Stimulus-specific adaptations in the gaze control system of the barn owl

Abstract

Abrupt orientation to novel stimuli is a critical, memory-dependent task performed by the brain. In the present study, we examined two gaze control centers of the barn owl: the optic tectum (OT) and the arcopallium gaze fields (AGFs). Responses of neurons to long sequences of dichotic sound bursts comprised of two sounds differing in the probability of appearance were analyzed. We report that auditory neurons in the OT and in the AGFs tend to respond stronger to rarely presented sounds (novel sounds) than to the same sounds when presented frequently. This history-dependent phenomenon, known as stimulus-specific adaptation (SSA), was demonstrated for rare sound frequencies, binaural localization cues [interaural time difference (ITD) and level difference (ILD)] and sound amplitudes. The manifestation of SSA in such a variety of independent acoustic features, in the midbrain and in the forebrain, supports the notion that SSA is involved in sensory memory and novelty detection. To track the origin of SSA, we analyzed responses of neurons in the external nucleus of the inferior colliculus (ICX; the source of auditory input to the OT) to similar sequences of sound bursts. Neurons in the ICX responded stronger to rare sound frequencies, but did not respond differently to rare ITDs, ILDs, or sound amplitudes. We hypothesize that part of the SSA reported here is computed in high-level networks, giving rise to novelty signals that modulate tectal responses in a context-dependent manner.

Figure 1.

Example of an ITD tuning curve. A, Raster plot showing responses of a tectal unit to sounds with different ITD values. Stimulus duration was 50 ms (horizontal bar) starting at time 0 (vertical line). B, The average response per trial as a function of the ITD value. The best ITD value is designated by the black vertical line. Two ITD values of equal distances (±10 μs) from the best ITD (gray arrows) were selected to test for SSA in this neuron.

Figure 2.

Auditory stimuli used in the study. A, The oddball stimulus. Sequences of sounds were comprised of two sounds: stimulus 1 was presented frequently (with a probability of 0.85) and stimulus 2 was presented rarely. In the second block, the roles were reversed: stimulus 1 was rare and stimulus 2 was common. B, The constant order stimulus. Long sequences of sounds were comprised of 10 repetitions of stimulus 1 alternating with 10 repetitions of stimulus 2. The response to the first stimulus in a sequence of 10 (rare, gray circle) was compared with the response to the last stimulus in the sequence (common, black circle).

Figure 3.

Example of a single AGF site response to an ITD oddball stimulus. A, Dot raster showing 40 responses to stimulus 1 (ITD, −80 μs). The bottom 20 rows show responses to the rarely presented sound (embedded in a sequence of sounds with an ITD of −100 μs). The top 20 rows show randomly picked responses to the same sound presented frequently. B, The average response to stimulus 1 and stimulus 2 when common (black bars) are compared with the average response to the same stimuli when rare (gray bars). Error bars represent SE. C, D, Poststimulus time responses to stimulus 1 (C) and to stimulus 2 (D) are shown (lines are smoothed for display). Gray lines designate responses to the rare presentation; black lines designate responses to the common presentation. The shaded area indicates the onset and duration of sound stimulation. The arrowhead in D points to an inhibitory window not visible in the average response to rare stimuli.

Figure 4.

Summary of ITD oddball tests from all recording sites in the AGFs. A–C, Results are separated to ITD gaps smaller than 30 μs (A), between 40 and 60 μs (B), and larger than 60 μs (C). The left column presents the scatterplots of SI₁ versus SI₂. Gray points designate recordings from verified single units. The dashed lines mark the first quadrant, where both SIs are positive. The number of points above and below the diagonal line are shown in the bottom right corner. The middle column presents the histograms of the NIs distribution. The black vertical line marks the zero axis (NI, 0). The right column shows the population PSTHs normalized and averaged across all sites. Gray lines designate the population response to the rare stimulus and black lines designate the population response to the common stimulus. The bar in the top plot represents the duration of stimulation.

