Regulation of Parvalbumin Basket cell plasticity in rule learning

doi:10.1016/j.bbrc.2015.02.023

Biochemical and Biophysical Research Communications

Volume 460, Issue 1, 24 April 2015, Pages 100-103

https://doi.org/10.1016/j.bbrc.2015.02.023 Get rights and content

Abstract

Local inhibitory Parvalbumin (PV)-expressing Basket cell networks shift to one of two possible opposite configurations depending on whether behavioral learning involves acquisition of new information or consolidation of validated rules. This reflects the existence of PV Basket cell subpopulations with distinct schedules of neurogenesis, output target neurons and roles in learning. Plasticity of hippocampal early-born PV neurons is recruited in rule consolidation, whereas plasticity of late-born PV neurons is recruited in new information acquisition. This involves regulation of early-born PV neuron plasticity specifically through excitation, and of late-born PV neuron plasticity specifically through inhibition. Therefore, opposite learning requirements are implemented by distinct local networks involving PV Basket cell subpopulations specifically regulated through inhibition or excitation.

Section snippets

PV Basket cell plasticity upon learning

Reinforced trial-and-error learning protocols provide experimental settings to investigate how plasticity is adjusted during learning. Effective acquisition and combination of potentially task-relevant information is essential during early phases of trial-and-error learning, whereas reliable application of validated routines dominates when prediction errors get vanishingly small [1]. At the circuit level, these contrasting requirements are reflected by shifts in the configuration of local

PV Basket cell functions

PV-positive Basket cells are widely distributed GABAergic inhibitory interneurons that provide local feedforward and feedback inhibition through perisomatic boutons onto principal excitatory neurons [3], [4], [5]. In addition, PV Basket cells inhibit each other reciprocally through perisomatic innervation and are dynamically coupled electrically through gap junctions [3], [5]. Accordingly, PV Basket cells filter activation of principal neurons, and networks of PV Basket cells have major roles

Subpopulations of PV Basket cells defined by time schedule of neurogenesis

To investigate whether PV Basket cells might differ systematically as a function of when they are generated during neurogenesis, we labeled proliferating cells with BrdU and analyzed BrdU/PV double-positive cells in hippocampal CA3 and CA1, primary somatosensory whisker cortex, and dorsal striatum of adult mice. Hippocampal PV neurons generated at E9.5 or E11.5 were predominantly high- and intermediate-high PV, whereas neurons generated at E13.5 or E15.5 were predominantly intermediate-low- and

Rule learning involves plasticity in either early- or late-born PV neurons

To determine how PV neurons generated at early and late embryonic developmental time points are affected by learning, we subjected BrdU-labeled mice to either contextual fear conditioning (cFC) or environmental enrichment (EE). cFC had a major impact on PV value distributions in hippocampal CA3 and CA1 cells labeled at E9.5 or E11.5, whereas cells labeled at E13.5 or E15.5 were not noticeably affected. By contrast, EE affected PV value distributions of hippocampal CA3 and CA1 cells labeled at

Subpopulation cell-plasticity specifically regulated through excitation or inhibition

To investigate whether early-born PV neurons specifically respond to changes in synaptic excitation, we treated adult mice pharmacogenetically with the competitive inhibitor of NMDA receptors AP5. The NMDA inhibitor induced lower contents of high-PV and higher contents of low-PV neurons in hippocampal CA3. Notably, AP5 specifically affected PV levels in early-born neurons, whereas late-born neurons were not affected. To further investigate specific regulation of PV subpopulation cell-plasticity

Early- and late-born PV Basket cells target distinct principal neurons subpopulations

The consistent experience-related plasticity regulation of the two subpopulations of PV Basket cells raised the issue of whether these might also exhibit distinct output targets related to behavioral function [15], [17]. While PV Basket cells exhibit high probabilities of connectivity to local principal neurons, early-born PV neurons are more abundant in deep cortical layers of neocortex, whereas late-born neurons are more abundant in upper layers [20], suggesting that early- and late-born PV

Plasticity regulation through excitation or inhibition in learning

Our findings suggest that PV neuron regulation specifically through excitation provides a mechanism to match implementation of validated rules in learning to early-born PV neuron cell plasticity. Likewise, regulation of PV neurons specifically through inhibition matches enhanced plasticity and learning to late-born PV neuron cell plasticity. This might involve specific learning-related gating mechanisms as revealed in recent studies of Pavlovian conditioning (e.g. [26]). Concerning the

Distinct functional roles of PV Basket cell subpopulations

Our results establish late-born PV Basket cells as the subpopulation that specifically accounts for positive regulation of plasticity during learning, upon EE, and during critical period-like plasticity. Enhancing inhibitory connectivity and reducing PV and GAD-67 levels in late-born PV neurons might enhance further learning by reducing the impact of PV-mediated inhibition of principal neuron subpopulations [28], [29] under acquisition regimes involving local circuit disinhibition. By contrast,

Conflict of interest

None.

