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Complementary control of sensory adaptation by two types of cortical interneurons.

Natan RG, Briguglio JJ, Mwilambwe-Tshilobo L, Jones SI, Aizenberg M, Goldberg EM, Geffen MN - Elife (2015)

Bottom Line: By selectively reducing responses to frequently, but not rarely, occurring sounds, auditory cortical neurons are thought to enhance the brain's ability to detect unexpected events through stimulus-specific adaptation (SSA).We found that two types of cortical interneurons differentially amplify SSA in putative excitatory neurons.A mutually coupled excitatory-inhibitory network model accounts for distinct mechanisms by which cortical inhibitory neurons enhance the brain's sensitivity to unexpected sounds.

View Article: PubMed Central - PubMed

Affiliation: Department of Otorhinolaryngology Head and Neck Surgery, Perelman School of Medicine, University of Pennsylvania, Philadelphia, United States.

ABSTRACT
Reliably detecting unexpected sounds is important for environmental awareness and survival. By selectively reducing responses to frequently, but not rarely, occurring sounds, auditory cortical neurons are thought to enhance the brain's ability to detect unexpected events through stimulus-specific adaptation (SSA). The majority of neurons in the primary auditory cortex exhibit SSA, yet little is known about the underlying cortical circuits. We found that two types of cortical interneurons differentially amplify SSA in putative excitatory neurons. Parvalbumin-positive interneurons (PVs) amplify SSA by providing non-specific inhibition: optogenetic suppression of PVs led to an equal increase in responses to frequent and rare tones. In contrast, somatostatin-positive interneurons (SOMs) selectively reduce excitatory responses to frequent tones: suppression of SOMs led to an increase in responses to frequent, but not to rare tones. A mutually coupled excitatory-inhibitory network model accounts for distinct mechanisms by which cortical inhibitory neurons enhance the brain's sensitivity to unexpected sounds.

No MeSH data available.


Related in: MedlinePlus

Local field potentials recorded in A1 exhibit SSA.(A) Representative peri-stimulus local field potentials (LFPs) across cortical layers. Top: mean response to deviant tones. Bottom: mean response to standard tones. Gray dashed lines indicate tone onset and offset. Green dashed lines indicate the margins between cortical layers. (B) Mean LFP collected from the thalamo-recipient granular layer, in response to standard (gray) and deviant (red) tones. Gray dashed lines indicate tone onset and offset.DOI:http://dx.doi.org/10.7554/eLife.09868.004
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fig1s1: Local field potentials recorded in A1 exhibit SSA.(A) Representative peri-stimulus local field potentials (LFPs) across cortical layers. Top: mean response to deviant tones. Bottom: mean response to standard tones. Gray dashed lines indicate tone onset and offset. Green dashed lines indicate the margins between cortical layers. (B) Mean LFP collected from the thalamo-recipient granular layer, in response to standard (gray) and deviant (red) tones. Gray dashed lines indicate tone onset and offset.DOI:http://dx.doi.org/10.7554/eLife.09868.004

Mentions: We first tested whether SSA is present in inputs from the thalamus. Current source density (CSD) analysis has been extensively used to quantify inputs from the thalamus (Metherate and Cruikshank, 1999; Kaur et al., 2005; Szymanski et al., 2009; Happel et al., 2014). We used a linear probe to record LFPs using electrodes spaced 50 microns apart inserted perpendicularly to brain surface in the primary auditory cortex. The multi-electrode probe is 775-µm long, spanning layers 1–6 of mouse A1. CSD is computed as the second spatial derivative of the LFPs across the depth of the cortex (Figure 1E, Figure 1—figure supplement 1A, 20 sessions, 15 mice). Typically, in response to tones, CSD exhibits a negative basin, termed sink, within a short delay of tone onset, localized to electrodes in thalamo-recipient layer (Figure 1F, Figure 1—figure supplement 1B) (Kaur et al., 2005; Szymanski et al., 2009). The amplitude of current in the sink was taken as a measure of the combined strength of post-synaptic inputs onto layer 4 neurons, which should reflect the strength of the thalamic inputs to the cortex (Metherate and Cruikshank, 1999; Kaur et al., 2005; Szymanski et al., 2009; Happel et al., 2014).


