Relationships between the superior colliculus and hippocampus: Neural and behavioral considerations

Abstract

AbstractTheories of superior collicular and hippocampal function have remarkable similarities. Both structures have been repeatedly implicated in spatial and attentional behaviour and in inhibitory control of locomotion. Moreover, they share certain electrophysiological properties in their single unit responses and in the synchronous appearance and disappearance of slow wave activity. Both are phylogenetically old and the colliculus projects strongly to brainstem nuclei instrumental in the generation of theta rhythm in the hippocampal EECOn the other hand, close inspection of behavioural and electrophysiological data reveals disparities. In particular, hippocampal processing mainly concerns stimulus ambiguity, contextual significance, and spatial relations or other subtle, higher order characteristics. This requires the use of largely preprocessed sensory information and mediation of poststimulus investigation. Although collicular activity must also be integrated with that of “higher” centres (probably to a varying degree, depending on the nature of stimuli being processed and the task requirements), its primary role in attention is more “peripheral” and specific in controlling orienting/localisation via eye and body movements toward egocentrically labelled spatial positions. In addition, the colliculus may exert a nonspecific influence in alerting higher centres to the imminence of information potentially worthy of focal attention. Nevertheless, it is noteworthy that collicular and hippocampal lesions produce deficits on similar tasks, although the type of deficit is usually different (often opposite) in each case. Functional overlap between hippocampus and colliculus (i.e., strategically synchronised or mutually interdependent activity) is virtually certain vis-à-vis stimulus sampling, for example in the acquisition of information via vibrissal movements and visual scanning. In addition, insofar as stimulus significance is a factor in collicular orienting mechanisms, the hippocampus — cingulate – cortex — colliculus pathway may play a significant role, modulating collicular responsiveness and thus ensuring an attentional strategy appropriate to current requirements (stimulus familiarity, stage of learning). A tentative “reciprocal loop” model is proposed which bridges physiological and behavioural levels of analysis and which would account for the observed degree and nature of functional overlap between the superior colliculus and hippocampus.