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The irregular firing properties of thalamic head direction cells mediate turn-specific modulation of the directional tuning curve

Tsanov, M., Chah, E., Noor, M. S., Egan, C., Reilly, R. B., Aggleton, John Patrick, Erichsen, Jonathan Thor, Vann, Seralynne Denise and O'Mara, S. M. 2014. The irregular firing properties of thalamic head direction cells mediate turn-specific modulation of the directional tuning curve. Journal of Neurophysiology 112 (9) , pp. 2316-2331. 10.1152/jn.00583.2013

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Abstract

Head-direction cells encode an animal's heading in the horizontal plane. However, it is not clear why the directionality of a cell's mean firing rate differs for clockwise, compared to counter-clockwise head turns (this difference is known as the 'separation angle') in anterior thalamus. Here we investigated, in freely-behaving rats, if intrinsic neuronal firing properties are linked to this phenomenon. We found a positive correlation between the separation angle and the spiking variability of thalamic head-direction cells. To test whether this link is driven by hyperpolarisation-inducing currents, we investigated the effect of thalamic reticular inhibition during high-voltage spindles on directional spiking. While the selective directional firing of thalamic neurons was preserved, we found no evidence for entrainment of thalamic head-direction cells by high-voltage spindle oscillations. We then examined the role of depolarisation-inducing currents in the formation of separation angle. Using a single-compartment Hodgkin-Huxley model, we show that modelled neurons fire with higher frequencies during the ascending phase of sinusoidal current injection (mimicking the head-direction tuning curve), when simulated with higher high-threshold calcium channel conductance. These findings demonstrate that the turn-specific encoding of directional signal strongly depends on the ability of thalamic neurons to fire irregularly in response to sinusoidal excitatory activation. Another crucial factor for inducing phase lead to sinusoidal current injection was the presence of spike-frequency adaptation current in the modelled neurons. Our data support a model in which intrinsic biophysical properties of thalamic neurons mediate the physiological encoding of directional information.

Item Type: Article
Date Type: Publication
Status: Published
Schools: Medicine
Optometry and Vision Sciences
Neuroscience and Mental Health Research Institute (NMHRI)
Subjects: R Medicine > RE Ophthalmology
Publisher: American Physiological Society
ISSN: 0022-3077
Funders: Wellcome Trust
Date of Acceptance: 12 August 2014
Last Modified: 17 Apr 2019 21:06
URI: http://orca.cf.ac.uk/id/eprint/63751

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