Quantal duration of auditory memories

Science

Volumn 274, Issue 5294, 1996, Pages 1909-1914

  Chew, Sek Jin ^a,b   Vicario, David S ^a   Nottebohm, Fernando ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b SINGAPORE NATIONAL EYE CENTRE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; AUDITORY MEMORY; BIRD; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HABITUATION; MALE; NEOSTRIATUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SINGLE UNIT ACTIVITY; STIMULUS RESPONSE; VOCALIZATION;

ACOUSTIC STIMULATION; ANIMALS; BIRDS; CYCLOHEXIMIDE; DACTINOMYCIN; FEMALE; GENE EXPRESSION; HABITUATION, PSYCHOPHYSIOLOGIC; MALE; MEMORY; NEOSTRIATUM; NEURONAL PLASTICITY; NEURONS; PROTEIN BIOSYNTHESIS; RNA; TIME FACTORS; VOCALIZATION, ANIMAL;

ANIMALIA; AVES; FRINGILLIDAE; TAENIOPYGIA GUTTATA;

EID: 2642670471     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.274.5294.1909     Document Type: Article

References (31)

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3. S. J. Chew, C. V. Mello, F. Nottebohm, E. D. Jarvis, D. S. Vicario, Proc. Natl. Acad. Sci. U.S.A. 92, 3406 (1995).
4. G. E. Vates, B. M. Broome, C. V. Mello, F. Nottebohm, J. Comp. Neurol. 366, 613 (1996).
5. Zebra finches (97 male and 96 female) obtained from our breeding colony were prepared for long-term recording as described (3). Auditory stimuli (11) were played from a speaker placed 0.5 m from the bird in a soundproof experimental chamber (3, 12). During training the bird was freely moving; electrophysiological recording was carried out in awake, restrained birds. Insulated tungsten microelectrodes were used to record physiological activity in the right or left caudal NCM at sites that exhibited habituation to novel songs (3). Recording sessions lasted ∼5 hours. All procedures conformed to an animal use protocol approved by the Rockefeller University Animal Care and Use Committee. The auditory stimulus and microelectrode data were digitized at 20 kHz. Single-unit action potential waveforms were digitally discriminated and displayed as rasters (Experimenters Workbench, Dataware). Single-unit responses were quantified by averaging the firing rate during the stimulus period (plus the ensuing 100 ms) and then subtracting the firing rate during the control period (500 ms preceding stimulus onset). This mean firing rate per presentation was used to produce averages, for example, of 10 successive presentations (Fig. 1D) or of the first 50 presentations.
6. Birds that had heard the testing stimulus earlier had been exposed to 200 repetitions thereof at an ISI of 11 s; testing also occurred at an ISI of 11 s.
7. Single units are difficult to "hold" with a recording electrode for periods of more than 30 min. Therefore, most of this study was done with MUA data.
8. The multi-unit response amplitude to each stimulus presentation was calculated by subtracting the rootmean-square (rms) value over the 500-ms preceding stimulus onset from the rms over the period from stimulus onset to offset plus 100 ms. The difference between the two root-mean-square values measures the net response per unit time and corrects for differences in duration between stimuli. Each amplitude was then normalized to the response amplitude on the first presentation (typically the largest) and plotted as a function of stimulus iteration. We used the least-squares method to determine the slope of the straight line that best fitted each set of 100 normalized responses to a stimulus that the bird had or had not heard during an earlier training session. The habituation rate was defined as the absolute value of the slope of the best-fit line (Fig. 2A). Habituation rates were independent of the absolute response level at any given site and so could be used to compare different sites, in different birds, recorded at different intervals after training. We have previously shown that the distributions of habituation rates to novel and familiar songs differ significantly (3). Figure 2A demonstrates, too, that habituation to the familiar song occurred, typically, during the first few repetitions of the stimulus, after which responses stayed at a lower level; it took longer for this lower level to be reached by responses to a novel song.
9. All statistical comparisons were done with the Student's t tast (P < 0.05. two-tailed).
10. The distribution of entries in Fig. 2B suggests that, even though there was a relatively abrupt change in habituation rate between 46 and 48 hours, a less marked drift toward higher habituation rates occurred between 15 and 46 hours after onset of training. Our stringent criterion for forgetting - habituation rates similar to those induced by presentations of a novel song - did not recognize these changes, which may, however, represent an early forgetting stage that deserves further study.
