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Cited by 458Neuroscience and Neuropharmacology ResearchNeural dynamics and brain functionMemory and Neural Mechanisms

Plasticity of Cortical Excitatory-Inhibitory Balance

Open access
Froemke, Robert C.·2015·Annual Review of Neuroscience
DOI 10.1146/annurev-neuro-071714-034002PMC PMC4652600
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Abstract

Synapses are highly plastic and are modified by changes in patterns of neural activity or sensory experience. Plasticity of cortical excitatory synapses is thought to be important for learning and memory, leading to alterations in sensory representations and cognitive maps. However, these changes must be coordinated across other synapses within local circuits to preserve neural coding schemes and the organization of excitatory and inhibitory inputs, i.e., excitatory-inhibitory balance. Recent studies indicate that inhibitory synapses are also plastic and are controlled directly by a large number of neuromodulators, particularly during episodes of learning. Many modulators transiently alter excitatory-inhibitory balance by decreasing inhibition, and thus disinhibition has emerged as a major mechanism by which neuromodulation might enable long-term synaptic modifications naturally. This review examines the relationships between neuromodulation and synaptic plasticity, focusing on the induction of long-term changes that collectively enhance cortical excitatory-inhibitory balance for improving perception and behavior.

AI snapshot

Written from the paper’s full text.

TL;DR

This review argues that cortical neuromodulators—acetylcholine, noradrenalin, oxytocin, and others—transiently reduce inhibition to gate long-term excitatory and inhibitory plasticity, after which inhibitory tuning is adjusted to restore excitatory-inhibitory balance. It synthesizes in vitro and in vivo evidence, especially from auditory cortex, linking disinhibition to receptive-field shifts and improved perception.

Key findings

  • Neuromodulators share a disinhibitory mode of action: nucleus basalis acetylcholine decreases tone-evoked inhibition, locus coeruleus noradrenalin decreases tonic inhibition, and oxytocin reduces call-evoked inhibition. Acetylcholine pairing shifts excitatory tuning within minutes, with inhibitory tuning matching over 1–3 h; noradrenalin pairing can increase responses up to tenfold; oxytocin enhancement is followed after 1 h by increased and temporally restructured inhibition.
  • Excitatory plasticity rules include LTP induced by brief (~1-s) trains above 20 Hz and LTD by sustained 1 Hz stimulation for several minutes; STDP induces LTP when postsynaptic spikes follow presynaptic activation within 10 ms and LTD when postsynaptic spikes precede presynaptic spiking by 10–100 ms. Heterosynaptic LTD can occur within approximately 10 min after LTP induction and dynamically targets the original best stimulus if it is presented.
  • Excitatory-inhibitory balance is present globally at hearing onset, but fine-scale balance emerges over the first postnatal month and requires sensory experience. In rats, patterned tone exposure between P9 and P11 produced persistent overrepresentation of the exposed frequency, whereas later exposure at P14+ failed to affect tonotopic maps.
  • Pairing barely perceptible 4 kHz tones with nucleus basalis stimulation improved go/no-go behavioral performance for several hours, even when pairing occurred under anesthesia; without further pairing or reinforcement, tuning shifts and behavioral improvements returned to baseline after a few hours.

Methods

  • Narrative review; no new primary experimental data are reported.
  • Synthesizes published in vitro slice and in vivo recording studies across auditory, visual, barrel cortex, hippocampus, and amygdala, including whole-cell voltage-clamp, field potentials, behavioral tasks, and pharmacological/optogenetic neuromodulation.
  • Main analysis is a conceptual synthesis of neuromodulation, disinhibition, BCM/STDP rules, heterosynaptic and inhibitory plasticity, and cortical excitatory-inhibitory balance.

Limitations

  • Stated: the paper notes that it remains unclear how cellular LTP/LTD relate to learning and memory; much less is known about heterosynaptic and inhibitory plasticity in vivo; how induction procedures relate to natural activity is unclear; how cortical neurons regain original tuning after pairing is unclear; little is known about how hypothalamic peptides contact cortical circuits or which auditory cortex elements express oxytocin receptors; and dopamine’s synaptic mechanisms for receptive-field plasticity remain to be determined.
  • Evident: as a review, it does not use a systematic search or meta-analysis, and its evidence base is selective and heavily weighted toward auditory cortex. Many mechanistic findings come from slices or anesthetized preparations, which may not fully capture awake, behaving circuit dynamics.

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Integrity signals

Registry

Crossref · 10.1146/annurev-neuro-071714-034002

Cites

175 of 175 references verified0 citation errors · 0 not checkable

Statistics

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Claims the paper makes

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  • Findingown data

    The experimentally determined inhibitory STDP window is similar but not identical to that used by Vogels et al. (2011).

