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Frequency-specific adaptation and its underlying circuit model in the auditory midbrain.

Shen L, Zhao L, Hong B - Front Neural Circuits (2015)

Bottom Line: The adapted tuning was compared with the original tuning measured with an unbiased sequence.We found inhomogeneous changes in frequency tuning in IC, exhibiting a center-surround pattern with respect to the neuron's best frequency.These results suggest that frequency-specific adaptation in auditory midbrain can be accounted for by an adapted frequency channel and its lateral spreading of adaptation, which shed light on the organization of the underlying circuitry.

View Article: PubMed Central - PubMed

Affiliation: Department of Biomedical Engineering, School of Medicine, Tsinghua University Beijing, China.

ABSTRACT
Receptive fields of sensory neurons are considered to be dynamic and depend on the stimulus history. In the auditory system, evidence of dynamic frequency-receptive fields has been found following stimulus-specific adaptation (SSA). However, the underlying mechanism and circuitry of SSA have not been fully elucidated. Here, we studied how frequency-receptive fields of neurons in rat inferior colliculus (IC) changed when exposed to a biased tone sequence. Pure tone with one specific frequency (adaptor) was presented markedly more often than others. The adapted tuning was compared with the original tuning measured with an unbiased sequence. We found inhomogeneous changes in frequency tuning in IC, exhibiting a center-surround pattern with respect to the neuron's best frequency. Central adaptors elicited strong suppressive and repulsive changes while flank adaptors induced facilitative and attractive changes. Moreover, we proposed a two-layer model of the underlying network, which not only reproduced the adaptive changes in the receptive fields but also predicted novelty responses to oddball sequences. These results suggest that frequency-specific adaptation in auditory midbrain can be accounted for by an adapted frequency channel and its lateral spreading of adaptation, which shed light on the organization of the underlying circuitry.

No MeSH data available.


The magnitude of the adaptive change of the RF displayed a center-surround pattern. (A) Left: the profile of the change ratio of the responses at the adaptor (ΔRf = adaptor) with respect to the adaptor position. ΔRf = adaptor was normalized by the individual peak response of the non-adapted tuning. Middle and right: response at the adaptor frequency in the adapted condition against the original condition for each test (normalized by the individual peak response of original tuning) when the adaptor was in the center (middle panel) or on the flank of the RF (right panel). The mean value is indicated by a green cross. The number of tests showing increasing (gray) or decreasing (black) responses is annotated above or below the diagonal, respectively. (B) Left: the profile of the change ratio of the maximal response (ΔRpeak) with respect to the adaptor position. ΔRpeak was normalized by the individual maximal response of original tuning. Middle and right: the distributions of ΔRpeak when adaptors were in the center (middle panel) or on the flank (right panel). The numbers denote the number of tests with decreased (Dec.) and increased (Inc.) responses. (C) Left: the profile of the shift magnitude of the BF (ΔBF) with respect to the adaptor position. Positive values indicate repulsive shifts (Rep.) while negative values represent attractive shifts (Att.). Middle and right: the distributions of ΔBF when the adaptors were in the center (middle panel) or on flank of the RF (right panel). The numbers denote the number of tests with attractive and repulsive shifts. All error bars indicate the mean ± SE.
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Figure 3: The magnitude of the adaptive change of the RF displayed a center-surround pattern. (A) Left: the profile of the change ratio of the responses at the adaptor (ΔRf = adaptor) with respect to the adaptor position. ΔRf = adaptor was normalized by the individual peak response of the non-adapted tuning. Middle and right: response at the adaptor frequency in the adapted condition against the original condition for each test (normalized by the individual peak response of original tuning) when the adaptor was in the center (middle panel) or on the flank of the RF (right panel). The mean value is indicated by a green cross. The number of tests showing increasing (gray) or decreasing (black) responses is annotated above or below the diagonal, respectively. (B) Left: the profile of the change ratio of the maximal response (ΔRpeak) with respect to the adaptor position. ΔRpeak was normalized by the individual maximal response of original tuning. Middle and right: the distributions of ΔRpeak when adaptors were in the center (middle panel) or on the flank (right panel). The numbers denote the number of tests with decreased (Dec.) and increased (Inc.) responses. (C) Left: the profile of the shift magnitude of the BF (ΔBF) with respect to the adaptor position. Positive values indicate repulsive shifts (Rep.) while negative values represent attractive shifts (Att.). Middle and right: the distributions of ΔBF when the adaptors were in the center (middle panel) or on flank of the RF (right panel). The numbers denote the number of tests with attractive and repulsive shifts. All error bars indicate the mean ± SE.

Mentions: First, we investigated the relationship between the change in the adaptor response (ΔRf = adaptor) and the adaptor position (Figure 3A). The suppression of adaptor responses becomes gradually released when the adaptor moves away from the RF center, and turns into a slight increment when the adaptors are outside the RF (Figure 3A, left). To explore the distributions of response changes at the adapting frequency in the neural population, the adaptor response in each adapted tuning was plotted against that in the corresponding non-adapted tuning for the case of center adaptors (Figure 3A, middle) and flank adaptors (Figure 3A, right). Decreases were observed in the majority of the tests with center adaptors (91%, 352/387) and in the minority of tests with flank adaptors (41%, 95/232). The mean percentages of adaptor response change measured with biased ensemble relative to that measured with uniform ensemble were −34% and 175%, respectively (see the green crosses in Figure 3A right two panels).


