Directionally selective mnemonic properties of neurons in the lateral dorsal nucleus of the thalamus of rats

Abstract

The hippocampal formation has been extensively studied for its special role in visual spatial learning and navigation. To ascertain the nature of the associations made, or computations performed, by hippocampus, it is important to delineate the functional contributions of its afferents. Therefore, single units were recorded in the lateral dorsal nucleus of the thalamus (LDN) as rats performed multiple trials on a radial maze. Many LDN neurons selectively discharged when an animal's head was aligned along particular directions in space, irrespective of its location in the test room. These direction-sensitive cells were localized to the dorsal aspect of the caudal two-thirds of the LDN, the site of innervation by retinal recipient pretectal and intermediate/deep-layer superior colliculus cells (Thompson and Robertson, 1987b). The directional specificity and preference of LDN cells were disrupted if rats were placed on the maze in darkness. If the room light was then turned on, the original preference was restored. If the light was again turned off, directional firing was maintained briefly. Normal directional firing lasted about 2-3 min. After this time, the directional preference (but not specificity) appeared to "rotate" systematically in either the clockwise or counterclockwise direction. The duration of normal directional discharge patterns in darkness could be extended to 30 min by varying the behavior of the animal. LDN cells required visual input to initialize reliable directional firing. After the rat viewed the environment, directional specificity was maintained in the absence of visual cues. Maximal directional firing was achieved only when the rat viewed the entire test room, and not just the scene associated with the directional preference of the cell. Thus, contextual information seems important. Also, a significant correlation was found between directional specificity and errors made on the maze during acquisition of the task. It was concluded that the LDN may pass on to the hippocampal formation directional information that is not merely a reflection of current sensory input. As such, the LDN may serve an important integrative function for limbic spatial learning systems.

Path integration in mammals

“…When a rat reenters a familiar test environment, it has to be exposed to its visual surroundings in order to reset its head direction system. If the lights are then turned off, the cells maintain their direction specific firing for a given time span; their activity then starts drifting, as expected, if we assume that the updating process occurred through the angular components of self-motion cues (Mizumori and Williams, 1993). Likewise, in a cylindrical test apparatus with a single cue card, the head direction cells may maintain their directional preference after the removal of the cue card, but this preference drifts slowly over time.…”

Is there a geometric module for spatial orientation? Insights from a rodent navigation model.

“…Upon the entry to a familiar environment, head direction ⌽ is initialized with value ⌽ vis by setting ␣ hd ϭ 1. While our model of the head direction network (see Equations A8 and A11) is algorithmic (Franz, Schölkopf, Mallot, & Bülthoff, 1998), rather than neuronal, it captures the fact that head direction cells are anchored to visual cues of the environment (Mizumori & Williams, 1993).…”

A Continuous Attractor Network Model Without Recurrent Excitation: Maintenance and Integration in the Head Direction Cell System

“…HD cells were first electrophysiologically recorded in the rat postsubiculum (PoSC) (Ranck, 1984;Taube et al, 1990a), and then found in numerous other structures including the laterodorsal thalamic nucleus (Mizumori and Williams, 1993), the dorsal striatum (Wiener, 1993), the retrosplenial cortex (Chen et al, 1994), the anterodorsal thalamic nucleus (ADN) (Taube, 1995;Blair and Sharp, 1995), the lateral mammillary nucleus (LMN) (Stackman and Taube, 1998), and the dorsal tegmental nucleus (DTN) .…”