Lesions of the rat postsubiculum impair performance on spatial tasks

doi:10.1016/0163-1047(92)90629-I

Behavioral and Neural Biology

Volume 57, Issue 2, March 1992, Pages 131-143

https://doi.org/10.1016/0163-1047(92)90629-I Get rights and content

Previous studies have identified a population of neurons in the postsubiculum that discharge as a function of the rat's head direction in the horizontal plane (Taube, Muller, & Ranck, 1990a). To assess the contribution of these cells in spatial learning, Long—Evans rats were tested in a variety of spatial and nonspatial tasks following bilateral electrolytic or neurotoxic lesions of the postsubiculum. Compared to unlesioned control animals, lesioned animals were impaired on two spatial tasks, a radial eight-arm maze task and a Morris water task, although the performance scores of both lesion groups improved over the course of behavioral testing. In contrast, lesioned animals were unimpaired on two nonspatial tasks, a cued version of the water maze task and a conditioned taste-aversion, paradigm. In addition, lesioned animals showed transient hyperactivity in an open-field activity test. These results support the concept that neurons in the postsubiculum are part of a neural network involved in the processing of spatial information.

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Cited by (104)

A Thalamic Reticular Circuit for Head Direction Cell Tuning and Spatial Navigation
2020, Cell Reports
As we navigate in space, external landmarks and internal information guide our movement. Circuit and synaptic mechanisms that integrate these cues with head-direction (HD) signals remain, however, unclear. We identify an excitatory synaptic projection from the presubiculum (PreS) and the multisensory-associative retrosplenial cortex (RSC) to the anterodorsal thalamic reticular nucleus (TRN), so far classically implied in gating sensory information flow. In vitro, projections to TRN involve AMPA/NMDA-type glutamate receptors that initiate TRN cell burst discharge and feedforward inhibition of anterior thalamic nuclei. In vivo, chemogenetic anterodorsal TRN inhibition modulates PreS/RSC-induced anterior thalamic firing dynamics, broadens the tuning of thalamic HD cells, and leads to preferential use of allo- over egocentric search strategies in the Morris water maze. TRN-dependent thalamic inhibition is thus an integral part of limbic navigational circuits wherein it coordinates external sensory and internal HD signals to regulate the choice of search strategies during spatial navigation.
Retrosplenial cortex and its role in cue-specific learning and memory
2019, Neuroscience and Biobehavioral Reviews
The retrosplenial cortex (RSC) contributes to spatial navigation, as well as contextual learning and memory. However, a growing body of research suggests that the RSC also contributes to learning and memory for discrete cues, such as auditory or visual stimuli. In this review, we summarize and assess the Pavlovian and instrumental conditioning experiments that have examined the role of the RSC in cue-specific learning and memory. We use the term cue-specific to refer to these putatively non-spatial conditioning paradigms that involve discrete cues. Although these paradigms emphasize behavior related to cue presentations, we note that cue-specific learning and memory always takes place against a background of contextual stimuli. We review multiple ways by which contexts can influence responding to discrete cues and suggest that RSC contributions to cue-specific learning and memory are intimately tied to contextual learning and memory. Indeed, although the RSC is involved in several forms of cue-specific learning and memory, we suggest that many of these can be linked to processing of contextual stimuli.
A new perspective on the head direction cell system and spatial behavior
2019, Neuroscience and Biobehavioral Reviews
Citation Excerpt :
Lesions of the cortical regions in which HD cells are found yield mixed effects on tasks which depend on a sense of direction. For example, Taube et al. (1992) found that rats with lesions of the postsubiculum were impaired in performance of a radial arm maze and a Morris water maze, but in both instances performance of lesioned animals improved with training. Kesner and Giles (1998) found that rats with combined post- and parasubiculum damage were impaired in remembering which maze arm they’d recently visited on a radial maze, and similar lesions also resulted in deficits in a Morris water maze and a T-maze alternation task (Liu et al., 2001; Bett et al., 2012).
The head direction cell system is an interconnected set of brain structures containing neurons whose firing is directionally tuned. The robust representation of allocentric direction by head direction cells suggests that they provide a neural compass for the animal. However, evidence linking head direction cells and spatial behavior has been mixed. Whereas damage to the hippocampus yields profound deficits in a range of spatial tasks, lesions to the head direction cell system often yield milder impairments in spatial behavior. In addition, correlational approaches have shown a correspondence between head direction cells and spatial behavior in some tasks, but not others. These mixed effects may be explained in part by a new view of the head direction cell system arising from recent demonstrations of at least two types of head direction cells: ‘traditional’ cells, and a second class of ‘sensory’ cells driven by polarising features of an environment. The recognition of different kinds of head direction cells now allows a nuanced assessment of this system’s role in guiding navigation.
En route to delineating hippocampal roles in spatial learning
2019, Behavioural Brain Research
Citation Excerpt :
Interestingly, however, it is worth noting that the platform location was eventually learned by both of these lesion groups after additional training, broadly mirroring the performance observed by rats with hippocampal damage in the current experiment (Experiment 1: Active Swim condition) and in [4]. Other candidate brain regions spared in the current experiments and identified as playing a key role in the MWM task include the anterior thalamic nuclei (for acquisition deficits see e.g. [62,63]; see also [64] for a review), the subicular complex [4,65], presubiculum and parasubiculum [66,67], and some neocortical regions [e.g. 68, 69]. Experiment 4 tested the rats used in Experiments 1 and 3 with the aim of identifying a previously reported hippocampal-induced deficit in learning based on environmental shape [20–22].
The precise role played by the hippocampus in spatial learning tasks, such as the Morris Water Maze (MWM), is not fully understood. One theory is that the hippocampus is not required for ‘knowing where’ but rather is crucial in ‘getting there’. To explore this idea in the MWM, we manipulated ‘getting there’ variables, such as passive transport or active swimming towards the hidden platform, in rats with and without hippocampal lesions.
Our results suggested that for intact rats, self-motion cues enroute to the hidden goal were a necessary component for ‘place learning’ to progress. Specifically, intact rats could not learn the hidden goal location, when passively transported to it, despite extensive training. However, when rats were either given hippocampal lesions, or placed in a light-tight box during transportation to the hidden goal, passive-placement spatial learning was facilitated. In a subsequent experiment, the ‘getting there’ component of place navigation was simplified, via the placement of two overhead landmarks, one of which served as a beacon. When ‘getting there’ was made easier in this way, hippocampal lesions did not induce deficits in ‘knowing where’ the goal was. In fact, similar to the facilitation observed in passive-placement spatial learning, hippocampal lesions improved landmark learning relative to controls. Finally, demonstrating that our lesions were sufficiently deleterious, hippocampal-lesioned rats were impaired, as predicted, in an environmental-boundary based learning task. We interpret these results in terms of competition between multiple memory systems, and the importance of self-generated motion cues in hippocampal spatial mapping.
Lesions within the head direction system reduce retrosplenial c-fos expression but do not impair performance on a radial-arm maze task
2018, Behavioural Brain Research
The lateral mammillary nuclei are a central structure within the head direction system yet there is still relatively little known about how these nuclei contribute to spatial performance. In the present study, rats with selective neurotoxic lesions of the lateral mammillary nuclei were tested on a working memory task in a radial-arm maze. This task requires animals to distinguish between eight radially-oriented arms and remember which arms they have entered within a session. Even though it might have been predicted that this task would heavily tax the head direction system, the lesion rats performed equivalently to their surgical controls on this task; no deficit emerged even when the task was made more difficult by rotating the maze mid-way through testing in order to reduce reliance on intramaze cues. Rats were subsequently tested in the dark to increase the use of internally generated direction cues but the lesion rats remained unimpaired. In contrast, the lateral mammillary nuclei lesions were found to decrease retrosplenial c-Fos levels. These results would suggest that the head direction system is not required for the acquisition of the standard radial-arm maze task. It would also suggest that small decreases in retrosplenial c-Fos are not sufficient to produce behavioural impairments.
String-pulling for food by the rat: Assessment of movement, topography and kinematics of a bilaterally skilled forelimb act
2018, Learning and Motivation
Citation Excerpt :
Other research supports a role for a directional vector or polar coordinate representational system in accounting for a range of spatial behaviors (Blodgett, McCutchan, & Mathews, 1949; Hamilton, Akers, Weisend, & Sutherland, 2007; Skinner et al., 2003). This directional vector is further supported by the discovery of head direction cells in a network of brain structures that are tuned to rat’s directional heading (Calton et al., 2003; Stackman, Clark, & Taube, 2002; Taube, Muller, & Ranck, 1990; Taube, Kesslak, & Cotman, 1992) and that CA1 cell activity is tuned to spatial distance (Kjelstrup et al., 2008). Considering the view that the manipulatory scale neural system evolved from brain structures that mediate ambulatory scale movement (Grillner & Wallen, 1985; Iwaniuk & Whishaw, 2000; Karl & Whishaw, 2013), it is possible a directional vector is used to encode manipulatory scale movement during string-pulling behavior.
A variety of behavioral tests have been developed to assess skilled forelimb function in the rat, including tests that assess use of a single limb in reaching for food and placing it in the mouth for eating. The present study describes bilateral hand use in string-pulling to obtain a food reward. The movement consists of alternating forelimb movements in which a limb is advanced to grasp a string and withdraw it toward the body in order to retrieve a food reward. The movements of aim, advance, grasp, pull and push are associated with hand shape changes including collect, overgrasp, grasp and release. The topography and kinematics of limb and hand movement are assessed by digitizing methods that derive trajectory, distance, and velocity measures. The task is acquired by a rat within a few days of training, features few missed grasps, shows improvements with practice, and yields dozens of independent reaches by each hand in a single test session. The present analysis provides simple methods for describing each independent forelimb and hand movement and its topographic and kinematic properties. The similarities between string-pulling and other rat forelimb movements are discussed in relation to the idea that rat forelimb movements are conserved in tasks such as string-pulling, walking, reaching for food and grid walking. The task is also discussed with respect to its potential to investigate neural and cognitive bases of fine motor control.