Frequency-specific adaptation and its underlying circuit model in the auditory midbrain.

Shen L, Zhao L, Hong B - Front Neural Circuits (2015)

The magnitude of the adaptive change of the RF displayed a center-surround pattern. (A) Left: the profile of the change ratio of the responses at the adaptor (ΔRf = adaptor) with respect to the adaptor position. ΔRf = adaptor was normalized by the individual peak response of the non-adapted tuning. Middle and right: response at the adaptor frequency in the adapted condition against the original condition for each test (normalized by the individual peak response of original tuning) when the adaptor was in the center (middle panel) or on the flank of the RF (right panel). The mean value is indicated by a green cross. The number of tests showing increasing (gray) or decreasing (black) responses is annotated above or below the diagonal, respectively. (B) Left: the profile of the change ratio of the maximal response (ΔRpeak) with respect to the adaptor position. ΔRpeak was normalized by the individual maximal response of original tuning. Middle and right: the distributions of ΔRpeak when adaptors were in the center (middle panel) or on the flank (right panel). The numbers denote the number of tests with decreased (Dec.) and increased (Inc.) responses. (C) Left: the profile of the shift magnitude of the BF (ΔBF) with respect to the adaptor position. Positive values indicate repulsive shifts (Rep.) while negative values represent attractive shifts (Att.). Middle and right: the distributions of ΔBF when the adaptors were in the center (middle panel) or on flank of the RF (right panel). The numbers denote the number of tests with attractive and repulsive shifts. All error bars indicate the mean ± SE.
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Figure 3: The magnitude of the adaptive change of the RF displayed a center-surround pattern. (A) Left: the profile of the change ratio of the responses at the adaptor (ΔRf = adaptor) with respect to the adaptor position. ΔRf = adaptor was normalized by the individual peak response of the non-adapted tuning. Middle and right: response at the adaptor frequency in the adapted condition against the original condition for each test (normalized by the individual peak response of original tuning) when the adaptor was in the center (middle panel) or on the flank of the RF (right panel). The mean value is indicated by a green cross. The number of tests showing increasing (gray) or decreasing (black) responses is annotated above or below the diagonal, respectively. (B) Left: the profile of the change ratio of the maximal response (ΔRpeak) with respect to the adaptor position. ΔRpeak was normalized by the individual maximal response of original tuning. Middle and right: the distributions of ΔRpeak when adaptors were in the center (middle panel) or on the flank (right panel). The numbers denote the number of tests with decreased (Dec.) and increased (Inc.) responses. (C) Left: the profile of the shift magnitude of the BF (ΔBF) with respect to the adaptor position. Positive values indicate repulsive shifts (Rep.) while negative values represent attractive shifts (Att.). Middle and right: the distributions of ΔBF when the adaptors were in the center (middle panel) or on flank of the RF (right panel). The numbers denote the number of tests with attractive and repulsive shifts. All error bars indicate the mean ± SE.
Mentions: First, we investigated the relationship between the change in the adaptor response (ΔRf = adaptor) and the adaptor position (Figure 3A). The suppression of adaptor responses becomes gradually released when the adaptor moves away from the RF center, and turns into a slight increment when the adaptors are outside the RF (Figure 3A, left). To explore the distributions of response changes at the adapting frequency in the neural population, the adaptor response in each adapted tuning was plotted against that in the corresponding non-adapted tuning for the case of center adaptors (Figure 3A, middle) and flank adaptors (Figure 3A, right). Decreases were observed in the majority of the tests with center adaptors (91%, 352/387) and in the minority of tests with flank adaptors (41%, 95/232). The mean percentages of adaptor response change measured with biased ensemble relative to that measured with uniform ensemble were −34% and 175%, respectively (see the green crosses in Figure 3A right two panels).

Bottom Line: The adapted tuning was compared with the original tuning measured with an unbiased sequence.We found inhomogeneous changes in frequency tuning in IC, exhibiting a center-surround pattern with respect to the neuron's best frequency.These results suggest that frequency-specific adaptation in auditory midbrain can be accounted for by an adapted frequency channel and its lateral spreading of adaptation, which shed light on the organization of the underlying circuitry.

View Article: PubMed Central - PubMed

Affiliation: Department of Biomedical Engineering, School of Medicine, Tsinghua University Beijing, China.

ABSTRACT
Receptive fields of sensory neurons are considered to be dynamic and depend on the stimulus history. In the auditory system, evidence of dynamic frequency-receptive fields has been found following stimulus-specific adaptation (SSA). However, the underlying mechanism and circuitry of SSA have not been fully elucidated. Here, we studied how frequency-receptive fields of neurons in rat inferior colliculus (IC) changed when exposed to a biased tone sequence. Pure tone with one specific frequency (adaptor) was presented markedly more often than others. The adapted tuning was compared with the original tuning measured with an unbiased sequence. We found inhomogeneous changes in frequency tuning in IC, exhibiting a center-surround pattern with respect to the neuron's best frequency. Central adaptors elicited strong suppressive and repulsive changes while flank adaptors induced facilitative and attractive changes. Moreover, we proposed a two-layer model of the underlying network, which not only reproduced the adaptive changes in the receptive fields but also predicted novelty responses to oddball sequences. These results suggest that frequency-specific adaptation in auditory midbrain can be accounted for by an adapted frequency channel and its lateral spreading of adaptation, which shed light on the organization of the underlying circuitry.

No MeSH data available.