Both dorsal and ventral hippocampus contribute to spatial learning in Long–Evans rats

doi:10.1016/S0304-3940(03)00473-7

Neuroscience Letters

Volume 345, Issue 2, 17 July 2003, Pages 131-135

https://doi.org/10.1016/S0304-3940(03)00473-7 Get rights and content

Abstract

The hippocampus (HPC) may be functionally heterogeneous in supporting spatial learning in rats. Thus, dorsal but not ventral HPC lesions have been reported to impair acquisition in the Morris water task which consists of finding a submerged platform in a pool filled with opaque water. To further investigate the functional differences between dorsal and ventral HPC regions, we used a one-trial matching to position water task in which the submerged platform occupied a different position during each session. This task is very sensitive to HPC damage. The results show that either dorsal or ventral HPC NMDA lesions disrupt the rapid acquisition of new place information. The acquisition deficit diminishes with training in both lesion groups. The data thus suggest that the entire HPC axis is involved in acquisition of spatial information.

Section snippets

Acknowledgements

We would like to thank Matthew Shapiro and Klaudiusz Weiss for useful comments on a previous version of this paper. This research has been supported by an NSERC grant awarded to R.J. McDonald.

References (19)

R.J. McDonald et al.
Parallel information processing in the water maze: evidence for independent memory systems involving dorsal striatum and hippocampus
Behav. Neural Biol.
(1994)
J. O'Keefe et al.
Fornix lesions selectively abolish place learning in the rat
Exp. Neurol.
(1975)
B. Poucet et al.
Effects of short-lasting inactivations of the ventral hippocampus and medial septum on long-term and short-term acquisition of spatial information in rats
Behav. Brain Res.
(1991)
D.G. Amaral et al.
Hippocampal formation
R.N. Auer et al.
Neurobehavioral deficit due to ischemic brain damage limited to half of the CA1 sector of the hippocampus
J. Neurosci.
(1989)
D.M. Bannerman et al.
Double dissociation of function within the hippocampus: spatial memory and hyponeophagia
Behav. Neurosci.
(2002)
D.M. Bannerman et al.
Double dissociation of function within hippocampus: a comparison of dorsal, ventral, and complete hippocampal cytotoxic lesions
Behav. Neurosci.
(1999)
L. de Hoz et al.
Retrograde amnesia and hippocampal damage: recovery of an apparently lost memory
Soc. Neurosci. Abstr.
(2001)
L. de Hoz et al.
Rats with a small percentage of hippocampus spared temporally can learn a reference memory task in the water maze
Soc. Neurosci. Abstr.
(1999)

There are more references available in the full text version of this article.

Cited by (101)

