Neuronal responses related to the novelty and familarity of visual stimuli in the substantia innominata, diagonal band of Broca and periventricular region of the primate basal forebrain

Abstract

This study examined correlates of memory processes in neuronal activity recorded from the substantia innominata, the diagonal band of Broca and the periventricular region or the basal forebrain of monkeys performing recognition and/or visual discrimination tasks. Two types of neurons were found that responded differentially to stimuli on the basis of their novelty or their familiarity. Neurons (5/572) in the periventricular region rostral to the thalamus and caudal to the anterior commissure responded to familiar stimuli with increases in firing rate. Neurons in the substantia innominata (16/1058) and in the diagonal band (14/489) responded maximally to novel stimuli, with smaller responses to reappeared presentations of these stimuli. The properties of these two types of neurons were similar in three respects: (1) the magnitude of the differential response to novel and familiar presentations of stimuli were largest for stimuli presented on successive trials, and were attenuated for stimuli that had not been seen for some intervening trials; (2) both types of neurons responded to highly familiar stimuli as if they were novel if they had not been recently seen; (3) both types responded to two- and three-dimensional stimuli; and were recorded in rhesus monkeys trained on the recognition tasks and in untrained cynomolgus monkeys. An injection of HRP into the periventricular region of one monkey resulted in retrograde labeling of ventromedial regions of the prefrontal, cingulate and temporal cortices, of the amygdala, medial thalamus, supramammillary region of the midbrain. These data indicate that information about the novelty, familiarity or recency of presentation of visual stimuli is reflected in the responses of some basal forebrain neurons. Neurons in the substantia innominata and diagonal band of Broca could not be distinguished using the battery of applied tests, suggesting functional mechanisms common to both regions. The results of the anatomical experiment suggest that ventromedial limbic cortical and subcortical regions projecting to or through the periventricular region may be important for the transmission of information about visual stimuli and for memory function.