Article Figures & Data
Figures
- Figure 1.
Song system schematic and tyrosine hydroxylase staining in NIf. A, Schematic diagram of the three major song system pathways: premotor, anterior forebrain, and ascending auditory. HVC, which is part of all three pathways, receives auditory input indirectly from Field L via NIf. Field L is the primary forebrain structure that receives auditory input from the thalamic nucleus Ovoidalis. NIf provides the major auditory input to HVC. The anterior forebrain pathway includes HVC, Area X, DLM, LMAN, and RA. The premotor pathway includes HVC and RA. Area X, Song-related region of the basal ganglia; DLM, medial portion of the dorsolateral nucleus of the anterior thalamus; Field L, primary thalamorecipient auditory area of the telencephalon; LMAN, lateral portion of the magnocellular nucleus of the anterior nidopallium; Ov, nucleus Ovoidalis of the thalamus; Resp., respiratory areas of the brainstem; Syrinx, avian vocal organ. B, Parasaggital brain section labeled with an antibody to tyrosine hydroxylase (TH). NIf is densely innervated with TH-positive fibers. Arrowheads indicate borders of NIf.
- Figure 2.
Low doses of NE in NIf increase HVC auditory responsiveness relative to spontaneous activity. In each of these examples, recordings were made in HVC during baseline auditory trials (left), after low-dose NE (0.5 or 1 mm) administration in the ipsilateral NIf (center), and after recovery (right). The top portion of each panel shows the raster plot of spike events during 30 auditory trials and the middle portion is the cumulative PSTH. The neural record is an example of one auditory trial. The bottom trace is the amplitude waveform of the auditory stimulus. A, After administration of a low dose of NE to NIf, spontaneous multiunit (MU) HVC activity was decreased and auditory responsiveness, as measured by the AR, was increased. Recovery was observed 6 min later. B, Single HVC unit (SU) recorded during administration of a low dose of NE to NIf. This unit demonstrated decreased spontaneous firing and an increased AR after low-dose NE in NIf. Recovery was observed 6 min later. C, Mean single-unit AR for HVC was significantly increased by application of a low dose of NE to the ipsilateral NIf (n = 5). D, Likewise, mean multiunit HVC AR was significantly increased by low NE in NIf (n = 5). Baseline AR values are shown as open bars, AR values after NE as black bars, and AR values after recovery as hatched bars. *p < 0.05. Error bars represent SEM.
- Figure 3.
High doses of NE in NIf eliminate HVC auditory responsiveness. In contrast to the effects of low doses of NE in NIf, higher doses (5 or 8 mm) led to a suppression of HVC auditory responsiveness. A, Multiunit (MU) recording in HVC during baseline recordings (left), after application of a high dose of NE to the ipsilateral NIf (center), and after 12 min of recovery (right). High-dose NE decreased both spontaneous and auditory activity in HVC. B, Single-unit (SU) recording in HVC during a similar experiment. Application of high-dose NE to NIf resulted in a complete loss of auditory responsiveness by this unit (center). Recovery was observed 10 min later (right). C, Mean single-unit AR for HVC was significantly decreased by application of a high dose of NE to the ipsilateral NIf (n = 7) (left). Likewise, mean multiunit AR for HVC was significantly decreased by high-dose NE in NIf (n = 5) (right). Baseline AR values are shown as open bars, AR values after NE as black bars, and AR values after recovery as hatched bars. *p < 0.05. Error bars represent SEM. D, To determine whether individual HVC units demonstrate both enhancement and suppression of auditory responsiveness, single HVC units were recorded throughout a series of doses of NE to the ipsilateral NIf. Whereas the baseline AR values of this unit were stable (open bars), sequential application of two low doses of NE to the ipsilateral NIf each caused an increase in the auditory response (gray bars). A subsequent high dose of NE to NIf caused a complete loss of auditory responsiveness (black bar). The auditory response returned to baseline levels after 15 min. The total time between the first baseline trial and the last recovery trial was 123 min.
