Noradrenergic Inputs Mediate State Dependence of Auditory Responses in the Avian Song System

Cardin, Jessica A.; Schmidt, Marc F.

doi:10.1523/jneurosci.1951-04.2004

Cited by 100 publications

(96 citation statements)

References 46 publications

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“…AChE has also been seen in noncholinergic areas of the brain and has been shown to be important in degrading other neuropeptides as well as AChE (22,23,24). Another fundamental issue concerns the initial site of auditory gating, which is now recognized to be the NIf, from which the HVC receives most or all of its auditory input (6). If so, then from where are the cholinergic inputs to the NIf coming?…”

Section: Discussionmentioning

confidence: 99%

Connections of thalamic modulatory centers to the vocal control system of the zebra finch

Akutagawa

Konishi

2005

Proc. Natl. Acad. Sci. U.S.A.

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The vocal control system of zebra finches shows auditory gating in which neuronal responses to the individual bird's own song vary with behavioral states such as sleep and wakefulness. However, we know neither the source of gating signals nor the anatomical connections that could link the modulatory centers of the brain with the song system. Two of the song-control nuclei in the forebrain, the HVC (used as the proper name) and the interfacial nucleus of the nidopallium, both show auditory gating, and they receive input from the uvaeform nucleus (Uva) in the thalamus. We used a combination of anterograde and retrograde tracing methods to show that the dorsal part of the reticular formation and the medial habenula (MHb) project to the Uva. We also show by choline acetyl transferase immunohistochemistry that the MHb is cholinergic and sends cholinergic fibers to the Uva. Our findings suggest that the Uva might serve as a hub to coordinate neuromodulatory input into the song system. auditory gating ͉ cholinergic ͉ song system ͉ thalamus T he song system is a discrete, interconnected series of brain nuclei in songbirds that controls singing, which is a learned vocal behavior ( Fig. 1) (1). In addition to displaying song motor activity, neurons of most song nuclei selectively respond to playback of the individual bird's own song (BOS) (2). Responses to the BOS are not created de novo in each song nucleus (3) but are relayed from the HVC to a vocal motor pathway that includes the robust nucleus of the arcopallium (RA) and the tracheosyringeal part of the hypoglossal nucleus. Auditory information also is transmitted from the HVC to an anterior forebrain pathway that includes area X within the songbird medial striatum; the nucleus dorsolateralis anterior thalami, pars medialis; the lateral magnocellular nucleus of the anterior nidopallium; and the RA. The source of auditory input to the HVC is thought to be the interfacial nucleus of the nidopallium (NIf), in which selectivity for the BOS is not as exclusive as in the HVC (4). Both the degree and selectivity of BOS-evoked responses in the HVC vary with natural and induced behavioral states such as sleeping, wakefulness, and anesthesia. This phenomenon is called ''auditory gating'' (5) and provides evidence that links the modulation of auditory input with the vocal control system. The first site of gating in the chain of song nuclei is thought to be the NIf (6). However, little is known about the source of signals that control gating in the NIf. Although several candidate sources for neural modulation have been postulated (7,8), the connections between these areas and the song system remain tenuous. The present study provides anatomical evidence that the uvaeform nucleus (Uva), which projects to both the NIf and HVC, receives cholinergic fibers from neurons in the medial habenula (MHb) and also afferents from the nucleus reticularis superior, pars dorsalis (RSd). These thalamic areas are neuromodulatory centers in other vertebrates, suggesting that the Uva in songbirds ma...

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Section: Discussionmentioning

confidence: 99%

Connections of thalamic modulatory centers to the vocal control system of the zebra finch

Akutagawa

Konishi

2005

Proc. Natl. Acad. Sci. U.S.A.

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“…In the song system, a similar role has been found for NE in modulating the salience of auditory signals. NE application to the forebrain nucleus interface of the nidopallium (NIf) increases or decreases auditory responses in a dose-dependent manner (Cardin and Schmidt 2004). Similarly, NE could increase the salience of signals within RA, either through decreasing spontaneous activity, increasing evoked activity, or both.…”

Section: Consequences Of Ne Action In Ramentioning

confidence: 99%

“…In songbirds, NE gates statedependent auditory responses in the song system (Cardin and Schmidt 2004;Dave et al 1998). Because RA is a sensorimotor nucleus, NE release in RA could modulate both auditory and premotor activity during singing.…”

Section: Implications For Behaviormentioning

confidence: 99%

“…These neuromodulators potentially mediate the sensitivity of song behavior to social (Collins 2004;Nowicki and Searcy 2004) and seasonal (Brenowitz 2004) factors. In particular, NE modulates auditory responses in the song system (Cardin and Schmidt 2004;Dave et al 1998). Moreover, NE has been associated with song production: decreases in NE levels decrease singing frequency (Barclay et al 1996) and singing-related gene expression (Castelino and Ball 2005).…”