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¹: This research was supported by NIA Grants AG00096 and AG07918 and by NIMH Grant MH19691. The authors thank Todd Herbst, Kamran Kamali, and Carol Woods for help in performing the experiments.

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Lesions of the rat postsubiculum impair performance on spatial tasks

Behavioural Brain Research

Behavioral Brain Research

Physiology and Behavior

Behavioural Brain Research

Brain Research Bulletin

Behavioural Brain Research

Progress in Neurobiology

Single-unit analysis of different hippocampal cell types during classical conditioning of rabbit nictitating membrane response

Journal of Neurophysiology

Commissural connections of the hippocampal region in the rat, with special reference to their mode of termination

Journal of Comparative Neurology

Muscimol injections in the medial septum impair spatial learning

Brain Research

Acquisition of a complex place task in rats with selective ibotenate lesions of hippocampal formation: Combined lesions of subiculum and entorhinal cortex versus hippocampus

Behavioral Neuroscience

Hippocampal representation in place learning

Journal of Neuroscience

Acquisition of concurrent conditional discriminations in rats with ibotenate lesions of hippocampus and of subiculum

Psychobiology

On the role of hippocampal connections in the performance of place and cue tasks: Comparisons with damage to hippocampus

Behavioral Neuroscience

Intrinsic projections of the retrohippocampal region in the rat brain. I. The subicular complex

Journal of Comparative Neurology