    “The shape of the experimentally determined inhibitory STDP window (Figure 1b) is similar but not identical to that used by Vogels et al. (2011), although several different formulations of inhibitory STDP learning rules can have similar functional consequences, in terms of calibrating or balancing inhibition with excitation and controlling overall network excitability (Luz & Shamir 2012).”
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    • cites Vogels et al. 2011

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  • Findingcitation

    Repetitive nucleus basalis pairing shifts excitatory tuning curves within several minutes, followed by a delayed change in inhibitory tuning.

    “We examined the synaptic basis for these changes in cortical frequency tuning curves with in vivo voltage-clamp recordings from deeper layer neurons and found that repetitive nucleus basalis pairing shifted excitatory tuning curves within several minutes, followed by a delayed change in inhibitory tuning (Froemke et al. 2007, 2013).”
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  • Findingcitation

    Over 1-3 h, inhibitory tuning eventually matches the new profile of excitation, recovering the fine-scale balance of excitation and inhibition.

    “Over 1–3 h, inhibitory tuning eventually matched the new profile of excitation, recovering the fine-scale balance of excitation and inhibition (Figure 3a–d).”
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  • Findingcitation

    The persistent changes in cortical inputs after nucleus basalis pairing depend on NMDA receptor activation.

    “these changes depended on NMDA receptor activation (Froemke et al. 2013)”
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  • Findingcitation

    Pairing target tones with nucleus basalis stimulation for a few minutes under anesthesia still produces lasting gains in perceptual abilities for several hours after recovery.

    “Importantly, we could pair target tones with nucleus basalis stimulation for a few minutes when animals were anesthetized and still observed lasting gains in perceptual abilities for several hours after animals recovered (Froemke et al. 2013).”
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    Findingown data

    The process of inhibitory re-balancing after nucleus basalis pairing requires sensory experience, as keeping animals in silence prevents inhibition from re-balancing excitation.

    “This process required sensory experience, as keeping animals in silence prevented inhibition from re-balancing excitation.”
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    Findingcitation

    Cortical but not thalamic inputs are changed persistently by nucleus basalis pairing.

    “cortical but not thalamic inputs were changed persistently by nucleus basalis pairing (Froemke et al. 2007)”
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    Premisecitation

    Inhibitory synapses are plastic and are controlled directly by a large number of neuromodulators, particularly during episodes of learning.

    “Recent studies indicate that inhibitory synapses are also plastic and are controlled directly by a large number of neuromodulators, particularly during episodes of learning.”
    • Also stated in: § Inhibitory Plasticity · boosted
      “Over the past decade, numerous studies have shown that inhibitory synapses themselves are also plastic.”
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    Premisecitation

    We are still far from understanding how cellular phenomena like LTP and LTD relate to learning, memory, and other cognitive processes.

    “Despite these advances, we are still far from understanding how cellular phenomena like LTP and LTD relate to learning, memory, and other cognitive processes (Cahill et al. 2001, Martin et al. 2000, Thompson 2005).”
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    Premisecitation

    Most studies of long-term synaptic plasticity have focused on LTP and LTD of specific excitatory synapses onto excitatory neurons in the hippocampus and neocortex.

    “Most studies of long-term synaptic plasticity have focused on long-term potentiation (LTP) and long-term depression (LTD) of specific excitatory synapses onto excitatory neurons in the hippocampus and neocortex (Bliss & Collingridge 1993).”
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    Premisecitation

    Much is known about the induction of excitatory plasticity in terms of the spike rates and precise spike timing required for LTP or LTD.

    “Much is now known about the induction of excitatory plasticity, in terms of the spike rates and precise spike timing required for LTP or LTD (Bi & Poo 1998, Bienenstock et al. 1982, Froemke et al. 2006, Kirkwood et al. 1993, Sjöström et al. 2001), as well as the mechanisms by which these long-term changes are expressed (Feldman 2009, Malenka & Nicoll 1999).”
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    Premisecitation

    LTP and LTD are classically induced by changes in presynaptic input firing rate, with brief (~1-s) trains of high-frequency stimulation above 20 Hz generally inducing LTP, whereas sustained low-frequency stimulation (1 Hz for several minutes) induces LTD.

    “Classically, LTP and LTD are induced by changes in presynaptic input firing rate, with brief (approximately 1-s) trains of high-frequency stimulation above 20 Hz generally inducing LTP, whereas sustained low-frequency stimulation (1 Hz for several minutes) induces LTD (Bliss & Collingridge 1993, Bliss & Lømo 1973, Kirkwood et al. 1993).”
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    Premisereasoning

    STDP learning rules appear to be much more heterogeneous across different synapses and systems when three or more spikes occur in a short period of time or when synapses are physically located further in the dendrites from the site of axosomatic action potential generation.

    “However, STDP learning rules appear to be much more heterogeneous across different synapses and systems when three or more spikes occur in a short period of time or when synapses are physically located further in the dendrites from the site of axosomatic action potential generation.”
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    Premisecitation

    At most excitatory connections, spike timing-dependent LTP is induced when postsynaptic spikes reliably follow presynaptic activation within 10 ms, whereas timing-dependent LTD is induced when postsynaptic spikes occur first before presynaptic spiking by 10-100 ms.

