Dysgranular retrosplenial cortex lesions in rats disrupt cross-modal object recognition

Abstract

The retrosplenial cortex supports navigation, with one role thought to be the integration of different spatial cue types. This hypothesis was extended by examining the integration of nonspatial cues. Rats with lesions in either the dysgranular subregion of retrosplenial cortex (area 30) or lesions in both the granular and dysgranular subregions (areas 29 and 30) were tested on cross-modal object recognition (Experiment 1). In these tests, rats used different sensory modalities when exploring and subsequently recognizing the same test objects. The objects were first presented either in the dark, i.e., giving tactile and olfactory cues, or in the light behind a clear Perspex barrier, i.e., giving visual cues. Animals were then tested with either constant combinations of sample and test conditions (light to light, dark to dark), or changed "cross-modal" combinations (light to dark, dark to light). In Experiment 2, visual object recognition was tested without Perspex barriers, but using objects that could not be distinguished in the dark. The dysgranular retrosplenial cortex lesions selectively impaired cross-modal recognition when cue conditions switched from dark to light between initial sampling and subsequent object recognition, but no impairment was seen when the cue conditions remained constant, whether dark or light. The combined (areas 29 and 30) lesioned rats also failed the dark to light cross-modal problem but this impairment was less selective. The present findings suggest a role for the dysgranular retrosplenial cortex in mediating the integration of information across multiple cue types, a role that potentially applies to both spatial and nonspatial domains.

Figure 1.

Schematic diagram showing the four different trial types in the cross-modal object recognition task. Left images in each pair show the sample phase, while right images show the test phase. The different symbols represent different objects. In any light-phase condition, lights were turned on and barriers were placed between the rat and the object to prevent tactile exploration; during dark phases these barriers were removed but the lights were turned off. Light–light and dark–dark trials do not require a cross-modal switch, while dark–light and light–dark trials do.

Figure 2.

(A) Series of coronal sections showing the cases with the largest (light gray) and smallest (dark gray) lesions in the dysgranular retrosplenial (RSdysg) lesion cohort. The numbers correspond to the distance behind bregma in millimeters (Paxinos and Watson 2007). (B) Coronal NeuN sections showing the retrosplenial cortex (both hemispheres) from a sham surgery control rat (top), and a representative rat from the RSdysg lesion group (bottom). (cb) Cingulum bundle; (dys) dysgranular retrosplenial cortex; (gran) granular retrosplenial cortex.

Figure 3.

(A) Series of coronal sections showing the cases with the largest (light gray) and smallest (dark gray) lesions in the combined dysgranular and granular retrosplenial (RScomb) lesion cohort. The numbers correspond to the distance behind bregma in millimeters (Paxinos and Watson 2007). (B) Coronal NeuN sections showing the retrosplenial cortex (both hemispheres) from a sham surgery control rat (top), and a representative rat from the RScomb lesion group (bottom). (cb) Cingulum bundle; (dys) dysgranular retrosplenial cortex; (gran) granular retrosplenial cortex.

Figure 4.

Cohort 1: mean recognition (D2) scores seen at test for the four trial types. Two trial types (dark–dark and light–light) did not require a switch between cue modalities as the same cue types were available at both sample and test. The other two trial types were designed to force the rats to switch between different cue modalities between the sample and the test phases (light–dark and dark–light). Both the Sham 1 and RSdysg groups performed above chance levels on the light–light and dark–dark trials, but only the Sham1 animals were above chance for the dark–light switch. Error bars, SEM.

Figure 5.

Cohort 2: Mean recognition (D2) scores achieved on dark–dark, light–light, and dark–light trials. While both Sham2 and RScomb rats spent significantly more time with the novel object in dark–dark trials, only the Sham2 rats performed above chance levels in the light–light and dark–light trials on this task. Error bars, SEM.

Figure 6.

Examples of objects used during the visual object recognition task. Objects were indistinguishable with regard to shape, material, texture, and smell, as determined by the failure of the rats to recognize these objects in the dark. However, these same objects differed in color and pattern, and so could potentially be visually distinguished when subsequently tested in the light. Scale bar, 5 cm.

Figure 7.

Cohort 1: mean recognition (D2) scores on the dark–dark and light–light sessions of the object recognition task without barriers. Any objects that could be recognized in the dark were removed from the analysis. Consequently, neither the Sham1 nor the RSdysg group was above chance discrimination on the dark–dark trials. On the light–light trials, where the same objects are used as in the dark–dark trials, both groups spent significantly more time with the novel object. Error bars, SEM.

Figure 8.

Cohort 2: mean recognition (D2) scores of the Sham2 and RScomb groups on the dark–dark and light–light sessions of the object recognition task without barriers. Any objects that had been recognized in the dark were removed from the analysis. Consequently, neither group was above chance on the dark–dark trials. On the light–light trials, where the same objects are used as in the dark–dark trials, both groups spent significantly more time with the novel object. Error bars, SEM.