Behavioural Brain Research 155 (2004) 97–108 Testing the importance of the retrosplenial guidance system: effects of different sized retrosplenial cortex lesions on heading direction and spatial working memory Seralynne D. Vann , John P. Aggleton School of Psychology, Cardiff University, Park Place, PO Box 901, Cardiff CF10 3YG, UK Received 13 February 2004; received in revised form 6 April 2004; accepted 6 April 2004 Available online 11 May 2004 Abstract The present study: (1) tested the importance of the retrosplenial cortex for learning a specific heading direction and distance and, (2) determined if lesion size could explain apparent inconsistencies in the results of different research groups. Dark agouti rats received either ‘complete’ cytotoxic retrosplenial cortex lesions or ‘standard’ lesions, the latter sparing the caudal retrosplenial cortex. Animals were first tested on two versions of a “landmark” task in a water maze. In condition 1 animals could use both heading direction and allocentric position, while in condition 2 only heading direction was effective. In condition 1, animals with complete retrosplenial lesions were impaired by the end of training, their profile of performance being consistent with a failure to use allocentric position information. When the water maze task changed (condition 2) so that allocentric cues became redundant, the animals with complete retrosplenial lesions were able to head in the appropriate direction although they showed longer swim paths. Subsequent testing in the radial-arm maze provided more evidence that retrosplenial lesions can disrupt the use of distal (allocentric) room cues. The impairments seen with retrosplenial lesions were often mild but throughout the study performance of rats with ‘complete’ lesions was more disrupted than those with ‘standard’ lesions, who often did not differ from the controls. These findings show that lesion size is a critical factor and may explain why some studies have failed to find comparable deficits after retrosplenial cortex lesions. © 2004 Elsevier B.V. All rights reserved. Keywords: Heading direction; Radial-arm maze; Rats; Retrosplenial cortex; Spatial memory; Water maze 1. Introduction The rodent retrosplenial cortex (area 29) is thought to be important for spatial learning and memory. Evidence comes from the lesion induced deficits found for both reference and working memory tests in the water maze [10,24,27,29], and for tests of spatial working memory in the radial-arm maze [6,27,29]. The present study had two interlinked goals. The first was to identify more precisely the nature of these spatial impairments. For this, attention focused on the hypothesis that the retrosplenial cortex provides directional guidance information [12]. The second goal arises from the large variations found between studies in the severity of spatial impairment associated with retrosplenial lesions. By Corresponding author. Tel.: +44-29-2087-6253; fax: +44-29-2087-4858. E-mail address: vannsd@cardiff.ac.uk (S.D. Vann). comparing lesions of different sizes in the same study we provide the first direct test of the importance of this factor. The retrosplenial cortex is densely connected with the anterior thalamus and laterodorsal thalamus [26], regions thought to be important for directional learning [25,32]. Fur- thermore, like the anterodorsal and laterodorsal thalamic nu- clei, the retrosplenial cortex contains head direction cells [4,5]. For these reasons the first experiment tested the ability to head in a fixed direction and distance from a cue (land- mark) placed within a water maze [21]. Two task variants were used. In the first condition rats could use not only the direction of the platform from the landmark but also its ab- solute position [21], which changed from session to session. In the second condition the landmark and, hence the plat- form, changed position on every trial, so providing a purer test of the ability to learn a specific trajectory and distance. In further tests we also examined the nature of the retros- plenial lesion deficit found in the radial-arm maze. Previous studies have indicated that this deficit may reflect a reduced 0166-4328/$ – see front matter © 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.bbr.2004.04.005