11. Those sounds, which provided a set of conspecific and heterospecific stimuli that the birds had not previously heard, were digitized at 20 kHz (Signal, Engineering Design). The songs and words from human speech were 1.2 to 2.0 s long, and calls were 100 to 400 ms long.
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16. Seventeen birds were trained with 200 iterations (massed) each of two songs, followed by 50 iterations of each of five other songs, and this latter spaced protocol was repeated four times. At an ISI of 11 s, the spaced-training part of this protocol took 3 hours. Another two songs were then played with the massed-training paradigm. The total duration of this protocol was 5.5 hours. In a second version of this protocol, birds (n = 8) were trained with 50 iterations (massed training: ISI = 11 s, total training time = 9.2 min) of each of two novel songs; this was then followed by 10 iterations of each of a group of five other novel songs, and the latter sequence was repeated five times (spaced training: ISI = 11 s, total training time = 46 min). We then played another three songs using the massed-training paradigm. Thus, in 1.5 hours, we exposed the bird to 50 iterations of five songs presented in the massed-training paradigm, and 50 iterations of five songs presented in the spaced-training paradigm.
17. When a total of 50 iterations of each song were used, habituation was lost after only 7 hours for songs presented in the massed-training manner (Fig. 4C), but spaced training (16) produced habituation that persisted for at least 43 hours (14).
18. Five zebra finches that were trained with canary song presented in a spaced paradigm heard four groups of 50 iterations for each of five stimuli, for a total of 200 iterations for each stimulus; this training was compared with 200 massed iterations for a same canary song.
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22. ACT (40 nl, 50 μM) or CYC (40 nl, 1 ng/nl), dissolved in saline, was injected into 46 adult male or female zebra finches into a right- or left-hemisphere NCM recording sue that exhibited habituation to novel songs. These injectons were made with a glass micropipette (tip outer diameter, 20 μm). As a control, saline vehicle alone was injected into the other hemisphere. The effective sphere of the ACT or CYC injections, as determined by immunocytochemistry, was limited to a subregion of NCM (3). Such injections did not affect auditory responses or the immediate habituation of NCM neurons to playbacks of a novel song. The physiological effect of these RNA and protein synthesis blockers in NCM was reversed in <1 hour, as determined by the loss of long-term habituation for stimuli presented 0.5 hour, but not 1 hour, after injection [S. J. Chew, thesis, Rockefeller University (1966)], allowing for a fairly accurate pinpointing of the time when gene expression or protein synthesis is necessary for the maintenance of long-term habituation. The side of drug injection was alternated in successive experiments to eliminate side-to-side biases in injection or recording technique. Starting 1 hour after drug injection, insulated tungsten microelectrodes were used to record physiological activity at the injection sites. Comparison of simultaneous recordings in the two sides controlled for nonspecific effects or drug diffusion and for the particular songs used in any given experiment. The two sides were previously shown not to differ in habituation rates (13). Test stimuli were presented in the same order as during training, starting 1 hour after injection.
23. The presence and duration of the first sensitive period was not established with protocols 2 and 3 because training with a single song with either of these protocols lasted 2.2 and 2.4 hours. The second, third, and fourth sensitive periods during which injections of ACT or CYC in NCM blocked long-term habituation were very similar, regardless of whether we used protocols 1, 2, or 3 . In addition, protocols 2 and 3 revealed a fifth and sixth sensitive period of mnemogenic RNA and protein synthesis, while retaining those that had occurred earlier (Fig. 5).
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29. This effect was noticed, for example, when testing 10 or 24 hours after onset of training in birds that received injections of blockers at 0.5 to 3 or 14 to 15 hours, respectively.
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31. We thank S. Creel, R. Desimone, C. Gilbert, N. Heintz, M. E. Nottebohm, M. Young, J. Wallman, T. Wiesel, and two anonymous reviewers for their helpful comments on the manuscript, and N. Naqvi for help with the single-unit analysis. Supported by PHS grants MH18343 (F.N.) and MH40900 (D.S.V.) and by the Herbert Singer and the Mary Flagler Cary Charitable Trust.