Section: Introductionmentioning

confidence: 99%

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Noradrenergic Modulation of Activity in a Vocal Control Nucleus In Vitro

Solis

Perkel

2006

Journal of Neurophysiology

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Solis, Michele M. and David J. Perkel. Noradrenergic modulation of activity in a vocal control nucleus in vitro. J Neurophysiol 95: 2265-2276, 2006. First published December 21, 2005 doi:10.1152/jn.00836.2005. Norepinephrine (NE) can profoundly modulate sensory processing, but its effect on motor function is less well understood. Birdsong is a learned behavior involving sensory and motor processes that are influenced by NE. A potential site of NE action is the robust nucleus of the arcopallium (RA): RA receives noradrenergic inputs and has adrenergic receptors, and it is a sensorimotor area instrumental to song production. We hypothesized that NE modulates RA neurons, and as a first test, we examined the effect of NE on RA activity in vitro. We recorded spontaneous activity extracellularly from isolated RA neurons in brain slices made from adult male zebra finches. These neurons exhibited regular tonic activity with firing rates averaging 5.5 Hz. Bath application of NE rapidly and reversibly decreased firing for the majority of neurons, to the extent that spontaneous activity was often abolished. This was likely a direct effect on the cell recorded, because it occurred with blockade of fast excitatory and inhibitory synaptic transmission or of all synaptic transmission. The NE-induced suppression involved ␣2-adrenergic receptors: yohimbine, an antagonist, completely reversed the suppression, and clonidine, an agonist, partially mimicked it. Perforated patch recordings revealed that NE induced a conductance increase in RA neurons; however, this did not prevent cells from firing when stimulated by afferents in HVC. For some neurons, NE application resulted in an increase in signal-to-noise ratio for spikes evoked by HVC stimulation. Thus NE could strongly modulate the spontaneous activity of RA cells, potentially enhancing signals relayed through RA.

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“…An animal's physiological and behavioural state is known to be an important factor affecting the specific actions of neuromodulators in the case of modulation of sensory pathways (Kay and Laurent, 1999;Christensen et al, 2000;Cardin and Schmidt, 2004). Whether the same applies to modulation of motor circuits has been unclear, as fewer examples are known of context-dependent modulation of motor output (Nusbaum and Marder, 1989).…”

Section: Discussionmentioning

confidence: 99%

Neuromodulation of the locust frontal ganglion during the moult: a novel role for insect ecdysis peptides

Zilberstein

Ewer

Ayali

2006

Journal of Experimental Biology

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SUMMARY In insects, continuous growth requires the periodic replacement of the exoskeleton during the moult. A moulting insect displays a stereotypical set of behaviours that culminate in the shedding of the old cuticle at ecdysis. Moulting is an intricate process requiring tightly regulated physiological changes and behaviours to allow integration of environmental cues and to ensure the proper timing and sequence of its components. This is under complex hormonal regulation, and is an important point of interaction between endocrine and neural control. Here, we focus on the locust frontal ganglion (FG), an important player in moulting behaviour, as a previously unexplored target for ecdysis peptides. We show that application of 10-7 mol l-1 ecdysis-triggering hormone (ETH) or 10-7 mol l-1 and 10-6 mol l-1 Pre-ecdysis-triggering hormone (PETH) to an isolated FG preparation caused an increase in bursting frequency in the FG, whereas application of 10-6 mol l-1 eclosion hormone (EH) caused an instantaneous, though temporary, total inhibition of all FG rhythmic activity. Crustacean cardioactive peptide (CCAP), an important peptide believed to turn on ecdysis behaviour, caused a dose-dependent increase of FG burst frequency. Our results imply a novel role for this peptide in generating air-swallowing behaviour during the early stages of ecdysis. Furthermore, we show that the modulatory effects of CCAP on the FG motor circuits are dependent on behavioural state and physiological context. Thus, we report that pre-treatment with ETH caused CCAP-induced effects similar to those induced by CCAP alone during pre-ecdysis. Thus, the action of CCAP seems to depend on pre-exposure to ETH, which is thought to be released before CCAP in vivo.

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Noradrenergic Inputs Mediate State Dependence of Auditory Responses in the Avian Song System

Cited by 100 publications

References 46 publications

Connections of thalamic modulatory centers to the vocal control system of the zebra finch

Connections of thalamic modulatory centers to the vocal control system of the zebra finch

Noradrenergic Modulation of Activity in a Vocal Control Nucleus In Vitro

Neuromodulation of the locust frontal ganglion during the moult: a novel role for insect ecdysis peptides

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