Cortical interneurons ensure maintenance of frequency tuning following adaptation

Natan, Ryan G.; Rao, Wei; Mn, Geffen

doi:10.1101/172338

Cited by 3 publications

(9 citation statements)

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“…The model accounted for observed experimental results including the differential role of SSTs and PVs in SSA [2], forward suppression [8], tuning-curve adaptation [7], and the effects of PV activation on feedforward functional connectivity [9]. We found that compensating currents between the two types of inhibitory neurons explain experimental findings of differential effects of their modulation on excitatory activity.…”

Section: Introductionmentioning

confidence: 73%

“…Specifically, SSTs, but not PVs facilitate stimulus-specific adaptation [2]. PVs and SSTs play distinct roles in adaptation to repeated tones along the frequency response function of the target neuron [7]. SSTs and PVs drive bi-directional effects on forward suppression [8].…”

Section: Introductionmentioning

confidence: 95%

“…Forward suppression (FWS) parameters from [8,22]. Tuning-curve adaptation (TCA) parameters from [7]. PV activation parameters from [9].…”

Section: Three-unit Rate Modelmentioning

confidence: 99%

“…Neurons in A1 adapt to repeated tones [2]. This adaptation is proportional to the strength of their tone-evoked responses: it is stronger in the center of the frequency response function, and weaker for the sidebands [7]. A recent study found that PVs and SSTs exert a differential effect on this form of adaptation: Suppressing PVs drives disinhibition selective to the sidebands in the adapted state, whereas suppressing SSTs drives disinhibition both in the center and at the sidebands of the frequency response function of excitatory neurons [7].…”

Section: Differential Adaptation To Repeated Tones Along the Frequencmentioning

confidence: 99%

“…This adaptation is proportional to the strength of their tone-evoked responses: it is stronger in the center of the frequency response function, and weaker for the sidebands [7]. A recent study found that PVs and SSTs exert a differential effect on this form of adaptation: Suppressing PVs drives disinhibition selective to the sidebands in the adapted state, whereas suppressing SSTs drives disinhibition both in the center and at the sidebands of the frequency response function of excitatory neurons [7]. To understand how inhibitory neurons affect adaptation across different frequency-tuned inputs, we presented a sequence of 8 tones at each frequency to generate adapting tuning curves (Fig 7A), and repeated this stimulus with PV and SST suppression for the model circuit.…”

Section: Differential Adaptation To Repeated Tones Along the Frequencmentioning

confidence: 99%

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A circuit model of auditory cortex

Park

Geffen

2020

PLoS Comput Biol

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The mammalian sensory cortex is composed of multiple types of inhibitory and excitatory neurons, which form sophisticated microcircuits for processing and transmitting sensory information. Despite rapid progress in understanding the function of distinct neuronal populations, the parameters of connectivity that are required for the function of these microcircuits remain unknown. Recent studies found that two most common inhibitory interneurons, parvalbumin-(PV) and somatostatin-(SST) positive interneurons control sound-evoked responses, temporal adaptation and network dynamics in the auditory cortex (AC). These studies can inform our understanding of parameters for the connectivity of excitatory-inhibitory cortical circuits. Specifically, we asked whether a common microcircuit can account for the disparate effects found in studies by different groups. By starting with a cortical rate model, we find that a simple current-compensating mechanism accounts for the experimental findings from multiple groups. They key mechanisms are twofold. First, PVs compensate for reduced SST activity when thalamic inputs are strong with less compensation when thalamic inputs are weak. Second, SSTs are generally disinhibited by reduced PV activity regardless of thalamic input strength. These roles are augmented by plastic synapses. These roles reproduce the differential effects of PVs and SSTs in stimulus-specific adaptation, forward suppression and tuning-curve adaptation, as well as the influence of PVs on feedforward functional connectivity in the circuit. This circuit exhibits a balance of inhibitory and excitatory currents that persists on stimulation. This approach brings together multiple findings from different laboratories and identifies a circuit that can be used in future studies of upstream and downstream sensory processing.