    “Specifically, at most excitatory connections, spike timing– dependent LTP is induced when postsynaptic spikes reliably follow presynaptic activation within 10 ms, whereas timing-dependent LTD is induced when postsynaptic spikes occur first before presynaptic spiking by 10–100 ms (Bell et al. 1997, Bi & Poo 1998, D’amour & Froemke 2015, Debanne et al. 1994, Feldman 2000, Froemke and Dan 2002, Markr”
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    Premisenone given

    The hallmark of STDP is a relatively brief time window on the order of tens of milliseconds by which paired pre- and postsynaptic spiking determines the sign and magnitude of long-term synaptic modification.

    “The hallmark of STDP is a relatively brief time window on the order of tens of milliseconds by which paired pre- and postsynaptic spiking determines the sign and magnitude of long-term synaptic modification (Figure 1a).”
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    Premisecitation

    These stimulus patterns depolarize postsynaptic neurons, allowing for NMDA receptor activation and postsynaptic Ca2+ increases, which are sufficient to induce either LTP or LTD in a manner that depends on the duration and amplitude of Ca2+ influx.

    “In terms of mechanism, these stimulus patterns depolarize postsynaptic neurons, allowing for N-methyl-D-aspartate (NMDA) receptor activation and postsynaptic Ca2+ increases, which are sufficient to induce either LTP or LTD in a manner that depends on the duration and amplitude of Ca2+ influx (Froemke et al. 2005, Nishiyama et al. 2000, Yang et al. 1999).”
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    Premisecitation

    GABAergic inhibition keeps NMDA receptors nominally in check, and transient reduction of inhibition is an effective means for gating plasticity in response to electrical or sensory stimulation.

    “GABAergic inhibition keeps NMDA receptors nominally in check, and transient reduction of inhibition is an effective means for gating plasticity in response to electrical or sensory stimulation (Artola et al. 1990, Chun et al. 2013, Froemke et al. 2007, Kuhlman et al. 2013).”
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    Premisecitation

    Increases of activity in cultured cortical neurons by prolonged disinhibition led to a decrease in miniature excitatory postsynaptic current (mEPSC) amplitude and a normalization of firing rates after 48 h.

    “Specifically, Turrigiano et al. (1998) showed that increases of activity in cultured cortical neurons by prolonged disinhibition led to a decrease in miniature excitatory postsynaptic current (mEPSC) amplitude and a normalization of firing rates after 48 h.”
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    Premisecitation

    Heterosynaptic LTD requires NMDA receptor activation and depends on the release of Ca2+ from internal stores.

    “Heterosynaptic LTD requires NMDA receptor activation (presumably at paired inputs) and depends on the release of Ca2+ from internal stores (Nishiyama et al. 2000, Royer & Paré 2003).”
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    Premisecitation

    High-frequency stimulation induced LTP at tetanized inputs but produced heterosynaptic LTD at specific neighboring unpaired inputs, and after inducing LTD with low-frequency stimulation, heterosynaptic LTP was induced at neighboring inputs.

    “They found that high-frequency stimulation induced LTP at tetanized inputs but produced heterosynaptic LTD at specific neighboring unpaired inputs. Conversely, after inducing LTD with low-frequency stimulation, heterosynaptic LTP was induced at neighboring inputs.”
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    Premisecitation

    Excitatory and inhibitory best stimuli for both frequency and intensity tend to be the same, and the overall profiles of excitation and inhibition are highly correlated.

    “Excitatory and inhibitory best stimuli for both frequency and intensity tend to be the same, and the overall profiles of excitation and inhibition are highly correlated (Dorrn et al. 2010; Froemke et al. 2007, 2013; Tan & Wehr 2009; Volkov & Galazjuk 1991; Wehr & Zador 2003).”
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    Premisecitation

    A short delay (usually a few milliseconds) occurs between the onset of excitatory and inhibitory conductances, allowing for a high degree of temporal precision for action potential generation in response to sensory stimuli.

    “A short delay (usually a few milliseconds) occurs between the onset of excitatory and inhibitory conductances, allowing for a high degree of temporal precision for action potential generation in response to sensory stimuli (Wehr & Zador 2003).”
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    Premisecitation

    Young rats exposed chronically to tonic white noise for the first month of life had less organized maps, with more broadly tuned neurons, and the critical period for frequency map development was delayed seemingly indefinitely.

    “Conversely, young rats exposed chronically to tonic white noise for the first month of life had less organized maps, with more broadly tuned neurons, and the critical period for frequency map development was delayed seemingly indefinitely (Chang & Merzenich 2003).”
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    Premisecitation

    The ratio of evoked inhibition scaled with the magnitude of excitation, but this form of equalized excitatory-inhibitory balance was due to recruitment of parvalbumin-positive but not somatostatin-positive interneurons.

