired with a UCS applied to the skin above the wrist, also producing a forearm flexion reflex, and second with a UCS applied more proximally on the forearm, producing a backward withdrawal reflex of the forelimb. The two procedures, termed "concordant" and "discordant," respectively, were carried out in a different order on the same cats, separated by 2 mo of rest. The effects of conditioning were assessed from the characteristics of the motor reponses induced by the CS and from the properties of the CTC transmission analyzed on the cortical field potentials induced by IN stimulation. The concordant procedure resulted in persistent enhancement of the amplitude and rate of occurrence of the forearm flexions induced by the CS. Concomitantly, an increase of the di- and/or trisynaptic excitatory negative component of the field potentials induced by the CS in layers III and V of the elbow motor cortical representation was observed. In contrast, during the discordant procedure, the forearm flexions initially induced by the IN stimulation were progressively abolished in favor of forearm extensions, and, in parallel, a depression of the excitatory negative component of the cortical responses and the appearance of a later large positive event were observed. The selectivity and the associative nature of the motor and synaptic changes were tested. The two kinds of events appeared to be linked. It was concluded that somesthetic information given by the UCS seems to be a critical factor in the determination of both the motor and synaptic CTC changes induced by associative conditioning. Alterations of cerebellocortical transmission appeared to constitute one of the neurobiological substrates for conditioned motor changes.