- Figure 4.
NE in NIf modulates NIf and HVC auditory responsiveness. A, In this experiment, multiunit (MU) activity in an ipsilateral NIf-HVC pair was recorded simultaneously during application of a low dose of NE to NIf. Both NIf (top) and HVC (bottom) demonstrated baseline auditory responses (left). After administration of low-dose NE to NIf, auditory responsiveness was increased relative to spontaneous activity at both recording sites (middle). Both NIf and HVC recovered auditory responses similar to the original control responses after 14 min (right). B, In all similar experiments (n = 3), low doses of NE to NIf caused a significant increase in both NIf (left) and HVC (right) AR values. C, In contrast, administration of high-dose NE to NIf (n = 4) significantly decreased both NIf (left) and HVC (right) AR values. Baseline AR values are shown as open bars, AR values after NE as black bars,and AR values after recovery as hatched bars. *p < 0.05. Error bars represent SEM.
- Figure 5.
α-Adrenergic agonists in NIf replicate the effects of NE. In these experiments, we tested the specificity of the noradrenergic effects on auditory responsiveness by injecting receptor-specific agonists into NIf while recording from HVC. Bar graphs on the right represent cumulative data from all experiments targeting a given receptor subtype. The mean AR values during baseline recordings are shown as open bars, mean AR values after agonist administration as blackbars, and mean AR values after recovery as hatched bars. A, Auditory responses at a multiunit (MU) recording site in HVC (left) were increased after administration of a low dose of 1 mm phenylephrine, an α1-receptor specific agonist (center). As shown in the graph on the right, mean AR values were significantly increased by low doses of α1 agonists (n = 4). B, Administration of a high dose of 8 mm cirazoline, another α1-receptor-specific agonist, resulted in a significant decrease in HVC spontaneous activity and auditory response. High doses of α1 agonists significantly decreased HVC AR values in all similar experiments (n = 4) (right). C, Both auditory responsiveness and spontaneous activity at this multiunit HVC recording site were decreased by administration of 5 mm clonidine, an α2-receptor specific agonist, to the ipsilateral NIf. The mean AR value for HVC was significantly reduced by α2 agonists in NIf (n = 6) (right). *p < 0.05. Error bars represent SEM.
- Figure 6.
Injection of α-adrenergic antagonists into NIf blocks arousal-mediated suppression of HVC responses. A, Schematic of the two types of randomly intermixed auditory trials used in arousal experiments. During resting trials, a lightly sedated bird was presented with the BOS stimulus. During aroused trials, the bird was aroused by an air puff to the chest 1 sec before the beginning of the BOS stimulus. The two types of trials were then separated for analysis. B, Multiunit (MU) HVC auditory responses were recorded during resting (left) and aroused (right) auditory stimulus trials in the absence of any manipulation of NIf. Arousal resulted in complete suppression of HVC auditory responses. C, After infusion of α1 and α2 receptor-specific antagonists (5 mm benoxathian and 5 mm idazoxan) to the ipsilateral NIf, a second series of intermixed resting and aroused trials was performed. α-Adrenergic antagonists prevented the arousal-mediated suppression of HVC auditory responses. D, After 15 min of recovery, arousal again elicited a suppression of HVC auditory responses.
- Figure 7.
α-Adrenergic antagonists in NIf block state-dependent changes in HVC auditory activity. Cumulative data from arousal experiments (n = 7). Under baseline conditions (left bars), arousal caused a complete suppression of HVC auditory responses. After administration of α1- and α2-adrenergic receptor antagonists into the ipsilateral NIf, HVC demonstrated auditory responses even in the aroused state (center bars). There was no significant difference between resting and aroused auditory responsiveness, as measured by AR, after drug application to NIf. Similarly, the antagonists in NIf did not significantly affect resting auditory responses in HVC. After 15 min, arousal again suppressed auditory responses (right bars). In each pair of bars, the resting AR values are shown as open bars and aroused AR values are shown as black bars. * p < 0.05. Error bars represent SEM.