    “The ratio of evoked inhibition scaled with the magnitude of excitation, but interestingly, this form of equalized excitatory-inhibitory balance was due to recruitment of parvalbumin-positive but not somatostatin-positive interneurons.”
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    Premisecitation

    On individual branches, the numbers of inhibitory puncta scaled with the numbers of excitatory puncta at several different developmental stages in vitro; inhibition could attenuate excitation effectively if coactivated at approximately the same time and place (on the order of approximately 20 ms and 10 μm).

    “On individual branches, the numbers of inhibitory puncta scaled with the numbers of excitatory puncta at several different developmental stages in vitro; additionally, inhibition could attenuate excitation effectively if coactivated at approximately the same time and place (on the order of approximately 20 ms and 10 μm).”
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    Premisecitation

    Although excitation and inhibition are globally balanced even early in life, fine-scale balance emerges later and requires sensory experience.

    “However, although these measures indicate that excitation and inhibition are globally balanced even early in life, fine-scale balance emerges later and requires sensory experience (Froemke & Jones 2011).”
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    Premisecitation

    Excitatory and inhibitory tone-evoked responses are present at hearing onset and equally strong throughout life, so global excitatory-inhibitory balance is intact.

    “excitatory and inhibitory tone-evoked responses were present at hearing onset and equally strong throughout life, i.e., global balance was intact (Dorrn et al. 2010).”
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    Premisecitation

    In adult rat auditory cortex, pairing tones with postsynaptic spiking does not induce STDP or lead to long-term changes in synaptic frequency tuning curves.

    “However, in adult rat auditory cortex, pairing tones with postsynaptic spiking does not induce STDP or lead to long-term changes in synaptic frequency tuning curves (Froemke et al. 2007).”
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    Premisecitation

    Cortical inhibitory responses generally are more sensitive to repetitive stimulation, adapting first and recovering more slowly than excitatory responses.

    “Cortical inhibitory responses generally seem more sensitive to repetitive stimulation, adapting first and recovering more slowly than excitatory responses (Kuhlman et al. 2013, Taub et al. 2013, Wehr & Zador 2005).”
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    Interpretationcitation

    Rapid disinhibition may enable excitatory responses to generate postsynaptic action potentials reliably or lead to strong NMDA receptor activation, gating LTP of paired excitatory and inhibitory inputs and engaging heterosynaptic plasticity to reconfigure receptive fields and increase fine-scale excitatory-inhibitory balance.

    “Rapid disinhibition may then enable excitatory responses to generate postsynaptic action potentials reliably or lead to strong NMDA receptor activation, gating LTP of paired excitatory and inhibitory inputs and perhaps engaging additional mechanisms of heterosynaptic plasticity to reconfigure receptive fields and increase fine-scale excitatory-inhibitory balance (D’amour & Froemke 2015, Froemke &”
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    Interpretationnone given

    In adult cortex, inhibitory circuits could be finely balanced and calibrated, permitting sensory inputs to evoke action potentials via AMPA receptor transmission before cotuned inhibition reduces excitability and NMDA receptors are activated.

    “For one, as mentioned above, inhibitory circuits could be finely balanced and calibrated in the adult cortex, permitting sensory inputs to evoke action potentials via AMPA receptor transmission, before cotuned inhibition reduces excitability and NMDA receptors are activated.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The excitatory-inhibitory sequence depends on the details of long-range and local circuit organization.

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    Interpretationnone given

    Growing evidence indicates that acetylcholine, noradrenalin, and oxytocin each act to disinhibit cortical networks, transiently disrupting excitatory-inhibitory balance to enable long-term changes in sensory receptive fields.

    “Growing evidence indicates that each acts to disinhibit cortical networks, transiently disrupting excitatory-inhibitory balance to enable long-term changes in sensory receptive fields.”
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    Premisecitation

    Acetylcholine has been implicated in attention or learning and memory processes for decades.

    “Investigators have implicated acetylcholine in attention or learning and memory processes for decades (Bartus et al. 1982, Carcea & Froemke 2013, Sarter et al. 2009, Weinberger 2007, Zaborszky 2002).”
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    Interpretationreasoning

    In vivo, neuromodulatory systems must be engaged either artificially via stimulation or through changes in behavioral context that might naturally evoke release.

    “In vivo, however, neuromodulatory systems must be engaged either artificially via stimulation of some sort (e.g., pharmacologically, electrically, or optically) or through changes in behavioral context that might naturally evoke release.”
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    Premisecitation

    Electrical or optogenetic stimulation of nucleus basalis simultaneously increases and decorrelates cortical responses.

    “Electrical or optogenetic stimulation of nucleus basalis simultaneously increases and decorrelates cortical responses (Goard & Dan 2009, Pinto et al. 2013).”
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    Premisecitation

    Lesions of the basal forebrain cholinergic system or blockade of cortical muscarinic receptors produce defects of attention and disrupt learning and memory.

