THE NEURAL BASIS OF LEARNING 



1483 



cortex of rabbit to be the major electrical event 

 paralleling the development of Type I conditioning 

 to a sound CS followed by shocks (US) to the paw. 

 If the shock to the paw is very weak, on the other 

 hand, the sound CS produces alpha block that un- 

 masks bursts of high frequency waves, but no 3 to 

 5 per sec. waves whatever appear. This report raises 

 the important but unsolved question of what sys- 

 tematic EEG differences, if any, are associated with 

 variation in strength of both CS and US. Popov & 

 Popov have further been concerned with long-lasting 

 cyclical alterations of alpha amplitude that accompany 

 light flash CS; the original papers should be consulted 

 for the relation of these to visual afterimages and 

 regarding their conditioning by sounds (191-193). 



Siihi ortical Structures 



Much recent experimentation has dealt with elec- 

 trical activity in subcortical structures during Type I 

 learning. Behind this work lie the three new concepts 

 about the nervous system thai render obsolete so 

 much of the neurophysiology of 5 or 10 years ago. 

 These are a) the demonstration in unanesthetized 

 animals of the widespread influence of the reticular 

 formation upon the organizing and integrating func- 

 tions of the brain, b) the possibility that the descending 

 sensory pathways constitute "feed-back' loops for 

 control of afferent input to the brain, and c) the 

 concept that limbic system structures arc intimately 

 concerned with emotional behavior and thus with 

 any learned activity that has an emotional component. 

 The reader will find these ideas discussed ai length 

 elsewhere in this volume. Our interest is in those 

 experiments which have been done to relate them 

 specifically to the learning situation. 



Il is clear that a CS (e.g. auditory clicks) not only 

 evokes the expected responses throughout the ap- 

 propriate sensor) system but in addition activates parts 

 of the brain to which anatomical projections from 

 thai modality have not been described or are poorly 

 understood (e.g. limbic system, reticular formation). 

 At a given recording site, the responses vary wide!) 

 in amplitude, latency and duration, but these features 

 have not yet been properly analyzed. Thus far, the 

 only reasonably consistent finding is that some elec- 

 trical response to the CS tends to be large and stable 

 in the conditioned animal, while being small, labile 

 and recordable at fewer brain locations in the un- 

 conditioned or extinguished animal. As in the case 

 of cortical electrical correlates, however, agreement 



has not been reached as to which subcortical events 

 are invariably related to learning. 



Important information on events in the lower 

 nuclei of classical afferent pathways comes mainly 

 from the auditory system of cats. Hernandez-Peon 

 and associates (90) studied the response of the cochlear 

 nucleus in Type I learning to tonal stimulation (CS) 

 paired with shock (US) to the hind leg. The cochlear 

 nucleus response, having diminished in size during 

 habituation of the animal to the apparatus, attained 

 large size and increased duration when the conditioned 

 leg withdrawal was fully developed. Similar results 

 have been reported in cats that received shocks 

 irregularly when click stimuli were being presented 

 (67); correlated with the behavioral response de- 

 veloped to clicks, the evoked response in the cochlear 

 nucleus and medial sjeniculate (and auditory cortex 

 as well 1 bee. inie large and regular in comparison with 

 responses in the habituated and extinguished state 

 (see also 30, 3 1 , 9 1 , no) 



A small amount of information is available about 

 the activities of the limbic swem in conditioning. 

 Waves of ;; 10 5 per sec. from a presumed caudal 

 hippocampal location have been reported to fill 

 die CS-US interval in a Type I situation; but such 

 waves were absenl from septal and other hippocampal 

 locations (149). Evoked responses appear and become 

 stable in the hippocampus and amygdala .is well as 



in the caudate nucleus when a s d I S is employed 



in Type I conditioning (67). The amygdala of the 

 cat seems unique among limbic structures in that 

 40 to 45 per see. waves of high amplitude appear in 

 it during conditioning of a shock to sound (135); 

 these diminish or disappear with extinction and can 

 be re-established by repetition of the conditioning 

 procedure. 



As for the reticular formation, some remarkable 

 electrical events within it appear to be related to 

 the learning process 1250). Cats were prepared with 

 electrodes in the cortex, reticular formation, and 

 ventral anterior and center median nuclei of the 

 thalamus. A tone (CS) was presented for 5 to 10 

 sec, followed shortly after its ousel by a brief train of 

 light flashes at 5 per sec. (US). Alter many pairings, 

 the tone alone produced both the alpha block CR 

 and new waves in the cortical leads. In addition, a 

 5 per sec. rhythm appeared in the subcortical loca- 

 tions which, at the reticular formation leads in 

 particular, developed promptly upon the tone-onset 

 and persisted long after the tone was turned off. 

 After very many pairings, the 5 per sec. rhythm 

 might last for more than a minute when the animal 



