Head Direction Cell Instability in the Anterior Dorsal Thalamus after Lesions of the Interpeduncular Nucleus

Abstract

Previous research has identified a population of cells throughout the limbic system that discharge as a function of the animal's head direction (HD). Altering normal motor cues can alter the HD cell responses and disrupt the updating of their preferred firing directions, thus suggesting that motor cues contribute to processing the HD signal. A pathway that conveys motor information may stem from the interpeduncular nucleus (IPN), a brain region that has reciprocal connections with HD cell circuitry. To test this hypothesis, we produced electrolytic or neurotoxic lesions of the IPN and recorded HD cells in the anterior dorsal thalamus (ADN) of rats. Direction-specific firing remained present in the ADN after lesions of the IPN, but measures of HD cell properties showed that cells had reduced peak firing rates, large directional firing ranges, and firing that predicted the animal's future heading more than in intact controls. Furthermore, preferred firing directions were moderately less influenced by rotation of a salient visual landmark. Finally, the preferred directions of cells in lesioned rats exhibited large shifts when the animals foraged for scattered food pellets in a darkened environment and when locomoting from a familiar environment to a novel one. We propose that the IPN contributes motor information about the animal's movements to the HD cell circuitry. Furthermore, these results suggest that the IPN plays a broad role in the discharge properties and stability of directionspecific activity in the HD cell circuit.

Intact landmark control and angular path integration by head direction cells in the anterodorsal thalamus after lesions of the medial entorhinal cortex

“…To start the test, the room lights were turned off and the rat was gently placed in the cylinder and allowed to forage for food pellets for 8 min. Similar to previous studies (Good-ridge et al, 1998; Golob and Taube, 1999; Clark et al, 2009, 2010), animals were not disoriented prior to being placed in the cylinder for dark testing. To track the HD of the rat, the red and green LEDs remained on during the dark session.…”

“…We also measured preferred direction stability by constructing HD × time plots for each HD cell recorded in control and lesion groups (Clark et al, 2009, 2010; Yoder and Taube, 2009). Figure 8A shows representative HD × time plots for individual HD cells recorded in each group.…”

Decoding signal processing in thalamo-hippocampal circuitry: implications for theories of memory and spatial processing

“…A small proportion of neurons modulated by linear velocity are found in the habenula and the interpeduncular nucleus (Sharp et al, 2006). This hypothesis is supported by the finding that damage to the interpeduncular nucleus disrupts anterodorsal head-direction stability (Clark et al, 2009). A parallel explanation for the effect of theta on the tuning curve of the head-direction cells is that Fig.…”

The neural correlates of navigation beyond the hippocampus

“…Furthermore, both structures contain cells that correlate with the animal's running speed (Sharp et al, 2006). Lesions of the IPN decreased the peak firing rate and increased the directional firing range of ADN HD cells, but did not abolish the HD signal (Clark et al, 2009); and as with the studies that manipulated brainstem nuclei, HD cells in IPN-lesioned animals had larger shifts in their preferred firing direction when navigation relied on internal cues for maintaining orientation. At present, the effects of lesions to these brainstem sites on either place cell or grid cell firing is not known.…”