Disruption of the head direction cell network impairs the parahippocampal grid cell signal

Abstract

Navigation depends on multiple neural systems that encode the moment-to-moment changes in an animal's direction and location in space.These include head direction (HD) cells representing the orientation of the head and grid cells that fire at multiple locations, forming a repeating hexagonal grid pattern. Computational models hypothesize that generation of the grid cell signal relies upon HD information that ascends to the hippocampal network via the anterior thalamic nuclei (ATN). We inactivated or lesioned the ATN and subsequently recorded single units in the entorhinal cortex and parasubiculum. ATN manipulation significantly disrupted grid and HD cell characteristics while sparing theta rhythmicity in these regions.These results indicate that the HD signal via the ATN is necessary for the generation and function of grid cell activity.

The Head-Direction Signal Plays a Functional Role as a Neural Compass during Navigation

“…Both grid cells and place cells utilize the firing of HD cells in the anterior thalamus, to varying degrees [8,9]. Unlike previous studies that have used inactivation to separate the contributions of theta rhythmicity [41] and HD cell firing [9] to the grid signal, the current experimental manipulation did not reduce excitatory drive to downstream regions, but instead only altered the directional accuracy of the HD signal.…”

“…If the spatial periodicity of grid cells depends on a directional tuning signal coming from HD cell inputs [43], selectively manipulating the directionality of HD cells while recording grid cells could provide a more direct test of this hypothesis. This type of manipulation might also provide greater insight into how this heading information is integrated into grid cell firing, beyond the binary distinction of whether or not it plays any role at all [9]. One might expect that using the same optogenetic manipulation to cause HD cells to become unstable would also cause a gradual rotation of grid cell firing nodes, in unison with the gradual circular drift of the HD signal observed in the current experiments.…”

“…Previous studies have found a tight coupling between co-recorded HD cells and place cells under cue conflict conditions [45], implying that there is some functional relationship between the two signals. HD cells appear to play a direct role in generating grid cell firing [9] and grid cells in turn likely provide critical information to the place cell network [46]. Although layer III of the entorhinal cortex, which contains HD cells [47], also has direct projections to the hippocampus [48], the HD network's contribution to place cells may be mediated by the grid cell network.…”

“…HD cells are the most basic of these representations, and fire according to animals' heading in the horizontal plane [7]. The firing of these HD cells is thought to be an important component of the more complex spatial tuning of grid cells and place cells [8,9]. Due to their directional representation, the HD signal formed by the firing of a population of HD cells has been conceived of as a 'neural compass' that can guide animals' behavior, and previous work has shown that an animal's heading over time can be reliably reconstructed from the firing of an ensemble of HD cells [10].…”

A new direction for grid cells

“…The maintenance of relative angular difference between modules of grid cells (Krupic et al, 2015) suggests a role in keeping track of directions. Input from cells that code head direction, namely, head-direction cells, seems to be necessary for the grid-like properties of grid cells (Winter, Clark & Taube, 2015). Disrupting the input of headdirection cells from the anterior thalamic nucleus to the entorhinal cortex (using anesthetics) disrupted the grid properties of grid cells.…”