The role of the dorsal and ventral hippocampus in olfactory working memory
Highlights
► The ventral hippocampus supports working memory for odor information. ► The dorsal hippocampus does not support working memory for odor information. ► All groups of rats could discriminate between the odors. ► There were no effects on odor pattern separation.
Introduction
There has been a recent surge in research concerning the differential roles of the dorsal and ventral portions of the hippocampus. The hypotheses driving this research are based on differences in intrinsic and extrinsic connectivity and molecular differences along the dorsal–ventral axis of the hippocampus (Amaral and Witter, 1989, Fanselow and Dong, 2010, Risold and Swanson, 1996). Theories encompassing ventral hippocampal function include a role in mediating anxiety (Bannerman et al., 2004, Barkus et al., 2010), hyponeophagia (Bannerman et al., 2002), retrieval of contextual and stimulus specific information during trace and delay fear conditioning (cf. Rogers et al., 2006, Rudy and Matus-Amat, 2005, Yoon and Otto, 2007), and behavioral inhibition (cf. Gray and McNaughton, 1983, Gray and McNaughton, 2001, McDonald et al., 2006). The dorsal hippocampus has been proposed as the neurological substrate underlying spatio-temporal processing (O’Keefe and Nadel, 1978, Rolls and Kesner, 2006).
On the basis of these hypotheses, numerous labs have effectively dissociated the dorsal and ventral halves of the hippocampus across spatial and nonspatial information processing (Bannerman et al., 1999, Moser and Moser, 1998). Despite the aforementioned dissociations, there is evidence that the ventral hippocampus may support spatial memory and assist in performance of spatial and nonspatial tasks primarily dependent upon the dorsal hippocampus if the animal is trained properly (DeHoz et al., 2003, McDonald et al., 2006). In contrast, the ventral, but not dorsal, hippocampus may be more important for mnemonic processing of olfactory information. Support for this idea comes from a series of fMRI studies showing that processing of odor information resulted in greater activation of the ventral compared to the dorsal hippocampus in mice and anterior compared to posterior hippocampus in humans (Cerf-Ducastel and Murphy, 2001, Kent et al., 2007). Thus, there is a good possibility that the ventral hippocampus supports processing of odor information (Cerf-Ducastel and Murphy, 2001, Kent et al., 2007, Pentkowski et al., 2006), whereas the dorsal hippocampus supports processing for spatial information (Moser and Moser, 1998, Rolls and Kesner, 2006). Whether working memory for odor information is a function of the ventral or dorsal hippocampus is not known. Thus, the purpose of the present study is to examine the role of the dorsal and ventral hippocampus in a working memory task for odors that consist of a series of aliphatic acids with unbranched carbon chains that varied from two- to six-carbons in length (see Cleland, Morse, Yue, & Linster, 2002). The odors were selected in order to assess whether the dorsal or ventral hippocampal lesions would also produce an odor pattern separation effect. A pattern separation function can be seen when there is poor performance for odors that are close together in terms of carbon chain lengths followed by improved performance as the distance in terms of carbon chain lengths increases. A separation function for odors could be based on perceptual-based similarity or memory -based similarity. In the present study the emphasis will be on memory-based similarity.
Section snippets
Subjects
Nineteen male Long Evans rats (260–350 g) were housed independently in standard plastic rodent cages and maintained on a 12-h light/dark cycle. All testing was conducted in the light proportion of the light/dark cycle. Each rat was initially food-deprived to approximately 85–90% of their free-feeding weight, but was allowed free access to water throughout testing. All surgical and experimental protocols conformed to University of Utah IACUC and AAALAC protocols and regulations. The health of the
Histology
Sections were photographed and the regions of interest were outlined using Image J. The ventral hippocampus comprised the ventral 50% of the hippocampus, including the ventral CA3 and CA1 pyramidal cell layers and the ventral dentate gyrus granule cell layer–the ventral subiculum was excluded. The dorsal hippocampus comprised the dorsal 50% of the hippocampus, including the dorsal CA3 and CA1 pyramidal cell layers and the dorsal dentate gyrus granule cell layer–the dorsal subiculum was
Discussion
The results indicate that the ventral, but not dorsal hippocampus, mediates working memory for odor information. It is important to note that the dorsal and ventral hippocampal lesioned groups did not have any difficulty in olfactory discrimination, suggesting intact olfactory perception. Additional data supporting a greater involvement of the ventral hippocampus compared to the dorsal hippocampus in processing odor information comes from the findings demonstrating that context conditioning to
References (37)
- et al.
The three-dimensional organization of the hippocampal formation: A review of anatomical data
Neuroscience
(1989) - et al.
Regional dissociations within the hippocampus–memory and anxiety
Neuroscience and Biobehavioral Reviews
(2004) - et al.
Hippocampal NMDA receptors and anxiety: At the interface between cognition and emotion
European Journal of Pharmacology
(2010) - et al.
Lesions of structures showing FOS expression to cat presentation: Effects on responsivity to a cat, cat odor, and nonpredator threat
Neuroscience and Biobehavioral Reviews
(2005) - et al.
Are the dorsal and ventral hippocampus functionally distinct structures?
Neuron
(2010) - et al.
Comparison between the behavioural effects of septal and hippocampal lesions: A review
Neuroscience and Biobehavioral Reviews
(1983) - et al.
Role of the hippocampus in goal-oriented tasks requiring retrieval of spatial versus non-spatial information
Neurobiology of Learning and Memory
(2010) - et al.
Gradual changes in hippocampal activity support remembering the order of events
Neuron
(2007) - et al.
Effects of ventral and dorsal CA1 subregional lesions on trace fear conditioning
Neurobiology of Learning and Memory
(2006) - et al.
A computational theory of hippocampal function, and empirical tests of the theory
Progress in Neurobiology
(2006)
Spatial memory in the rat requires the dorsolateral band of the entorhinal cortex
Neuron
Olfactory perceptual learning: The critical role of memory in odor discrimination
Neuroscience and Biobehavioral reviews
Differential contribution of dorsal vs. Ventral hippocampus to auditory trace fear conditioning
Neurobiology of Learning and Memory
Double dissociation of function within the hippocampus: Spatial memory and hyponeophagia
Behavioral Neuroscience
Double dissociation of function within the hippocampus: A comparison of dorsal, ventral, and complete hippocampus cytotoxic lesions
Behavioral Neuroscience
Olfactory perceptual stability and discrimination
Nature Neuroscience
Muscarinic receptor blockade in ventral hippocampus and prelimbic cortex impairs memory for socially transmitted food preference
Hippocampus
FMRI activation in response to odorants orally delivered in aqueous solutions
Chemical Senses
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