    “Lesions of this system or blockade of cortical muscarinic receptors produces defects of attention and disrupts learning and memory (McGaughy et al. 2000, Mesulam 2013).”
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    Premisecitation

    Repetitive pairing of nucleus basalis stimulation with pure tones for several minutes in anesthetized adult rats shifts frequency tuning curves toward the paired frequency, due to an increase in spikes evoked by the paired tone and a decrease in spiking evoked by the original best frequency.

    “Bakin & Weinberger (1996) repetitively paired nucleus basalis stimulation with pure tones for several minutes in anesthetized adult rats and observed a shift in frequency tuning curves toward the paired frequency, due to an increase in spikes evoked by the paired tone, and a decrease in spiking evoked by the original best frequency.”
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    • cites Bakin & Weinberger (1996)

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    Premisecitation

    Nucleus basalis stimulation enhances excitatory events and decreases inhibitory events in auditory cortex, transiently desynchronizing cortical EEG and breaking excitatory-inhibitory balance for seconds to minutes.

    “Nucleus basalis stimulation enhances excitatory events and decreases inhibitory events in the auditory cortex (Froemke et al. 2007, Letzkus et al. 2011, Metherate & Ashe 1993), transiently desynchronizing cortical EEG and breaking excitatory-inhibitory balance for seconds to minutes.”
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    Premisecitation

    Intracortical microstimulation can reliably produce long-lasting shifts in rat auditory cortex frequency tuning but does not change behavioral performance.

    “They then used intracortical microstimulation to reliably produce long-lasting shifts in rat auditory cortex frequency tuning but, surprisingly, did not observe any changes in behavioral performance (Talwar & Gerstein 2001).”
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    Premisecitation

    Locus coeruleus neurons are coupled together via gap junctions and can potentially act coherently to deliver a uniform modulatory signal simultaneously to many target structures for wide-scale control of brain state.

    “As locus coeruleus neurons are coupled together via gap junctions, these cells can potentially act in a coherent manner to deliver a uniform modulatory signal simultaneously to many target structures for wide-scale control of brain state (Carter et al. 2010, Constantinople & Bruno 2011, Sara 2009).”
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    Premisecitation

    Whereas nucleus basalis cholinergic neurons project largely to the cortex, locus coeruleus neurons project extensively throughout the central nervous system.

    “Whereas nucleus basalis cholinergic neurons project largely to the cortex, locus coeruleus neurons project extensively throughout the central nervous system (Berridge 2008, Fuxe et al. 2012).”
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    Interpretationreasoning

    These physiological changes last for several hours in the absence of additional stimulation but can lead to changes elsewhere or throughout auditory sensorimotor circuits to support enduring behavioral changes in the absence of direct changes to primary sensory cortex.

    “These physiological changes last for several hours in the absence of additional stimulation but can lead to changes elsewhere or throughout auditory sensorimotor circuits to support enduring behavioral changes in the absence of direct changes to primary sensory cortex.”
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  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Noradrenalin is a catecholamine neuromodulator involved in attention and arousal.

    “Noradrenalin is a catecholamine neuromodulator also involved in attention and arousal (Aston-Jones & Cohen 2005, Eldar et al. 2013, Sara 2009)”
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    Premisecitation

    Yu and Dayan (2005) postulated that acetylcholine might encode expected uncertainty, whereas noradrenalin encodes unexpected uncertainty.

    “Yu and Dayan (2005) surveyed the behavioral and psychopharmacological literature and postulated that acetylcholine might encode expected uncertainty, whereas noradrenalin encodes unexpected uncertainty.”
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  • May combine two claims.

    Premisecitation

    Both acetylcholine and noradrenalin are important for cortical plasticity.

    “However, both acetylcholine and noradrenalin are also important for cortical plasticity (Bear & Singer 1986, Carcea & Froemke 2013, Gu 2002, Seol et al. 2007)”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Bear & Singer 1986

      Not checked in the free run.

    • cites Carcea & Froemke 2013

      Not checked in the free run.

    • cites Gu 2002

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Locus coeruleus pairing decreases tonic, ongoing inhibition for a few minutes in rat auditory cortex in vivo and mouse cochlear nucleus in vitro.

    “locus coeruleus pairing instead seems to decrease tonic, ongoing inhibition for a few minutes in the rat auditory cortex in vivo (Martins & Froemke 2014) and mouse cochlear nucleus in vitro (Kuo & Trussell 2011).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Martins & Froemke 2014

      Not checked in the free run.

    • cites Kuo & Trussell 2011

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    Noradrenalin from the locus coeruleus provides a distinct form of inhibitory control separate from acetylcholine, leading to overall response gain changes.

    “Thus, noradrenalin from the locus coeruleus provides a distinct form of inhibitory control separate from that of acetylcholine, leading to overall response gain changes”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    The decrease in tonic inhibition leads to much larger responses (up to tenfold in amplitude) to any incoming input before excitability gradually recovers over an hour and tuning curves retain a new preference for paired inputs.

