Induction of selective plasticity in the frequency tuning of auditory cortex and auditory thalamus neurons by locus coeruleus stimulation

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Abstract

Neurons in primary sensory cortices display selective receptive field plasticity in behavioral situations ranging from classical conditioning to attentional tasks, and it is generally assumed that neuromodulators promote this plasticity. Studies have shown that pairing a pure-tone and a stimulation of the nucleus basalis magnocellularis mimics the selective receptive field facilitations described after classical conditioning. Here, we evaluated the consequences of repeated pairings between a particular sound frequency and a phasic stimulation of locus coeruleus (LC) on the frequency tuning of auditory thalamus and auditory cortex neurons. Selective alterations for the paired frequency were observed for more than 30% of the cells recorded both in cortex and in thalamus. There were as much selective increases as selective decreases at the cortical level, whereas selective increases were prevailing at the thalamic level. Selective changes usually persisted 15 min after pairing in cortex; they dissipated in thalamus, and so did the general increases in both structures. In animals with stimulation sites outside the LC, pairing induced either general changes or no effect. These results indicate that the selective plasticity induced in the frequency tuning of auditory cortex neurons by LC stimulation is bidirectional, thereby suggesting that noradrenergic activation can contribute to the different forms of plasticity observed after distinct behavioral paradigms.

Highlights

►Tone-LC stimulation pairing induces plasticity in auditory cortex and thalamus. ►>30% of the cells in each region show selective changes for the paired frequency. ►There are selective increases and selective decreases in cortex, they last >15min. ►Selective increases prevail in thalamus; they tend to dissipate over time. ►Stimulation sites outside the LC induce either general changes or no changes.

Introduction

It is now well documented that neurons in primary sensory cortices can display highly selective plasticity in a large diversity of situations ranging from classical conditioning and two tones discrimination to attentional task (reviews in Edeline, 1999, Weinberger, 2004, Fritz et al., 2005a, Fritz et al., 2007). It is also commonly assumed that neuromodulators are key factors whose activity can promote some of the effects observed in sensory cortices during behavioral training.

For at least three decades, a vast literature has described the action of neuromodulators in sensory cortices both at the cellular level (reviews in McCormick, 1992, McCormick and Bal, 1997) and at the functional level (Rasmusson, 2000, Gu, 2002, Berridge and Waterhouse, 2003, Weinberger, 2003). The auditory cortex (ACx) is probably the cortical area for which the largest number of studies has been carried out (reviews in Edeline, 2003, Metherate et al., 2005). A paradigm that has been extensively used to assess the impact of neuromodulators on the functional properties of auditory cortex cells relies on the systematic association between a particular sensory stimulus and a neuromodulator. The pairing protocol involved either a stimulation of the source nucleus or a iontophoretic application at the vicinity of the recorded cell. For the cholinergic system, except two studies using iontophoretic application (Metherate and Weinberger, 1989, Metherate and Weinberger, 1990), all the others used electrical stimulation of the nucleus basalis magnocellularis (e.g., Bakin and Weinberger, 1996, Kilgard and Merzenich, 1998a, Kilgard and Merzenich, 1998b). Similarly, the studies performed on the dopaminergic system involved electrical stimulation of the ventral tegmental area (Bao et al., 2001, Bao et al., 2003). In contrast, the only study performed on the noradrenergic system has used iontophoretic application. A pairing protocol between a particular sound frequency and a brief pulse of noradrenaline (NA) induced frequency-specific (FS) changes in the post-pairing neuron tuning curve (Manunta and Edeline, 2004). These FS effects were expressed by 28% of the recorded cells and mainly involved a selective decrease at the sound frequency paired with NA application. They were observed in the presence of propranolol, but not in the presence of phentolamine, suggesting that they were mediated by alpha-adrenoceptors.

The present study aimed at evaluating the effects of a pairing protocol between a stimulation of the locus coeruleus nucleus (LC) and a particular tone frequency. As the LC projects to the different auditory relays (Kromer and Moore, 1980, Klepper and Herbert, 1991, Thompson and Schofield, 2000, Mulders and Robertson, 2001), we recorded cells in auditory cortex and in auditory thalamus to compare the effects occurring at these two levels.

Section snippets

Subjects

Sprague–Dawley adult rats (280–350 g) were anesthetized by an initial injection of urethane (1.5 g/kg; i.p.) supplemented by additional doses (0.5 g/kg; i.p.) when reflex movements were observed after pinching the hindpaw (usually once or twice during a given recording session). The body temperature was maintained around 37 °C by a heating pad throughout the experiment. The stereotaxic frame supporting the animal was placed in a sound-attenuating chamber (IAC, model AC2).

Locus coeruleus implantation

Implantation of the

Histology

The analysis of histological material was done blind of the electrophysiological results and was performed independently by two co-authors (YM, JME). Out of 29 rats implanted with a stimulating electrode in the LC area, there were only 9 animals for which the electrode was unambiguously located within the LC. In the others, the electrodes were found in the laterodorsal tegmental nucleus (n = 3), the subcoeruleus/sublaterodorsal nucleus (n = 7), the mesencephalic trigeminal nucleus (n = 5), the

Discussion

A repeated pairing between a particular tone frequency and LC stimulation induced effects selective for that frequency in about 30% of the cells recorded in auditory cortex and in auditory thalamus. There were as much selective increases as selective decreases at the cortical level, whereas selective increases were prominent at the thalamic level. When general effects were observed, they were mainly general increases, i.e., enlargements of tuning curves. Selective effects usually persisted

Acknowledgements

This paper is dedicated to the memory of Jeff Winer for his constant support and encouragement, in particular for him pushing us to study neuromodulatory effects at the thalamic level.

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