Parallel and interrelated neural systems underlying adaptive navigation.

The ability to process in parallel multiple forms of sensory information, and link sensory-sensory associations to behavior, presumably allows for the opportunistic use of the most reliable and predictive sensory modalities in diverse behavioral contexts. Evolutionary considerations indicate that such processing may represent a fundamental operating principle underlying complex sensory associations and sensory-motor integration. Here, we suggest that animal navigation is a particularly useful model of such opportunistic use of sensory and motor information because it is possible to study directly the effects of memory on neural system functions. First, comparative evidence for parallel processing across multiple brain structures during navigation is provided from the literatures on fish and rodent navigation. Then, based on neurophysiological evidence of coordinated, multiregional processing, we provide a neurobiological explanation of learning and memory effects on neural circuitry mediating navigation.

Parallel processing across neural systems: implications for a multiple memory system hypothesis.

A common conceptualization of the organization of memory systems in brain is that different types of memory are mediated by distinct neural systems. Strong support for this view comes from studies that show double (or triple) dissociations between spatial, response, and emotional memories following selective lesions of hippocampus, striatum, and the amygdala. Here, we examine the extent to which hippocampal and striatal neural activity patterns support the multiple memory systems view. A comparison is made between hippocampal and striatal neural correlates with behavior during asymptotic performance of spatial and response maze tasks. Location- (or place), movement, and reward-specific firing patterns were found in both structures regardless of the task demands. Many, but not all, place fields of hippocampal and striatal neurons were similarly affected by changes in the visual and reward context regardless of the cognitive demands. Also, many, but not all, hippocampal and striatal movement-sensitive neurons showed significant changes in their behavioral correlates after a change in visual context, irrespective of cognitive strategy. Similar partial reorganization was observed following manipulations of the reward condition for cells recorded from both structures, again regardless of task. Assuming that representations that persist across context changes reflect learned information, we make the following conclusions. First, the consistent pattern of partial reorganization supports a view that the analysis of spatial, response, and reinforcement information is accomplished via an error-driven, or match-mismatch, algorithm across neural systems. Second, task-relevant processing occurs continuously within hippocampus and striatum regardless of the cognitive demands of the task. Third, given the high degree of parallel processing across allegedly different memory systems, we propose that different neural systems may effectively compete for control of a behavioral expression system. The strength of the influence of any one neural system on behavioral output is likely modulated by factors such as motivation, experience, or hormone status.