Origins of landmark encoding in the brain

Abstract

The ability to perceive one's position and directional heading relative to landmarks is necessary for successful navigation within an environment. Recent studies have shown that the visual system dominantly controls the neural representations of directional heading and location when familiar visual cues are available, and several neural circuits, or streams, have been proposed to be crucial for visual information processing. Here, we summarize the evidence that the dorsal presubiculum (also known as the postsubiculum) is critically important for the direct transfer of visual landmark information to spatial signals within the limbic system.

Figure 1

Landmark control of spatial signals. Each panel displays the response of a different spatial cell type in rats to a 90° rotation of the salient visual landmark cue – a white sheet of cardboard attached along the inside wall of the enclosure (represented by a red arc in each panel). (A) The directional tuning curve of an anterior thalamic head direction (HD) cell, (B) the place field of a hippocampal place cell, and (C) the firing pattern of an entorhinal cortical grid cell show angular shifts of the spatial signal that approximate the amount of cue card rotation. Panel A is based on polar coordinates from [10]; B and C are based on data in [18] and [118], respectively. Data shown in plots B and C have been smoothed to improve presentation. Peak firing rates are indicated for each plot.

Figure 2

Hypothesized landmark processing circuit and the visual stream pathways in rodents. A) Lateral and para-sagittal views of the rat brain showing the three major visual processing streams: dorsal (red arrows), ventral (purple arrows) and tectal (orange arrows). B) The head direction (HD) cell signal originates within the reciprocal connections between the dorsal tegmental nucleus and lateral mammillary nuclei (dashed red lines), and is generated from vestibular, proprioceptive, and motor information arriving from several subcortical areas. From the LMN, the HD signal projects rostrally to the anterodorsal thalamus, which projects to the postsubiculum (PoS). Current evidence suggests that landmark information from visual cortical areas could be conveyed to the HD cell circuit via several distinct routes, including the dorsal (red), ventral (purple), and tectal (orange) visual streams. Black arrows depict the major visual cortical projections. Abbreviations: ADN: anterodorsal thalamus, EC: entorhinal cortex, Hpc: hippocampus, LDN: lateral dorsal thalamus; LMN, lateral mammillary nuclei; Par: parietal cortex, PoR: postrhinal cortex, PoS: postsubiculum, Rsp: retrosplenial cortex, SC: superior colliculus, Vis: visual cortex.

Figure 3

Head direction (HD) cell and place cell responses to 90° cue rotation following lesions of various brain structures in rats. All HD cells are shown with dots outside the circle and were recorded from the anterodorsal thalamic nucleus (black dots) or the lateral mammillary nuclei (green dots). All place cells are shown with blue dots inside the circle. For all plots, each point represents the shift (in 6° bins) of a single cell’s preferred firing direction or place field that occurred following a 90° rotation of the cue card, with positive shifts corresponding to the same direction of cue card rotation, regardless of whether the cue rotation was clockwise (CW) or counter-clockwise (CCW). For simultaneously recorded cells, the average shift of these cells is depicted; in some cases, these averaged values fell between 6° bins. Arrows in each plot represent the mean vector length of the overall data. For each panel, the right column shows the brain pathways and corresponding areas that were lesioned. Abbreviations and the color scheme used for different visual streams are the same as in Figure 2. A) In control animals, the shifts in the preferred firing directions and place fields were similar to the amount of cue card rotation [13, 18]. The mean vectors for the place and HD cell data overlap; thus, only the mean place cell vector is visible. B) Postsubiculum lesions severely impaired the landmark control of anterodorsal thalamus [13] and mammillary Yoder, R.M. and Taube, J.S., Society for Neuroscience abstract 90.9. 2008] HD cells, as well as hippocampal place cells [18]. C) Within the dorsal visual stream pathway, parietal cortex lesions had no effect on HD [39] and place [40] cells, whereas retrosplenial cortex lesions moderately impaired the landmark control of HD cells [44]. D) In the ventral stream pathway, EC lesions had no effect on the landmark control of anterodorsal thalamus HD cells [60] and only a mild impairment on hippocampal place cells [19]. E) Lesion of visual cortex had a moderate impact on landmark control of place cells [31], whereas a lesion within the tectal stream pathway (within the lateral dorsal thalamus) had little effect on HD cells [65]. F) Within the limbic system, hippocampal lesions had little effect on HD cells in anterodorsal thalamus [35], and anterodorsal thalamus lesions had little effect on place cells in the hippocampus [18]. Hippocampal place cell data from visual cortex, parietal cortex, and EC lesions are based on data published in [31], [40] and [19], respectively, and provided by Bruno Poucet.