    “The decrease in tonic inhibition leads to much larger responses (up to tenfold in amplitude) to any incoming input before excitability gradually recovers over an hour and tuning curves retain a new preference for paired inputs.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Martins & Froemke 2014

      Not checked in the free run.

    • cites Kuo & Trussell 2011

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Repetitively pairing a pure tone with locus coeruleus stimulation often increases responses much more dramatically, and at first can boost responses to all stimuli, paired and unpaired, with some preference for the paired frequency.

    “In contrast, repetitively pairing a pure tone with locus coeruleus stimulation often increases the responses much more dramatically, and at first, pairing that is specific to the locus coeruleus can boost responses to all stimuli, paired and unpaired, although with some preference for the paired frequency itself (Edeline et al. 2011, Martins & Froemke 2014).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Edeline et al. 2011

      Not checked in the free run.

    • cites Martins & Froemke 2014

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Locus coeruleus neurons can respond to sensory stimuli and change their responses depending on context and experience.

    “Locus coeruleus neurons can also respond to sensory stimuli and change their responses depending on context and experience (Sara & Segal 1991).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Sara & Segal 1991

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Across species, systems, and different anesthetics or brain states, cholinergic activation generally increases cortical excitability and shifts tuning curves toward paired stimuli in a manner that conserves overall excitability and preserves global excitatory-inhibitory balance.

    “Across species, systems, and different anesthetics or brain states, cholinergic activation generally increases cortical excitability and shifts tuning curves toward paired stimuli in a manner that conserves overall excitability and preserves global excitatory-inhibitory balance (Froemke et al. 2007, Weinberger 2007).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Froemke et al. 2007

      Not checked in the free run.

    • cites Weinberger 2007

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    TGOT directly depolarizes fast-spiking interneurons, increasing the spontaneous rate of GABA release and leading to short-term depression of inhibitory connections onto excitatory cells.

    “TGOT directly depolarized fast-spiking interneurons, which increased the spontaneous rate of GABA release and led to short-term depression of inhibitory connections onto excitatory cells.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Owen et al. (2013)

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    The oxytocin receptor agonist TGOT decreases spontaneous firing but increases stimulus-evoked action potential generation in CA1 pyramidal neurons from hippocampal slices.

    “Recently, Owen et al. (2013) found that the oxytocin receptor agonist [Thr4,Gly7]-oxytocin (TGOT) decreased spontaneous firing but increased stimulus-evoked action potential generation, and TGOT decreased evoked IPSCs but increased spontaneous IPSCs in CA1 pyramidal neurons from hippocampal slices.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Owen et al. (2013)

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    TGOT decreases evoked IPSCs but increases spontaneous IPSCs in CA1 pyramidal neurons from hippocampal slices.

    “TGOT decreased evoked IPSCs but increased spontaneous IPSCs in CA1 pyramidal neurons from hippocampal slices.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Owen et al. (2013)

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Innocuous sounds generally do not activate locus coeruleus neurons but can lead to synaptic and spiking responses in these cells after being paired with locus coeruleus stimulation or foot shock.

    “Innocuous sounds generally do not activate locus coeruleus neurons but can lead to synaptic and spiking responses in these cells after being paired with locus coeruleus stimulation or other means of activating the circuit, such as foot shock (Martins & Froemke 2014).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Martins & Froemke 2014

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Endocannabinoids mediate depolarization-induced suppression of inhibition and have been implicated as a retrograde signal important for STDP.

    “Endocannabinoids mediate a form of short-term plasticity known as depolarization-induced suppression of inhibition, and endocannabinoids have been implicated as a retrograde signal important for STDP (Feldman 2009, Sjöström et al. 2003)”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Feldman 2009

      Not checked in the free run.

    • cites Sjöström et al. 2003

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Muscarine, serotonin, baclofen, and adenosine each reduce GABA release from fast-spiking interneurons onto excitatory cells in barrel cortex.

    “Kruglikov & Rudy (2008) demonstrated that muscarine, serotonin, baclofen (a GABAB receptor agonist), and adenosine each reduce GABA release from fast-spiking interneurons onto excitatory cells in barrel cortex.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Kruglikov & Rudy (2008)

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    D1-type receptors enhance both NMDA receptor excitatory currents and IPSCs, whereas D2-type receptors reduce NMDA receptor responses and IPSCs.

    “D1-type receptors can enhance both NMDA receptor excitatory currents and IPSCs, whereas D2-type receptors reduce NMDA receptor responses and IPSCs (Seamans & Yang 2004).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Seamans & Yang 2004

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Noradrenalin does not reduce GABA release at these connections, suggesting it might act on other populations of inhibitory cells or inhibitory synapses to control spontaneous activity and overall inhibitory tone.

    “Interestingly, noradrenalin did not function like this at these connections, suggesting that it might act on other populations of inhibitory cells or inhibitory synapses to control spontaneous activity and overall inhibitory tone.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Kruglikov & Rudy (2008)

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationcitation

    These dynamics by which initially imbalanced excitation and inhibition become balanced are reminiscent of changes to tone-evoked synaptic responses during postnatal development.

