Quantal Duration of Auditory Memories

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Science  13 Dec 1996:
Vol. 274, Issue 5294, pp. 1909-1914
DOI: 10.1126/science.274.5294.1909


  • Fig. 1.

    Comparison of single-unit and multi-unit activity in caudal NCM in response to 100 iterations of a novel song. (A) Amplitude waveform of the conspecific song stimulus. (B) Sound spectrogram of the song in (A). (C) Raster of activity in a single unit (5); each dot represents the time of occurrence of an action potential, and each row represents one song presentation (sequence ordered from bottom to top). (D) Mean firing rate (spikes per second ± SE) (5) of the response elicited in the single unit shown in (C) over each group of 10 trials (filled circles) and normalized MUA amplitude (8) for each trial recorded at the same site (open circles). The MUA habituation rate at this site was 0.38 (Fig. 3) (8).

  • Fig. 2.

    (A) Examples of MUA responses to the first 100 presentations of a novel (solid symbols) and a familiar (open symbols) conspecific song at a single site in caudal NCM. MUA response amplitudes were normalized to the response on the first presentation of the novel or familiar song, respectively; the first response to the familiar song overlies that for the novel one. The bird had been trained with the familiar song 6 hours earlier. The habituation rates for the novel and familiar songs in this example were 0.42 and 0.16, respectively, and the corresponding best fit lines are plotted for each set of points (8). (B) Time course of spontaneous loss of habituation for conspecific song (200 iterations at an ISI of 11 s). Habituation rates (8) were measured at various training-to-testing intervals in 23 birds, with a total of 10 to 16 different songs per bird. The rates for novel songs are shown at time zero. The time from the onset of training until the time at which the habituation rates became not significantly different from the rates for novel song was used to define the duration of habituation (10).

  • Fig. 3.

    The protocol for studying the time course of habituation rates in NCM in a single bird. Training consisted of presenting sequentially 200 iterations of each of up to 16 novel stimuli (A to P) at an ISI of 11 s (total time for each stimulus = 36.7 min). Testing consisted of recording MUA during 100 presentations of each of these now familiar stimuli at an ISI of 11 s (which remained constant even if the ISI used in training was, as in some experiments, shorter or longer). In experiments that assessed spontaneous forgetting, stimuli were tested in the reverse order (P to A) to create a wide range of training-to-testing intervals during a single recording session in each bird (13). In those experiments that tested for the importance of RNA and protein synthesis in memory retention, a single dose of CYC or ACT was injected (arrow) into NCM at various delays after onset of training. Testing began 1 hour after injection, starting with the first song presented during training (A to P). This protocol yielded 16 different training-to-injection intervals for each bird tested.

  • Fig. 4.

    (A) Duration of long-term habituation differed among stimulus classes. The habituation rates (±SE) are plotted as a function of the training-to-testing interval. The loss of long-term habituation to these familiar stimuli occurred at distinct times characteristic of the stimulus class, with all exemplars of that class being forgotten at the same time. The longest memory durations are seen for conspecific songs and female calls. In the following sentence, the number after each stimulus class indicates the number of exemplars tested for that class: HUM (words from human speech), 7; CAN (canary song), 5; BEN (Bengalese finch song), 3; MC (male zebra finch long call), 6; FC (female zebra finch long call), 6; SG (zebra finch song), 16; reversed conspecific vocalizations: RMC, 6; RFC, 6; RSG, 16. Forty-nine birds were tested with these stimuli. (B) Duration of long-term habituation depended on the ISI. ISI was systematically varied during training from 3.5 to 54 s, with 200 sequential iterations of each conspecific song stimulus in a total of 58 birds; training time for each song ranged from 11.6 min to 3 hours. Testing was always done at an ISI of 11 s. Small increments in ISI produced large, step-like increases in the duration of long-term habituation. (C). Duration of long-term habituation depended on the number of stimulus iterations. The number of sequential presentations of each conspecific song was systematically varied during training from 30 to 1000, with an ISI of 11 s in 52 birds. Small increases in the number of iterations produced large, step-like increases in the duration of long-term habituation. In all curves, at least four birds are represented per time point within 2 hours (graphs on left) or 5 hours (graphs on right) on either side of a step change leading from remembered to forgotten.

  • Fig. 5.

    Sensitive periods when injections of CYC and ACT into NCM resulted in loss of stimulus-specific habituation. The habituation rates (3, 8) shown (mean ± SE) were plotted as a function of the interval between the onset of training with a particular song and the time of injection. CYC curve (red): data from 0.5 to 19.8 hours were obtained with protocol 1 (ISI = 11 s); data from 20 to 51 hours, with protocol 2 (ISI = 40 s) (see text). ACT curve (blue): data from 0.5 to 19 hours were obtained with protocols 1 and 2; data from 20 to 87 hours, with protocol 2. ACT spaced curve (green): data were obtained with protocol 3. Each point represents data from 3 to 10 birds, with a mean of four birds per point in each training protocol. Abbreviations: SAL, saline; CYC, massed training, CYC injection; ACT, massed training, ACT injection; ACT Spaced, spaced training (five songs, each played 200 times in four groups of 50 iterations; ISI = 11 s), ACT injection. See text for other details.

  • Fig. 6.

    Temporal correspondence between times when spontaneous forgetting occurred (Fig. 4) and times when RNA and protein synthesis were required for maintaining long-term habituation in different stimulation paradigms (Fig. 5). Duration of habituation is plotted for different classes of stimuli (left graph), different ISIs (middle), and numbers of iterations (right); all numeric scales are logarithmic. In each type of experiment, spontaneous forgetting occurred only at three to five fixed times. The dashed horizontal lines indicate the ends of periods when macromolecular synthesis was required for habituation to be maintained, as determined by injecting CYC and ACT. Abbreviations are as in Fig. 4A. All stimulus classes were trained with 200 repetitions at an ISI of 11 s, with the exception of SG40 (conspecific song, ISI = 40 s) and SSG (spaced training with four groups of 50 iterations of conspecific songs).