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The thalamo-cortical auditory receptive fields: regulation by the states of vigilance, learning and the neuromodulatory systems

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Abstract

The goal of this review is twofold. First, it aims to describe the dynamic regulation that constantly shapes the receptive fields (RFs) and maps in the thalamo-cortical sensory systems of undrugged animals. Second, it aims to discuss several important issues that remain unresolved at the intersection between behavioral neurosciences and sensory physiology. A first section presents the RF modulations observed when an undrugged animal spontaneously shifts from waking to slow-wave sleep or to paradoxical sleep (also called REM sleep). A second section shows that, in contrast with the general changes described in the first section, behavioral training can induce selective effects which favor the stimulus that has acquired significance during learning. A third section reviews the effects triggered by two major neuromodulators of the thalamo-cortical system—acetylcholine and noradrenaline—which are traditionally involved both in the switch of vigilance states and in learning experiences. The conclusion argues that because the receptive fields and maps of an awake animal are continuously modulated from minute to minute, learning-induced sensory plasticity can be viewed as a "crystallization" of the receptive fields and maps in one of the multiple possible states. Studying the interplays between neuromodulators can help understanding the neurobiological foundations of this dynamic regulation.

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Notes

  1. The fact that parvalbumin immunoreactivity, almost exclusively limited to the neuropil, is much stronger in MGv than in any other divisions pleads in favor of this possibility (Cruikshank et al. 2001).

  2. Note that this GABAergic input can come from the inferior colliculus, from the thalamic reticular nucleus, or from the intrinsic MGB interneurons whose proportion varies from 33% of the cells in the cat to less than 1% in the rat (Huang et al. 1999; Winer and Larue 1988).

  3. Selective re-tunings in favor of the CS without increases (or even with decreases) in evoked responses during the training trials were also observed in the auditory thalamus, particularly in the dorsal division (Edeline and Weinberger, unpublished observations).

  4. The only exception was from the ventral division of the auditory thalamus where the selective effects tended to dissipate over time.

  5. Initial works have already pointed out that the different duration of the effects can be observed from one cell to another (Metherate et al. 1988a).

  6. In other cases, the data from cholinergic control animals were never presented (Kilgard and Merzenich 1998a, 1998b; Kilgard et al. 2001).

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Acknowledgements

It is a pleasure to thank Norman Weinberger and Elizabeth Hennevin for detailed and insightful comments on a preliminary version of this paper.

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Edeline, JM. The thalamo-cortical auditory receptive fields: regulation by the states of vigilance, learning and the neuromodulatory systems. Exp Brain Res 153, 554–572 (2003). https://doi.org/10.1007/s00221-003-1608-0

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