    “These dynamics by which initially imbalanced excitation and inhibition become balanced are reminiscent of the changes to tone-evoked synaptic responses during postnatal development, when animals have had limited exposure or experience with certain sounds (Dorrn et al. 2010).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Dorrn et al. 2010

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Locus coeruleus neurons project extensively throughout the brain.

    “whereas locus coeruleus neurons project extensively throughout the brain (Sara 2009).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Sara 2009

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The cholinergic system appears to be organized topographically in terms of projections to different cortical areas.

    “For example, the cholinergic system appears to be organized topographically in terms of projections to different cortical areas (Mesulam 2013), whereas locus coeruleus neurons project extensively throughout the brain (Sara 2009).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Mesulam 2013

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The locus coeruleus provides a major input to the oxytocinergic paraventricular nucleus.

    “The locus coeruleus provides a major input to the oxytocinergic paraventricular nucleus (Sawchenko & Swanson 1982).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Sawchenko & Swanson 1982

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Cholinergic projections can form synapses onto target cells, and cholinesterase can act quickly to break down acetylcholine and limit diffusion away from release sites.

    “Cholinergic projections can form synapses onto target cells, and cholinesterase can act quickly to break down acetylcholine and limit diffusion away from release sites (Sarter et al. 2009, Umbriaco et al. 1994).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Sarter et al. 2009

      Not checked in the free run.

    • cites Umbriaco et al. 1994

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    Shortly thereafter, on the timescale of minutes, heterosynaptic modifications to other excitatory synapses occur to decrease the strength of the originally strongest inputs and perhaps normalize or strengthen inputs functionally related to the paired inputs.

    “Shortly thereafter, on the timescale of minutes, heterosynaptic modifications to other excitatory synapses occur to decrease the strength of the originally strongest inputs and perhaps normalize or strengthen inputs functionally related to the paired inputs.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationreasoning

    Sensory inputs activated during this change in modulatory tone are disinhibited, leading to more reliable spike firing, enhanced activation of NMDA receptors, and LTP of excitatory synapses.

    “Sensory inputs activated during this change in modulatory tone are disinhibited, leading to more reliable spike firing, enhanced activation of NMDA receptors, and LTP of excitatory synapses.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationreasoning

    There need not be anything particularly unique about acetylcholine for attention and perceptual learning or oxytocin for pair-bond formation; details of circuitry and environmental stimuli might impart functional specialization.

    “In general, then, there need not be anything particularly unique about, for example, acetylcholine for attention and perceptual learning or oxytocin for pair-bond formation. Instead, the details of the circuitry and the types of environmental stimuli that activate these circuits might impart such functional specialization.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Noradrenalin and oxytocin projections may provide forms of volume transmission.

    “In contrast, noradrenalin and oxytocin projections may provide forms of volume transmission (Fuxe et al. 2012).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Fuxe et al. 2012

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    An increase in firing rate and STDP paradigms are effective experimental means for changing synaptic strength, but long-term synaptic modifications and changes to sensory responses can also be induced in the absence of postsynaptic spiking.

    “An increase in firing rate and STDP paradigms are effective experimental means for changing synaptic strength, but long-term synaptic modifications and changes to sensory responses can also be induced in the absence of postsynaptic spiking (Gambino et al. 2014, Lisman & Spruston 2005).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Gambino et al. 2014

      Not checked in the free run.

    • cites Lisman & Spruston 2005

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing), S4 (based). May combine two claims.

    Interpretationreasoning

    Cortical coding schemes and sensory representations ultimately rely on spikes, and fine-scale excitatory-inhibitory balance must be defined and coordinated by correlated pre- and postsynaptic activity.

    “However, cortical coding schemes and sensory representations ultimately rely on spikes, and in some sense, fine-scale excitatory-inhibitory balance must be defined and thus coordinated by correlated pre- and postsynaptic activity.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S2 (checkable), S4 (based). May combine two claims.

    Interpretationnone given

    Populations of excitatory and inhibitory synapses must likely be adjusted in a complex and coordinated manner to preserve excitatory-inhibitory balance and prevent neural systems from remaining hypo- or hyperexcitable for prolonged periods.

    “Populations of excitatory and inhibitory synapses must likely be adjusted in a complex and coordinated manner to preserve excitatory-inhibitory balance and prevent neural systems from remaining hypo- or hyperexcitable for prolonged periods.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: Inhibitory synapses can be modified.
    • Rests on an assumption: Excitatory-inhibitory balance must be preserved to prevent neural systems from remaining hypo- or hyperexcitable for prolonged periods.

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Interpretationreasoning

    Local dendritic and NMDA receptor spikes might also be involved in these processes during development or heightened and permissive periods of cortical neuromodulation.

