Behavioral state modulation of auditory activity in a vocal motor system

Science

Volumn 282, Issue 5397, 1998, Pages 2250-2254

  Dave, Amish S ^a   Yu, Albert C ^a   Margoliash, Daniel ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NORADRENALIN;

ANIMAL BEHAVIOR; ARTICLE; AUDITORY NERVOUS SYSTEM; AUDITORY RESPONSE; BIRD; BRAIN REGION; FEEDBACK SYSTEM; MOTOR PERFORMANCE; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; SENSORIMOTOR FUNCTION; SINGING; SLEEP; VOICE;

ACOUSTIC STIMULATION; ANESTHESIA; ANIMALS; AUDITORY PATHWAYS; FEEDBACK; LEARNING; MALE; MOTOR NEURONS; NEURAL PATHWAYS; NEURONS; NOREPINEPHRINE; PROSENCEPHALON; SLEEP; SONGBIRDS; VOCALIZATION, ANIMAL;

ANIMALIA; AVES; FRINGILLIDAE; TAENIOPYGIA GUTTATA;

EID: 0032545361     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.282.5397.2250     Document Type: Article

References (50)

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14. Techniques for unit recordings in freely moving songbirds have been described elsewhere [A. S. Dave, A. C. Yu, J. J. Gilpin, D. Margoliash, in Methods for Simultaneous Neuronal Ensemble Recordings, M. Nicolelis, S. Simon, J. Corless, Eds. (CRC Press, Boca Raton, FL, in press)]. Single or multiple units were obtained by manually turning a screw to advance the mechanical microdrive while the bird was restrained, releasing the bird, and recording ongoing, auditory and vocal premotor activity. Except where noted otherwise, isolated birds were induced to sing by broadcasting female calls (25). Song stimuli were broadcast while birds were quiescent (not vocalizing, beak-wiping, pecking, or hopping excessively) but apparently alert and attentive, perched with eyes open, and making occasional small head or eye movements in response to sounds. Any neuronal record to broadcast song that was preceded or followed within 30 s by singing was discarded. In a second paradigm, recordings commenced at nighttime. After obtaining a stable multiunit signal, the bird was released into the dark cage. BOS was presented every 30 s throughout the night and following day, while recording neuronal signals and vocalizations. Daytime videotape recordings facilitated visual assessment of the bird's activity.
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22. Responses were computed as the percentage of change in the average spiking rate during the stimuli (typically 30 repetitions) relative to the ongoing rate. Ongoing rates were computed from long (≈300 s) records. Of 29 HVc single units (19 sites, seven birds) that exhibited premotor activity in relation to singing, 19 also responded to broadcast sounds. When those neurons were presented with BOS and reversed BOS (REV) (N = 19 units, 13 recording sites, six birds) or BOS and conspecific songs (CON) (N = 13 units, six recording sites, two birds), they exhibited much stronger responses to BOS (BOS > REV: paired t = 3.42, df = 18, P < 0.004; BOS > CON: paired t = 4.14, df = 12, P < 0.002). In contrast, no RA neurons recorded under the same conditions exhibited any statistically significant response to BOS (N = 28 SU, 33 recording sites, four birds).
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24. RA activity was recorded from one adult (> PHD 150) (three sites, 3 days), from a PHD 59 to 69 juvenile (four sites, 4 days), and from a PHD 58 to 81 juvenile (eight sites, 7 days). BOS was presented at 30-s intervals starting 3.8 to 8.0 hours before light onset and thereafter throughout the day (6). Multiunit responses were averaged for each 20 repetitions (1-ms bins), and then the mean of the ongoing activity (the average over 2 to 5 s starting 1 s after stimulus offset) was subtracted. At each site, the presence of an auditory response during sleep or wakefulness was determined by comparing distributions (t tests) of the RMS values calculated over the duration of BOS and during ongoing activity. By this measure, 14/14 sites showed auditory activity during sleep (P≤0.0054), and 8/14 sites (3/3 birds) showed auditory activity during wakefulness (P<0.05) (data from one site were lost).
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26. Firing rates were estimated from peristimulus time histograms (PSTHs) with 50-ms bins. The strength of response was quantified from the PSTH as the ratio of the variance in firing rate during stimulus presentation over the variance in ongoing activity beginning 1 s after the stimulus offset. This measure is sensitive to slight stimulus-driven changes in temporal patterns of spike trains. Nevertheless, 33 recordings sites (28 single units, 15 multiunits) from four adult awake, freely moving birds gave a response strength for BOS of 1.00 ± 0.40 (1 = no response). In contrast, 72 recording sites (71 single units, 33 multiunits) from 12 urethane-anesthetized birds gave a response strength for BOS of 18.71 ± 33.81. This difference was significant (Mann-Whitney U, Z = -9.004, P < 0.0001). Twenty-two recordings sites (14 single units, 15 multiunits) from five awake but restrained birds gave a response strength for BOS of 2.77 ± 2.62. In only one awake-restrained bird were most sites auditory (six single units, six multiunits, seven sites). One of the animals with chronic head-gear and two of the awake-restrained animals were subsequently anesthetized, resulting in average increases in response strength of 111, 1860. and 634%.
27. In awake animals, the distribution of interspike intervals (ISIs) of ongoing activity of RA single units had a single mode corresponding to the mean of the regular pattern of firing. In anesthetized animals, ISI distributions typically had two modes, a long-interval (major) mode reflecting the regular firing pattern and a short-interval (minor) mode reflecting the complex bursts. The major mode was fit with a Gaussian, and then the Gaussian was subtracted from the data. The number of residual intervals from 0 to the Gaussian mean -2 SD, as a percentage of the total number of intervals, was taken as the index of bursting. With these procedures, 29 recording sites (33 single units) from five awake, freely moving animals had average ISIs of 30.7 ± 7.4 ms (32.6 Hz) for the major mode. The irregularity of firing for the major mode was 5.6 ± 4.9 ms (determined from the distribution of SD from the Gaussians). In contrast, data from 60 recording sites (68 single units) from 12 urethane-anesthetized birds resulted in an average ISI of 98.9 ± 32.6 ms (10.1 Hz) for the major mode. The irregularity of firing for the major mode was 20.9 ± 17.2 ms. These differences are significant (average ISI: Z = -8.095, P < 0.0001; irregularity: Z = -6.774, P < 0.0001). The index of bursting was 7.5 ± 83% for data from awake animals and significantly higher at 12.8 ± 7.4% from urethane-anesthetized birds (Z = -3.724. P < 0.0003).
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32. For NE injections into RA, the mean of the major mode of the ISI distributions for RA neurons decreased significantly from 98.7 ± 34.7 ms before injections to 63.1 ± 22.0 ms after injections (Z = -3.842, P < 0.0002). The SD of the major mode also decreased significantly from 16.2 ± 16.8 to 3.6 ± 2.3 ms (Z = -6.308, P < .0001), indicating an increase in the regularity of firing. The burstiness changed from 17.1 ± 8.9 to 14.0 ± 52%; this change was not significant (Z = -1.146, P = 0.2516). For NE injections into HVc, all three measures of RA ongoing activity changed significantly (P < 0.05) (mean ISI: 123.0 ± 26.9 to 102.4 ± 24.0 ms; irregularity: 29.0 ± 20.9 to 16.3 ± 15.6 ms; bursting; 14.3 ± 7.5 to 9.5 ± 5.7%).
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50. All procedures were approved by an institutional animal care and use committee. Supported by grants from the Whitehall Foundation, NIH (NS25677), and the Brain Research Foundation. A.S.D. and A.C.Y. were supported by NIH predoctoral fellowships.