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Characterization of synaptically connected nuclei in a potential sensorimotor feedback pathway in the zebra finch song system.

Williams SM, Nast A, Coleman MJ - PLoS ONE (2012)

Bottom Line: As previously reported, we found similar timing in spontaneous bursts of activity in MMAN and HVC.However, inactivation of MMAN resulted in no consistent change in auditory responses in HVC.Taken together, these results indicate that MMAN provides functional excitatory input to HVC but does not provide significant auditory input to HVC in anesthetized animals.

View Article: PubMed Central - PubMed

Affiliation: Claremont McKenna College, Claremont, California, United States of America.

ABSTRACT
Birdsong is a learned behavior that is controlled by a group of identified nuclei, known collectively as the song system. The cortical nucleus HVC (used as a proper name) is a focal point of many investigations as it is necessary for song production, song learning, and receives selective auditory information. HVC receives input from several sources including the cortical area MMAN (medial magnocellular nucleus of the nidopallium). The MMAN to HVC connection is particularly interesting as it provides potential sensorimotor feedback to HVC. To begin to understand the role of this connection, we investigated the physiological relation between MMAN and HVC activity with simultaneous multiunit extracellular recordings from these two nuclei in urethane anesthetized zebra finches. As previously reported, we found similar timing in spontaneous bursts of activity in MMAN and HVC. Like HVC, MMAN responds to auditory playback of the bird's own song (BOS), but had little response to reversed BOS or conspecific song. Stimulation of MMAN resulted in evoked activity in HVC, indicating functional excitation from MMAN to HVC. However, inactivation of MMAN resulted in no consistent change in auditory responses in HVC. Taken together, these results indicate that MMAN provides functional excitatory input to HVC but does not provide significant auditory input to HVC in anesthetized animals. We hypothesize that MMAN may play a role in motor reinforcement or coordination, or may provide modulatory input to the song system about the internal state of the animal as it receives input from the hypothalamus.

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Inactivation of MMAN resulted in little change in HVC auditory responses.A. Example of auditory evoked activity in MMAN and HVC before (left) and with (right) GABA application to MMAN. Top trace, PSTH of HVC response to ten iterations of BOS playback. Bin size, 25 ms. Middle trace, single, raw example of multiunit activity in HVC. Bottom trace, sonogram of BOS. B. Location of GABA application in MMAN approximated by rhodamine labeling (arrows). LMAN is outlined to the right of the dye (dotted semicircle, *). Scale bar, 200 µm. The dashed vertical line denotes the midline. Dorsal is upward. C. Average response of HVC to BOS presentation before (pre), during (GABA) and after (post) BOS presentation. In two experiments (filled squares) GABA application to MMAN did not produce a significant change in HVC response. In one experiment (open squares) there was a significant decrease in the HVC response to BOS during GABA application compared to pre and post GABA application (ANOVA, p<0.5, Tukey post-hoc). In one bird (open stars) the response to BOS increased throughout the duration of the experiment (pre, GABA, and post were all significantly different than each other; p<0.5, ANOVA, Tukey post-hoc). D. Normalized responses of data shown in C.
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pone-0032178-g006: Inactivation of MMAN resulted in little change in HVC auditory responses.A. Example of auditory evoked activity in MMAN and HVC before (left) and with (right) GABA application to MMAN. Top trace, PSTH of HVC response to ten iterations of BOS playback. Bin size, 25 ms. Middle trace, single, raw example of multiunit activity in HVC. Bottom trace, sonogram of BOS. B. Location of GABA application in MMAN approximated by rhodamine labeling (arrows). LMAN is outlined to the right of the dye (dotted semicircle, *). Scale bar, 200 µm. The dashed vertical line denotes the midline. Dorsal is upward. C. Average response of HVC to BOS presentation before (pre), during (GABA) and after (post) BOS presentation. In two experiments (filled squares) GABA application to MMAN did not produce a significant change in HVC response. In one experiment (open squares) there was a significant decrease in the HVC response to BOS during GABA application compared to pre and post GABA application (ANOVA, p<0.5, Tukey post-hoc). In one bird (open stars) the response to BOS increased throughout the duration of the experiment (pre, GABA, and post were all significantly different than each other; p<0.5, ANOVA, Tukey post-hoc). D. Normalized responses of data shown in C.

Mentions: As MMAN responds to auditory stimulation and provides functional excitatory synaptic input to HVC, it is possible that MMAN also provides sensory feedback to HVC and contributes to the auditory response in HVC. GABAA receptors have been localized in MMAN [36], so to test this idea we inactivated MMAN with GABA while recording auditory evoked activity in HVC (n = 4 in 3 birds). The effect of GABA in MMAN on auditory responses in HVC was calculated using the activity (response) during auditory stimuli (Figure 6), as the response strength was more variable, presumably due to a large variability in baseline activity. GABA inactivation of MMAN had no significant effect on ipsilateral HVC auditory activity in 2 of 4 experiments (Figure 6; one-way ANOVA, p>0.05). In one experiment there was a continual increase in auditory response, even after GABA had washed out of MMAN (stars in Figure 6C&D). This response was unusual, and each condition (pre, GABA, post) was significantly different from the others (Tukey post-hoc p<0.05). One other experiment showed a significant decrease in response to GABA inactivation of MMAN compared to pre and post (open squares in Figure 6C&D; ANOVA, p<0.05, Tukey post-hoc test). Pre and post were not different from each other (p>0.05, Tukey post-hoc test). The site of GABA injection was histologically confirmed in all cases (see Figure 6B for an example). In summary, inactivation of MMAN with GABA had little reliable effect on auditory response in HVC. These data suggest that MMAN is not a significant source of auditory input to HVC and its auditory activity may be the result of input through the feedback pathway.