    “Local dendritic and NMDA receptor spikes might also be involved in these processes during development or heightened and permissive periods of cortical neuromodulation.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationnone given

    Studies in the auditory cortex have proved useful for examining plasticity in vivo, to relate neuromodulation of excitatory-inhibitory balance to changes in synaptic receptive field organization and modifications of cortical receptive fields to improvements in sensory perception.

    “Studies in the auditory cortex in particular have proved useful for examining plasticity in vivo, to relate neuromodulation of excitatory-inhibitory balance to changes in synaptic receptive field organization and modifications of cortical receptive fields to improvements in sensory perception.”
    Quote in the paperNot a substantial claim
68 of 68

  • The paper relies on this without support.

    Plasticity of cortical excitatory synapses is important for learning and memory.

    “Plasticity of cortical excitatory synapses is thought to be important for learning and memory, leading to alterations in sensory representations and cognitive maps.”

  • The paper relies on this without support.

    Fine-scale excitatory-inhibitory balance is shaped by experience and is meaningful only in terms of the specific stimuli used to drive synaptic modifications.

    “(as fine-scale balance is shaped by experience, meaningful only in terms of specific stimuli used to drive synaptic modifications).”

  • The paper relies on this without support.

    The excitatory-inhibitory sequence depends on the details of long-range and local circuit organization.

    “Given that this excitatory-inhibitory sequence depends on the details of long-range and local circuit organization”

  • The paper relies on this without support.

    In vitro evoked inhibitory events are not necessarily functionally related to excitatory events in the fine-scale balance sense.

    “where evoked inhibitory events are not necessarily functionally related to excitatory events in the fine-scale balance sense”

  • The paper relies on this without support.

    Inhibitory synapses can be modified.

    “Much work has focused on the plasticity of excitatory synapses, but inhibitory synapses can also be modified.”

  • The paper relies on this without support.

    Excitatory-inhibitory balance must be preserved to prevent neural systems from remaining hypo- or hyperexcitable for prolonged periods.

    “Populations of excitatory and inhibitory synapses must likely be adjusted in a complex and coordinated manner to preserve excitatory-inhibitory balance and prevent neural systems from remaining hypo- or hyperexcitable for prolonged periods.”
6 of 6

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Long-lasting plasticity in the adult cortex requires activation of subcortical modulatory systems that provide behavioral context to incoming sensory signals.

    “long-lasting plasticity in the adult cortex requires activation of subcortical modulatory systems that provide behavioral context to incoming sensory signals”

    From Neuromodulation of maternal circuits by oxytocin (2019) · cites this paper as Froemke, 2015

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • One reference is assigned two different authors and years

    Minor

    References 123 and 130 give the same article title, journal, volume, pages, and identifier, but attribute it to different authors and publication years.

1 of 1

Cites

Flagged first, then by citations

Research works printed but not linked: 8

  1. Altura BM, 1977, Fed. Proc., 36, 1853
  2. Bartz JA, 2011, Trends Cogn. Sci., 15, 301
  3. Froemke RC, 2010, Front. Synaptic Neurosci., 2, 19
  4. Froemke RC, 2010, Front. Synaptic Neurosci., 2, 29
  5. Lamsa KP, 2010, Front. Synaptic Neurosci., 2, 16
  6. Larsen RS, 2010, Front. Synaptic Neurosci., 2, 9
  7. Pawlak V, 2010, Front. Synap. Neurosci., 2, 146
  8. Scanziani M, 1996, Nature, 422, 518

Cited by

Sorted by citations

Related

Authors
Froemke, R. C.
Affiliations
New York University (US)
Corresponding author
Froemke, Robert C.
ORCID
Froemke, Robert C.
Venue
Annual Review of Neuroscience
Publisher
Annual Reviews
Published
2015-07-08
Volume
38
Issue
1
Pages
195-219
ISSN
  • 0147-006X (ISSN-L)
  • 1545-4126
DOI
10.1146/annurev-neuro-071714-034002
PMC
PMC4652600
OpenAlex
W2139936417
Semantic Scholar
27984ef01511b3ee02dada5da79c588d91be4136
Cited by
458
References
175
Citations by year
2026: 39 · 2025: 63 · 2024: 42 · 2023: 42 · 2022: 35 · 2021: 48 · 2020: 46 · 2019: 39 · 2018: 48 · 2017: 27 · 2016: 21 · 2015: 8
FWCI
4.18
Type
journal article
Language
en
Open access
Locations
  • Annual Review of Neuroscience (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • McKnight Foundation
  • National Institute on Deafness and Other Communication Disorders (K99DC009635, DC12557, DC009635, R00DC009635, R01DC012557)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords
excitation-inhibition balance, synaptic plasticity, inhibitory synapses, neuromodulation, disinhibition, cortical circuits, learning and memory, sensory representation, neural coding
MeSH terms
Animals, Cerebral Cortex, Humans, Learning, Memory, Neural Inhibition, Neuronal Plasticity, Neurons, Neurotransmitter Agents

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-09.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-09.

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