Internal-state-dependent control of feeding behavior via hippocampal ghrelin signaling
2024, Neuron
Hunger is an internal state that not only invigorates feeding but also acts as a contextual cue for higher-order control of anticipatory feeding-related behavior. The ventral hippocampus is crucial for differentiating optimal behavior across contexts, but how internal contexts such as hunger influence hippocampal circuitry is unknown. In this study, we investigated the role of the ventral hippocampus during feeding behavior across different states of hunger in mice. We found that activity of a unique subpopulation of neurons that project to the nucleus accumbens (vS-NAc neurons) increased when animals investigated food, and this activity inhibited the transition to begin eating. Increases in the level of the peripheral hunger hormone ghrelin reduced vS-NAc activity during this anticipatory phase of feeding via ghrelin-receptor-dependent increases in postsynaptic inhibition and promoted the initiation of eating. Together, these experiments define a ghrelin-sensitive hippocampal circuit that informs the decision to eat based on internal state.
Cell Proliferation and Cell Death Levels in the Dentate Gyrus Correlate with Home Range Size Among Adult Male Meadow Voles
2023, Neuroscience
Neurogenesis occurs throughout adulthood within the dentate gyrus, and evidence indicates that these new neurons play a critical role in both spatial and social memory. However, a vast majority of past research on adult neurogenesis has involved experiments with captive mice and rats, making the generalizability of results to natural settings questionable. We assessed the connection between adult neurogenesis and memory by measuring the home range size of wild-caught, free-ranging meadow voles (Microtus pennsylvanicus). Adult male voles (n = 18) were captured, fitted with radio collars, and released back into their natural habitat, where each vole’s home range was assessed using 40 radio-telemetry fixes over the course of 5 evenings. Voles were then recaptured, and brain tissue was collected. Cellular markers of cell proliferation (pHisH3, Ki67), neurogenesis (DCX), and pyknosis were labeled on histological sections and then quantified using either fluorescent or light microscopy. Voles with larger home ranges had significantly higher pHisH3+ cell densities within the granule cell layer and subgranular zone (GCL + SGZ) of the dentate gyrus and higher Ki67+ cell densities in the dorsal GCL + SGZ. Voles with larger ranges also had significantly higher pyknotic cell densities in the entire GCL + SGZ and in the dorsal GCL + SGZ. These results support the hypothesis that cell proliferation and cell death within the hippocampus are involved with spatial memory formation. However, a marker of neurogenesis (DCX+) was not correlated with range size, suggesting that there may be selective cellular turnover in the dentate gyrus when a vole is ranging through its environment.
Consolidation of cellular memory representations in superficial neocortex
2023, iScience
Systems-level memory consolidation, a key concept in memory research, involves the conversion of memories that depend on the hippocampus for their formation into efficient hippocampus-independent forms, presumably encoded by cortico-cortical connections. Yet, little is understood about the nature of consolidated neural codes at the cellular ensemble level. Mice require an intact hippocampus for “virtual” spatial learning and to develop neocortical representations of the corresponding experiences. We find that, whereas a novel virtual environment is neither learned nor represented in superficial cortex following severe damage to hippocampus, pre-operatively learned memories and their corresponding sparse and widespread neural ensemble representations in cortical layers II–III are preserved, a sine qua non of memory consolidation. These findings provide a new window for future study of the cellular mechanisms of memory consolidation.
Ventral hippocampus-lateral septum circuitry promotes foraging-related memory
2022, Cell Reports
Remembering the location of a food or water source is essential for survival. Here, we reveal that spatial memory for food location is reflected in ventral hippocampus (HPCv) neuron activity and is impaired by HPCv lesion. HPCv mediation of foraging-related memory involves communication to the lateral septum (LS), as either reversible or chronic disconnection of HPCv-to-LS signaling impairs spatial memory retention for food or water location. This neural pathway selectively encodes appetitive spatial memory, as HPCv-LS disconnection does not affect spatial memory for escape location in a negative reinforcement procedure, food intake, or social and olfactory-based appetitive learning. Neural pathway tracing and functional mapping analyses reveal that LS neurons recruited during the appetitive spatial memory procedure are primarily GABAergic neurons that project to the lateral hypothalamus. Collective results emphasize that the neural substrates controlling spatial memory are outcome specific based on reinforcer modality.
Unpredictable mealtimes rather than social jetlag affects acquisition and retention of hippocampal dependent memory
2022, Behavioural Processes
Some degree of circadian rhythm disruption is hard to avoid in today’s society. Along, with many other deleterious effects, circadian rhythm disruption impairs memory. One way to study this is to expose rats to daylengths that are outside the range of entrainment. As a result, circadian processes and behaviors occur during phases of the light dark cycle in which they typically would not. Even brief exposures to these day lengths can impair hippocampal dependent memory. In a recent report, we created an unentrainable light dark cycle that was intended to resemble aspects of social jetlag. As predictable mealtime impacts circadian entrainment, in that report, we also created an unpredictable meal schedule with the idea that failure to entrain to a meal might afford a disadvantage in some instances. Both of these manipulations impaired retention in a spatial water plus-maze task. Using the same manipulations, the present study investigated their effects on acquisition in distributed and massed spatial water plus-maze paradigms. As in other reports with unentrainable daylengths, acquisition was not affected by our lighting manipulation. Conversely, in accordance with our past report, unpredictable mealtimes had a harmful effect on hippocampal dependent memory. Notably, impaired acquisition in the distributed version, and impaired retention in the massed version. In tandem, these data suggest that failure to consolidate or retrieve the information is the likely culprit. The unpredictable mealtime manipulation offers a unique opportunity to study the effects of circadian entrainment on memory.
Behaviour-driven Arc expression is greater in dorsal than ventral CA1 regardless of task or sex differences
2022, Behavioural Brain Research
Citation Excerpt :
However, it remains unclear whether cellular recruitment probability across the hippocampal long axis depends on task or is invariant to changes in cognitive-behavioural demands. To address this question, we quantified cellular recruitment with the IEG Arc across the longitudinal axis of CA1 in female and male rats performing the MWT or context fear discrimination (CFD), which are both impaired following hippocampal damage [17–22]. We focused our behavioral measures on the MWT and CFD due to: 1) their popularity as behavioral assays of long-term memory; 2) differences in extra-hippocampal circuit mechanisms that support the expression of spatial and fear memory in the MWT and CFD [23–25]; 3) to extend our previous results on Arc mRNA expression in the MWT across sexes [11].
Evidence from genetic, behavioural, anatomical, and physiological study suggests that the hippocampus functionally differs across its longitudinal (dorsoventral or septotemporal) axis. Although, how to best characterize functional and representational differences in the hippocampus across its long axis remains unclear. While some suggest that the hippocampus can be divided into dorsal and ventral subregions that support distinct cognitive functions, others posit that these regions vary in their granularity of representation, wherein spatial-temporal resolution decreases in the ventral (temporal) direction. Importantly, the cognitive and granular hypotheses also make distinct predictions on cellular recruitment dynamics under conditions when animals perform tasks with qualitatively different cognitive-behavioural demands. One interpretation of the cognitive function account implies that dorsal and ventral cellular recruitment differs depending on relevant behavioural demands, while the granularity account suggests similar recruitment dynamics regardless of the nature of the task performed. Here, we quantified cellular recruitment with the immediate early gene (IEG) Arc across the entire longitudinal CA1 axis in female and male rats performing spatial- and fear-guided memory tasks. Our results show that recruitment is greater in dorsal than ventral CA1 regardless of task or sex, and thus support a granular view of hippocampal function across the long axis. We further discuss how future experiments might determine the relative contributions of cognitive function and granularity of representation to neuronal activity dynamics in hippocampal circuits.

View all citing articles on Scopus

View full text

Both dorsal and ventral hippocampus contribute to spatial learning in Long–Evans rats

Abstract

Section snippets

Acknowledgements

Behav. Neural Biol.

Exp. Neurol.

Behav. Brain Res.

Hippocampal formation

Neurobehavioral deficit due to ischemic brain damage limited to half of the CA1 sector of the hippocampus

J. Neurosci.

Double dissociation of function within the hippocampus: spatial memory and hyponeophagia

Behav. Neurosci.

Double dissociation of function within hippocampus: a comparison of dorsal, ventral, and complete hippocampal cytotoxic lesions

Behav. Neurosci.

Retrograde amnesia and hippocampal damage: recovery of an apparently lost memory

Soc. Neurosci. Abstr.

Rats with a small percentage of hippocampus spared temporally can learn a reference memory task in the water maze

Soc. Neurosci. Abstr.