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

Abstract

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...

Spikes and Bursts in Two Types of Thalamic Projection Neurons Differentially Shape Sleep Patterns and Auditory Responses in a Songbird

“…Uva also receives somatosensory and visual inputs (Wild, 1994). As in mammalian thalamic relays, Uva receives information about ongoing motor instructions via respiratory and brainstem nuclei (Reinke and Wild, 1998) and is innervated by cholinergic fibers (Akutagawa and Konishi, 2005). One of Uva's behavior-related functions is to control the temporal patterning of learned songs (Williams and Vicario, 1993;Coleman and Vu, 2005).…”

Thalamic Gating of Auditory Responses in Telencephalic Song Control Nuclei

“…Although all of the injections of CTB into Uva were small, none of them was strictly confined to the nucleus. Nevertheless, they each resulted in retrograde labeling of cells in all the nuclei previously identified as sources of afferents to Uva, namely the dorsal column and external cuneate nuclei, predominantly layer 13 of the optic tectum, a cell group in the ventrolateral medulla, the medial habenular nucleus, and the dorsal part of the superior reticular nucleus of the thalamus (Wild, 1994;Reinke and Wild, 1998;Striedter and Vu, 1998;Akutagawa and Konishi, 2005). In addition, the present experiments revealed another potential source of input to Uva, namely LLV (Fig.…”

“…Suppression of HVC auditory responses by BF stimulation is much longer lasting (ϳ10 min) than suppression after high-frequency Uva stimulation (ϳ2 s) (Figs. 9, 10), and Uva neurons are not cholinergic (Akutagawa and Konishi, 2005), suggesting two distinct gating mechanisms. In addition to cholinergic gating of HVC auditory responses, adrenergic agonists and antagonists comodulate auditory responses in HVC and NIf (Cardin and Schmidt, 2004b).…”

“…medial habenula (Akutagawa and Konishi, 2005), a structure implicated in attention (Lecourtier and Kelly, 2005) and sleep/wake cycles in mammals (Haun et al, 1992;Valjakka et al, 1998); a similar function in birds may enable Uva to regulate auditory activity in HVC and NIf in a state-dependent manner. Third, the influence of Uva on HVC and NIf neuronal activity operates on a fast timescale, consistent with recent evidence showing that auditory responses in these nuclei can be gated synchronously by arousal and attention on a timescale of milliseconds to seconds (Nick and Konishi, 2001;Cardin and Schmidt, 2003).…”

“…The thalamus influences a wide variety of sensory and motor processes in the telencephalon, including gating of sensory information (Aguilar and Castro-Alamancos, 2005;Akutagawa and Konishi, 2005;Casagrande et al, 2005). In the zebra finch, a songbird that learns to sing using auditory feedback (Konishi, 1965a,b), the nucleus Uvaeformis (Uva), is the sole thalamic input to the telencephalic nucleus HVC (used as a proper name), a sensorimotor structure essential to singing and song perception (Nottebohm et al, 1976;Brenowitz, 1991;Del Negro et al, 1998;Gentner et al, 2000), and to the main auditory afferent of HVC, the telencephalic nucleus interface (NIf) (Cardin and Schmidt, 2004a;Coleman and Mooney, 2004) (see Fig.…”