Memory for Spatial Location: Role of the Hippocampus in Mediating Spatial Pattern Separation

Paul E. Gilbert, Raymond P. Kesner, William E. DeCoteau
1998 Journal of Neuroscience  
A paradigm based on measuring short-term memory for spatial location information as a function of spatial similarity between distal cues was developed to examine the role of pattern separation in the modulation of short-term memory for spatial information. A delayed-match-to-sample for spatial location task using a dryland version of the Morris water maze was used to assess spatial pattern separation in male Long-Evans rats. In the sample phase, animals were trained to displace an object that
more » ... vered a baited food well in one of 15 spatial locations along a row of food wells perpendicular to a start box. In the ensuing choice phase, the animal was allowed to choose between two objects identical to the sample phase object. One covered the same baited food well as did the object in the study phase (correct choice), and another foil object (incorrect choice) covered a different unbaited food well along the row of wells. Five spatial separations were randomly used to separate the correct object from the foil object. After reaching a criterion before the operation, animals were given either hippocampal or cortical control lesions. In trials after the operation, control animals matched their performance before the operation across all spatial separations. In contrast, hippocampal-lesioned animals displayed impairments across all spatial separations with the exception of the longest (105 cm) spatial separation. The results suggest that the hippocampus may serve to separate incoming spatial information by temporarily storing one place separate from another. It is proposed that hippocampal lesions decrease efficiency in pattern separation, resulting in impairments in trials with increased spatial similarity among workingmemory representations. The hippocampus has been assumed to subserve a number of processes including (1) spatial and temporal separation of events associated with temporary memory representations of new spatial information (Shapiro and Olton, 1994), (2) short-term memory or working-memory representations of new information (Olton et al., 1979; Kesner, 1990) , (3) consolidation or elaborative rehearsal of new information (Milner, 1966; Squire, 1992; Schacter et al., 1996) , (4) retrieval of new information based on flexibility and action (Eichenbaum, 1994; Johnson and Chalfonte, 1994) , and (5) the formation of cognitive maps (O'Keefe and Nadel, 1979) . There is ample evidence indicating an important role for the hippocampus in mediating consolidation, working-memory, retrieval, and cognitive map processes, but its role in the separation of patterns of incoming spatial information is in need of a moredetailed behavioral analysis (Milner, 1966; Olton et al., 1979; Kesner, 1990; Squire, 1992; Eichenbaum, 1994; Johnson and Chalfonte, 1994; Schacter et al., 1996) . Several computational models of hippocampal f unction suggest that the hippocampus is involved in pattern separation or orthogonalization of sensory input information (McNaughton, 1989; McNaughton and Nadel, 1990; Rolls, 1990; O'Reilly and McC lelland, 1994; Shapiro and Olton, 1994) . Based on sparse connections and strong inhibitory interactions within the hip-pocampus, these models posit that relevant sensory information is processed by hippocampal neurons perhaps by providing spatial and temporal markers for the coding of sensory information. This would ensure that new highly processed sensory information is organized within the hippocampus in such a way that remembering and temporarily storing one place separate from another place in time and space is enhanced. Similarly, Nadel (1994) suggested that one process function of the hippocampus is to separate and organize spatial representations within memory. Enhanced spatial similarity between distal cues and decreased efficiency in pattern separation could represent a key process deficiency in hippocampal-lesioned rats. One of the most popular means for testing hippocampal function is the water maze. In this task, enhanced spatial similarity between distal cues, because of different start locations, could account for impairments in the acquisition of the task. Support for this idea comes from the observations of Eichenbaum et al. (1990) who demonstrated that when fimbria-fornix-lesioned rats were trained on the water maze task from only a single starting position (a condition in which there is less spatial similarity among spatial cues), there were minimal learning deficits, whereas training from many different starting points resulted in learning difficulties. It is also interesting to note that the deficits observed in the fornix-lesioned group occurred only in trials requiring the flexible use of novel workingmemory information as in the variable-start condition. In a somewhat similar study, it was shown that when only one spatial location was correct on an eight-arm maze, total hippocampallesioned rats learned the task rather readily. However, they were impaired when the correct arm varied from trial to trial (Hunt et al., 1994) . Thus, pattern separation may play a role in working memory as well as in acquisition of new spatial information.
doi:10.1523/jneurosci.18-02-00804.1998 pmid:9425021 fatcat:m6vucadzl5bmbjhk22pipoy6qi