Figure 5.

Example of a single AGF site response to a frequency oddball test. A, Dot raster showing 40 responses to stimulus 1 (CF, 2 kHz). The bottom 20 rows show responses to the rarely presented sound (embedded in a sequence of sounds with a CF of 4 kHz). The top 20 rows show randomly picked responses to the same sound (CF, 2 kHz) frequently presented. B, The average response to stimulus 1 and stimulus 2 when common (black bars) are compared with the average response to the same stimuli when rare (gray bars). Error bars represent SE. C, D, Poststimulus time responses to stimulus 1 (C) and to stimulus 2 (D) are shown (lines are smoothed for display). Gray lines designate responses to the rare presentation; black lines designate responses to the frequent presentation. The shaded area indicates the onset and duration of sound stimulation.

Figure 6.

Summary of frequency oddball tests from all sites recorded in the AGFs. Results are shown for frequency gaps of 2 kHz. A, Scatterplot of SI₁ versus SI₂. Gray points designate recordings from verified single units. B, Histogram showing the distribution of NIs. C, PSTHs of the averaged normalized response to a rare stimulus (gray line) and to a frequent stimulus (black line). The format is as in Figure 4.

Figure 7.

Results from verified single-unit recordings in the AGFs. A, Normalized and averaged PSTHs of single unit responses to the frequency oddball test with frequency gaps of 2 kHz. B, Normalized and averaged PSTHs of single-unit responses to the ITD oddball test with ITD gaps of 20–60 μs. The average response to the rare stimulus is designated by the gray line and the average response to the common stimulus is designated by the black line. The bar in the left plot represents the duration of stimulation. The insets depict the histograms of the NIs distribution calculated from the population of single units. The black vertical line marks the zero axis (NI, 0). Both distributions significantly deviate from zero (t test, *p < 10⁻⁴).

Figure 8.

Summary of results from oddball tests in the OT. A, Scatterplot of SI₁ versus SI_2. of ITD oddball tests with 20–40 μs gaps between the ITD of stimulus 1 and stimulus 2. B, Scatterplot of SI₁ versus SI₂ obtained from frequency oddball tests with a 2 kHz gap between the center frequency of stimulus 1 and stimulus 2. The number of points above and below the diagonal line are shown in the bottom right corner. The dashed lines mark the first quadrant where both SIs are positive. All points represent multiunit recordings. The insets show the population average response to the stimulus that directly preceded a rare event (left bar) and to the first and second stimuli that immediately followed a rare event (middle bar and right bar, respectively). The gap in the histograms represents the position of the rare event in the sequence. The error bars designate the SE.

Figure 9.

Summary of the results from frequency constant order tests in the OT. Results from tests with frequency gaps of 660, 1330, and 2000 Hz are shown in A, B, and C respectively. Histograms in the left column show the population response (normalized and averaged across all recording sites) to the constant order sequence of 20 stimuli. The first 10 bars present responses to the stimuli with the lower CF (relative to the best frequency) and the last 10 bars present responses to the higher CF. Error bars indicate SEs. The SIs scatterplots are shown in the middle column. The number of points above and below the diagonal line are shown in the bottom right corner. Gray points designate recordings from single units. Insets depict the NI distributions. The abscissa of the NI histogram is between −0.2 and 0.55 in all histograms. The right column shows the population PSTHs, normalized and averaged. Gray lines designate the population response to the rare stimulus and black lines designate the population response to the common stimulus. The bar in the top plot represents the duration of stimulation.

Figure 10.

Summary of results from ITD constant order tests in OT. Results from constant order tests presented with an ITD gap of 20 μs are shown in A and results from tests with an ITD gap of 40 μs are shown in B. The format is as in Figure 8.

Figure 11.