Complementary control of sensory adaptation by two types of cortical interneurons.

Natan RG, Briguglio JJ, Mwilambwe-Tshilobo L, Jones SI, Aizenberg M, Goldberg EM, Geffen MN - Elife (2015)

Local field potentials recorded in A1 exhibit SSA.(A) Representative peri-stimulus local field potentials (LFPs) across cortical layers. Top: mean response to deviant tones. Bottom: mean response to standard tones. Gray dashed lines indicate tone onset and offset. Green dashed lines indicate the margins between cortical layers. (B) Mean LFP collected from the thalamo-recipient granular layer, in response to standard (gray) and deviant (red) tones. Gray dashed lines indicate tone onset and offset.DOI:http://dx.doi.org/10.7554/eLife.09868.004
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4641469&req=5

fig1s1: Local field potentials recorded in A1 exhibit SSA.(A) Representative peri-stimulus local field potentials (LFPs) across cortical layers. Top: mean response to deviant tones. Bottom: mean response to standard tones. Gray dashed lines indicate tone onset and offset. Green dashed lines indicate the margins between cortical layers. (B) Mean LFP collected from the thalamo-recipient granular layer, in response to standard (gray) and deviant (red) tones. Gray dashed lines indicate tone onset and offset.DOI:http://dx.doi.org/10.7554/eLife.09868.004
Mentions: We first tested whether SSA is present in inputs from the thalamus. Current source density (CSD) analysis has been extensively used to quantify inputs from the thalamus (Metherate and Cruikshank, 1999; Kaur et al., 2005; Szymanski et al., 2009; Happel et al., 2014). We used a linear probe to record LFPs using electrodes spaced 50 microns apart inserted perpendicularly to brain surface in the primary auditory cortex. The multi-electrode probe is 775-µm long, spanning layers 1–6 of mouse A1. CSD is computed as the second spatial derivative of the LFPs across the depth of the cortex (Figure 1E, Figure 1—figure supplement 1A, 20 sessions, 15 mice). Typically, in response to tones, CSD exhibits a negative basin, termed sink, within a short delay of tone onset, localized to electrodes in thalamo-recipient layer (Figure 1F, Figure 1—figure supplement 1B) (Kaur et al., 2005; Szymanski et al., 2009). The amplitude of current in the sink was taken as a measure of the combined strength of post-synaptic inputs onto layer 4 neurons, which should reflect the strength of the thalamic inputs to the cortex (Metherate and Cruikshank, 1999; Kaur et al., 2005; Szymanski et al., 2009; Happel et al., 2014).

Bottom Line: By selectively reducing responses to frequently, but not rarely, occurring sounds, auditory cortical neurons are thought to enhance the brain's ability to detect unexpected events through stimulus-specific adaptation (SSA).We found that two types of cortical interneurons differentially amplify SSA in putative excitatory neurons.A mutually coupled excitatory-inhibitory network model accounts for distinct mechanisms by which cortical inhibitory neurons enhance the brain's sensitivity to unexpected sounds.

View Article: PubMed Central - PubMed

Affiliation: Department of Otorhinolaryngology Head and Neck Surgery, Perelman School of Medicine, University of Pennsylvania, Philadelphia, United States.

ABSTRACT
Reliably detecting unexpected sounds is important for environmental awareness and survival. By selectively reducing responses to frequently, but not rarely, occurring sounds, auditory cortical neurons are thought to enhance the brain's ability to detect unexpected events through stimulus-specific adaptation (SSA). The majority of neurons in the primary auditory cortex exhibit SSA, yet little is known about the underlying cortical circuits. We found that two types of cortical interneurons differentially amplify SSA in putative excitatory neurons. Parvalbumin-positive interneurons (PVs) amplify SSA by providing non-specific inhibition: optogenetic suppression of PVs led to an equal increase in responses to frequent and rare tones. In contrast, somatostatin-positive interneurons (SOMs) selectively reduce excitatory responses to frequent tones: suppression of SOMs led to an increase in responses to frequent, but not to rare tones. A mutually coupled excitatory-inhibitory network model accounts for distinct mechanisms by which cortical inhibitory neurons enhance the brain's sensitivity to unexpected sounds.

No MeSH data available.


Related in: MedlinePlus