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Section: Introductionmentioning

confidence: 73%

Section: Introductionmentioning

confidence: 95%

“…Forward suppression (FWS) parameters from [8,22]. Tuning-curve adaptation (TCA) parameters from [7]. PV activation parameters from [9].…”

Section: Three-unit Rate Modelmentioning

confidence: 99%

Section: Differential Adaptation To Repeated Tones Along the Frequencmentioning

confidence: 99%

Section: Differential Adaptation To Repeated Tones Along the Frequencmentioning

confidence: 99%

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A circuit model of auditory cortex

Park

Geffen

2020

PLoS Comput Biol

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Neuroestrogens rapidly shape auditory circuits to support communication learning and perception: Evidence from songbirds

Vahaba

Remage‐Healey

2018

Hormones and Behavior

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Contribution to Special Issue on Fast effects of steroids. Steroid hormones, such as estrogens, were once thought to be exclusively synthesized in the ovaries and enact transcriptional changes over the course of hours to days. However, estrogens are also locally synthesized within neural circuits, wherein they rapidly (within minutes) modulate a range of behaviors, including spatial cognition and communication. Here, we review the role of brain-derived estrogens (neuroestrogens) as modulators within sensory circuits in songbirds. We first present songbirds as an attractive model to explore how neuroestrogens in auditory cortex modulate vocal communication processing and learning. Further, we examine how estrogens may enhance vocal learning and auditory memory consolidation in sensory cortex via mechanisms similar to those found in the hippocampus of rodents and birds. Finally, we propose future directions for investigation, including: 1) the extent of developmental and hemispheric shifts in aromatase and membrane estrogen receptor expression in auditory circuits; 2) how neuroestrogens may impact inhibitory interneurons to regulate audition and critical period plasticity; and, 3) dendritic spine plasticity as a candidate mechanism mediating estrogen-dependent effects on vocal learning. Together, this perspective of estrogens as neuromodulators in the vertebrate brain has opened new avenues in understanding sensory plasticity, including how hormones can act on communication circuits to influence behaviors in other vocal learning species, such as in language acquisition and speech processing in humans.

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Separate functional subnetworks of excitatory neurons show preference to periodic and random sound structures

Mehra

Mukesh

Bandyopadhyay

2021

Preprint

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Auditory cortex (ACX) neurons are sensitive to spectro-temporal sound patterns and violations in patterns induced by rare stimuli embedded within streams of sounds. We investigate the auditory cortical representation of repeated presentations of sequences of sounds with standard stimuli(common) with an embedded deviant (rare) stimulus in two conditions-Periodic (Fixed deviant position) or Random (Random deviant position), using extracellular single-unit and 2-photon Ca+2 imaging recordings in Layer 2/3 neurons of the mouse ACX. In the population average, responses increased over repetitions in the Random-condition and were suppressed or did not change in the Periodic-condition, showing irregularity preference. A subset of neurons also showed the opposite behavior, indicating regularity preference. Pairwise noise correlations were higher in Random-condition over Periodic-condition, suggesting the role of recurrent connections. 2-photon Ca+2 imaging of excitatory (EX) and parvalbumin-positive (PV) and somatostatin-positive (SOM) inhibitory neurons, showed different categories of adaptation or change in response over repetitions (categorized by the sign of the slope of change) as observed with single units. However, the examination of functional connectivity between pairs of neurons of different categories showed that EX-PV connections behaved opposite to the EX-EX and EX-SOM pairs that show more functional connections outside category in Random-condition than Periodic-condition. Finally considering Regularity preference, Irregularity preference and no preference categories, showed that EX-EX and EX-SOM connections to be in largely separate functional subnetworks with the different preferences, while EX-PV connections were more spread. Thus separate subnetworks could underlie the coding of periodic and random sound sequences.

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Cortical interneurons ensure maintenance of frequency tuning following adaptation

Cited by 3 publications

References 59 publications

A circuit model of auditory cortex

A circuit model of auditory cortex

Neuroestrogens rapidly shape auditory circuits to support communication learning and perception: Evidence from songbirds

Separate functional subnetworks of excitatory neurons show preference to periodic and random sound structures

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