Summary of results from frequency constant order tests in the ICX. A, The population response (normalized and averaged) to the constant order sequence with a frequency gap of 2 kHz. The first 10 bars present responses to the stimuli with the lower CF (relative to the best frequency) and the last 10 bars present responses to the higher CF. Error bars indicate SE. B, The NIs are shown versus the frequency gap used in the test. The line connects the average points at each frequency gap.

Figure 12.

Summary of results from ITD constant order tests in the ICX. A, Results from tests with ITD gaps of 20 μs. B, Results from tests with ITD gaps of 40 μs. Histograms in the left column show the population response (normalized and averaged across all recording sites) to the constant order sequence of 20 stimuli. The first 10 bars present responses to the stimuli with ITD values left of the best ITD and the last 10 bars present responses to ITD values right of the best ITD. Error bars indicate SEs. The NI distribution and the SIs scatterplots (insets) are shown in the middle column. The number of points above and below the diagonal line are shown in the top right and bottom left corners of the scatterplots, respectively. Right column shows the population PSTHs, normalized and averaged. Gray lines designate the population response to the rare stimulus and black lines designate the population response to the common stimulus. The bar in the top plot represents the duration of stimulation.

Figure 13.

Results of additional acoustic features in the OT and ICX. A, Population average response to a constant order sequence. The first 10 bars show the average responses to a sequence of sounds with low ABSI, the second 10 bars show the responses to a sequence of sounds with a higher ABSI (30 dB relative to the ABSI of the low sound). B, Scatterplot of SI₁ versus SI₂ of the same neurons as in A. The gray points designate recordings from single units. The inset shows the distribution of the NIs. The abscissa of the NI histogram is between −0.2 and 0.55 in all histograms. C, The population PSTHs, normalized and averaged, are shown for the rare stimulus (gray line) and for the frequent stimulus (black line). The responses to the low-intensity sound and to the high-intensity sound are shown separately in the top and bottom plots, respectively. D–F, Results from neurons in the ICX tested under the same stimulus conditions as in A–C. D, The population response to the constant order sequence. E, NI distribution and scatterplot of SIs. F, Population PSTH responses to rare (gray line) and frequent (black line) sound intensities. Responses to both low and high intensities are averaged together. G, Population response to a constant order sequence in which the ILD of the first 10 stimuli differed by 15 dB (toward contra lateral ear louder) from the ILD displayed in the second 10 stimuli. H, The scatterplot of SIs and the distribution of the NIs of all ILD tests. The gray points designate recordings from single units. I, The average response to rare (gray line) and frequent (black line) stimulus are shown separately for the louder contralateral ear (top plot) and the louder ipsilateral ear (bottom plot). J–L, Results from neurons in the ICX under the same stimulus conditions as in G–I.

Figure 14.

Summary of SSA effects in the ICX (left), OT (center), and AGFs (right). The error bars represent the average NI measured for frequency gaps of 2 kHz, ITD gaps of 40 μs, ABSI gaps of 30 dB, and ILD gaps of 15 dB. Error bars indicate the SE. Asterisks denote a significant deviation from zero (one-tailed, t test, p < 0.001; for all other cases p > 0.05).

Figure 15.

The onset of SSA effect in the OT. A, A close look at the time window starting 5 ms before and ending 40 ms after the onset of the stimulus is shown for the PSTHs from Figures 13C (ABSI, 30 dB gap), 9C (frequency, 2 kHz gap), 13I (ILD, 15 dB gap), and 10B (ITD, 40 μs gap). The top gray line shows the response to a rarely presented stimulus, the black line shows the response to a frequently presented stimulus, and the bottom gray line shows the difference between the two. The arrowheads indicate the stimulus onset. The black ticks present the latency of the population response to the frequent stimulus and the gray ticks present the latency of the difference signal. B, The stimulus indices versus the latencies to response are shown for frequency tests (top plot), ITD tests (middle plot), and ABSI tests (bottom plot). The horizontal lines designate the zero axes.