Characterization of synaptically connected nuclei in a potential sensorimotor feedback pathway in the zebra finch song system.

Williams SM, Nast A, Coleman MJ - PLoS ONE (2012)

Inactivation of MMAN resulted in little change in HVC auditory responses.A. Example of auditory evoked activity in MMAN and HVC before (left) and with (right) GABA application to MMAN. Top trace, PSTH of HVC response to ten iterations of BOS playback. Bin size, 25 ms. Middle trace, single, raw example of multiunit activity in HVC. Bottom trace, sonogram of BOS. B. Location of GABA application in MMAN approximated by rhodamine labeling (arrows). LMAN is outlined to the right of the dye (dotted semicircle, *). Scale bar, 200 µm. The dashed vertical line denotes the midline. Dorsal is upward. C. Average response of HVC to BOS presentation before (pre), during (GABA) and after (post) BOS presentation. In two experiments (filled squares) GABA application to MMAN did not produce a significant change in HVC response. In one experiment (open squares) there was a significant decrease in the HVC response to BOS during GABA application compared to pre and post GABA application (ANOVA, p<0.5, Tukey post-hoc). In one bird (open stars) the response to BOS increased throughout the duration of the experiment (pre, GABA, and post were all significantly different than each other; p<0.5, ANOVA, Tukey post-hoc). D. Normalized responses of data shown in C.
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pone-0032178-g006: Inactivation of MMAN resulted in little change in HVC auditory responses.A. Example of auditory evoked activity in MMAN and HVC before (left) and with (right) GABA application to MMAN. Top trace, PSTH of HVC response to ten iterations of BOS playback. Bin size, 25 ms. Middle trace, single, raw example of multiunit activity in HVC. Bottom trace, sonogram of BOS. B. Location of GABA application in MMAN approximated by rhodamine labeling (arrows). LMAN is outlined to the right of the dye (dotted semicircle, *). Scale bar, 200 µm. The dashed vertical line denotes the midline. Dorsal is upward. C. Average response of HVC to BOS presentation before (pre), during (GABA) and after (post) BOS presentation. In two experiments (filled squares) GABA application to MMAN did not produce a significant change in HVC response. In one experiment (open squares) there was a significant decrease in the HVC response to BOS during GABA application compared to pre and post GABA application (ANOVA, p<0.5, Tukey post-hoc). In one bird (open stars) the response to BOS increased throughout the duration of the experiment (pre, GABA, and post were all significantly different than each other; p<0.5, ANOVA, Tukey post-hoc). D. Normalized responses of data shown in C.
Mentions: As MMAN responds to auditory stimulation and provides functional excitatory synaptic input to HVC, it is possible that MMAN also provides sensory feedback to HVC and contributes to the auditory response in HVC. GABAA receptors have been localized in MMAN [36], so to test this idea we inactivated MMAN with GABA while recording auditory evoked activity in HVC (n = 4 in 3 birds). The effect of GABA in MMAN on auditory responses in HVC was calculated using the activity (response) during auditory stimuli (Figure 6), as the response strength was more variable, presumably due to a large variability in baseline activity. GABA inactivation of MMAN had no significant effect on ipsilateral HVC auditory activity in 2 of 4 experiments (Figure 6; one-way ANOVA, p>0.05). In one experiment there was a continual increase in auditory response, even after GABA had washed out of MMAN (stars in Figure 6C&D). This response was unusual, and each condition (pre, GABA, post) was significantly different from the others (Tukey post-hoc p<0.05). One other experiment showed a significant decrease in response to GABA inactivation of MMAN compared to pre and post (open squares in Figure 6C&D; ANOVA, p<0.05, Tukey post-hoc test). Pre and post were not different from each other (p>0.05, Tukey post-hoc test). The site of GABA injection was histologically confirmed in all cases (see Figure 6B for an example). In summary, inactivation of MMAN with GABA had little reliable effect on auditory response in HVC. These data suggest that MMAN is not a significant source of auditory input to HVC and its auditory activity may be the result of input through the feedback pathway.

Bottom Line: As previously reported, we found similar timing in spontaneous bursts of activity in MMAN and HVC.However, inactivation of MMAN resulted in no consistent change in auditory responses in HVC.Taken together, these results indicate that MMAN provides functional excitatory input to HVC but does not provide significant auditory input to HVC in anesthetized animals.

View Article: PubMed Central - PubMed

Affiliation: Claremont McKenna College, Claremont, California, United States of America.

ABSTRACT
Birdsong is a learned behavior that is controlled by a group of identified nuclei, known collectively as the song system. The cortical nucleus HVC (used as a proper name) is a focal point of many investigations as it is necessary for song production, song learning, and receives selective auditory information. HVC receives input from several sources including the cortical area MMAN (medial magnocellular nucleus of the nidopallium). The MMAN to HVC connection is particularly interesting as it provides potential sensorimotor feedback to HVC. To begin to understand the role of this connection, we investigated the physiological relation between MMAN and HVC activity with simultaneous multiunit extracellular recordings from these two nuclei in urethane anesthetized zebra finches. As previously reported, we found similar timing in spontaneous bursts of activity in MMAN and HVC. Like HVC, MMAN responds to auditory playback of the bird's own song (BOS), but had little response to reversed BOS or conspecific song. Stimulation of MMAN resulted in evoked activity in HVC, indicating functional excitation from MMAN to HVC. However, inactivation of MMAN resulted in no consistent change in auditory responses in HVC. Taken together, these results indicate that MMAN provides functional excitatory input to HVC but does not provide significant auditory input to HVC in anesthetized animals. We hypothesize that MMAN may play a role in motor reinforcement or coordination, or may provide modulatory input to the song system about the internal state of the animal as it receives input from the hypothalamus.

Show MeSH
Related in: MedlinePlus