Anticipatory Time Intervals of Head-Direction Cells in the Anterior Thalamus of the Rat: Implications for Path Integration in the Head-Direction Circuit

Abstract

Head-direction cells are neurons that signal a rat's directional heading in the horizontal plane. Head-direction cells in the anterior thalamus are anticipatory, so that their firing rate is better correlated with the rat's future head direction than with the present or past head direction. We recorded single-unit activity from head-direction cells in the anterior thalamus of freely moving rats. We measured the time interval by which each individual cell anticipated the rat's future head direction, which we refer to as the cell's anticipatory time interval (ATI). Head-direction cells in the anterior thalamus anticipated the rat's future head direction by an average ATI of approximately 17 ms. However, different anterior thalamic cells consistently anticipated the future head direction by different ATIs ranging between 0 and 50 ms. We found that the ATI of an anterior thalamic head-direction cell was correlated with several parameters of the cell's directional tuning function. First, cells with long ATIs sometimes appeared to have two peaks in their directional tuning function, whereas cells with short ATIs always had only one peak. Second, the ATI of a cell was negatively correlated with the cell's peak firing rate, so that cells with longer ATIs fired at a slower rate than cells with shorter ATIs. Third, a cell's ATI was correlated with the width of its directional tuning function, so that cells with longer ATIs had broader tuning widths than cells with shorter ATIs. These relationships between a cell's ATI and its directional tuning parameters could not be accounted for by artifactual broadening of the tuning function, which occurs for cells that fire in correlation with the future (rather than present) head direction. We found that when the rat's head is turning, the shape of an anterior thalamic head-direction cell's tuning function changes in a systematic way, becoming taller, narrower, and skewed. This systematic change in the shape of the tuning function may be what causes anterior thalamic cells to effectively anticipate the rat's future head direction. We propose a neural circuit mechanism to account for the firing behavior we have observed in our experiments, and we discuss how this circuit might serve as a functional component of a neural system for path integration of the rat's directional heading.

Reconstruction of the postsubiculum head direction signal from neural ensembles

“…These cells have baseline-to-baseline tuning curve widths of 100° (Taube et al, 1990a) and can be modeled as Gaussians with an average standard deviation of 66° (Blair and Sharp, 1995). In rodents, HD cells have been found in postsubiculum (Taube et al, 1990a,b;Sharp, 1996), in the anterior dorsal thalamic nuclei (Blair and Sharp, 1995;Knierim et al, 1995;Taube, 1995;Blair et al, 1997), in the lateral mammillary nuclei (Blair et al, 1998;Stackman and Taube, 1998), as well as the dorsal tegmental nucleus of Gudden (Sharp et al, 2001b), the lateral dorsal nucleus of the thalamus (Mizumori and Williams, 1993), the striatum (Wiener, 1993;Ragozzino et al, 2001), and the retrosplenial cortex (Chen et al, 1994a,b).…”

“…An alternative view presented by Blair and Sharp (Blair et al, 1997;Sharp et al, 2001a) suggested an interaction between the lateral mammillary nucleus and the dorsal tegmental nucleus as the locus of the attractor network. Despite these different perspectives, most theories assume that postsubiculum contains a complete HD signal (Taube et al, 1996;Redish, 1999;Sharp et al, 2001a).…”

Path integration in mammals

“…Cells in the anterior thalamus show anticipatory firing, signaling not the present heading of the rat but rather the heading it will attain up to 40 ms in the future (Blair et al, 1997). This suggests an influence of extrapolated motion and/or efference copy, an interpretation that is supported by the observation that cells in the anterior thalamus fail to fire in their preferred directions if the animal is restrained, and hence unable to execute motor commands (Taube et al, 1996).…”

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

“…This study explored the formation of anticipatory time interval (ATI) and the authors challenged the idea that ATI actively predicts direction by anticipating a future directional signal. ATI is a parameter closely related to the separation angle and is defined as the time displacement for which a cell's firing rate is best correlated with the directional position of the rat's head (Blair and Sharp, 1995;Blair et al, 1997). ATI values differ substantially across the Papez's circuit: however, the presence of ATI does not mean that there is a particular information processing pattern across monosynapticallyconnected regions.…”