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Parvalbumin interneuron inhibition onto anterior insula neurons projecting to the basolateral amygdala drives aversive taste memory retrieval
2021, Current Biology
Citation Excerpt :
However, our findings point out that the local circuit mechanisms and resultant internal representations necessary for effective memory retrieval may differ from those engaged in acquisition (Figure 4). CTA memory acquisition initiates a cascade of activity that is not dependent on aIC PV (Figure 4) but likely culminates in consolidation events that prime their necessity for precise memory retrieval.24 Even so, the necessity for aIC PV activation during CTA memory retrieval does not relate to taste recognition or the acquisition of familiarity per se (Figures 5 and 7).
Memory retrieval refers to the fundamental ability of organisms to make use of acquired, sometimes inconsistent, information about the world. Although memory acquisition has been studied extensively, the neurobiological mechanisms underlying memory retrieval remain largely unknown. Conditioned taste aversion (CTA) is a robust associative paradigm, through which animals can be trained to express aversion toward innately appetitive tastants. The anterior insula (aIC) is indispensable in the ability of mammals to retrieve associative information regarding tastants that have been previously linked with gastric malaise. Here, we show that CTA memory retrieval promotes cell-type-specific activation in the aIC. Using chemogenetic tools in the aIC, we found that CTA memory acquisition requires activation of excitatory neurons and inhibition of inhibitory neurons, whereas retrieval necessitates activation of both excitatory and inhibitory aIC circuits. CTA memory retrieval at the aIC activates parvalbumin (PV) interneurons and increases synaptic inhibition onto activated pyramidal neurons projecting to the basolateral amygdala (aIC-BLA). Unlike innately appetitive taste memory retrieval, CTA retrieval increases synaptic inhibition onto aIC-BLA-projecting neurons that is dependent on activity in aIC PV interneurons. PV aIC interneurons coordinate CTA memory retrieval and are necessary for its dominance when conflicting internal representations are encountered over time. The reinstatement of CTA memories following extinction is also dependent on activation of aIC PV interneurons, which increase the frequency of inhibition onto aIC-BLA-projecting neurons. This newly described interaction of PV and a subset of excitatory neurons can explain the coherency of aversive memory retrieval, an evolutionary pre-requisite for animal survival.
Critical periods of brain development
2020, Handbook of Clinical Neurology
Citation Excerpt :
During this period, a range of plasticity-permissive factors, such as brain derived neurotrophic factor (BDNF), further promote plastic changes by stimulating neurite motility and growth (Huang et al., 1999; Tyler and Pozzo-Miller, 2003). As inhibitory circuits mature, permissive factors gradually decline, and further circuit rewiring is impeded by the aforementioned plasticity brakes, which include the inhibitory activity of GABAergic interneurons such as parvalbumin-positive (PV +) cells (Caroni, 2015), extracellular matrix components including perineuronal nets (PNNs) (Wang and Fawcett, 2012), and myelin-associated proteins (Stephany et al., 2016). These brakes ensure the stability of cortical representations, ultimately making the mature cortex resistant to passive abnormal sensory experience (Hensch, 2005).
Brain plasticity is maximal at specific time windows during early development known as critical periods (CPs), during which sensory experience is necessary to establish optimal cortical representations of the surrounding environment. After CP closure, a range of functional and structural elements prevent passive experience from eliciting significant plastic changes in the brain.
The transition from a plastic to a more fixed state is advantageous as it allows for the sequential consolidation and retention of new and more complex perceptual, motor, and cognitive functions. However, the formation of stable neural representations may pose limitations on future revisions to the circuitry. If sensory experience is abnormal or absent during this time, it can have profound effects on sensory representations in adulthood, resulting in quasi-permanent adaptations that can make it nearly impossible to learn certain skills or process certain stimulus properties later on in life.
This chapter begins with a brief introduction to experience-dependent plasticity throughout the lifespan (Section Introduction). Next, we define what constitutes a CP (Section What Are Critical Periods?) and review some of the key CPs in the visual and auditory systems (Section Key Critical Periods of Sensory Systems). We then discuss the mechanisms whereby cortical plasticity is regulated both locally and through neuromodulatory systems (Section How Are Critical Periods Regulated?). Finally, we highlight studies showing that CPs can be extended beyond their normal epochs, closed prematurely, or reopened during adult life by merely altering sensory inputs (Section Timing of Critical Periods: Can CP Plasticity Be Extended, Limited, or Reactivated?).
Denervated mouse dentate granule cells adjust their excitatory but not inhibitory synapses following in vitro entorhinal cortex lesion
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Citation Excerpt :
These results demonstrate that dentate granule cells maintain their GABAergic synaptic set-point, while adjusting excitatory synapses in response to major changes in network connectivity, i.e., in vitro lesion-induced deafferentation. Work from recent years has shed new light on the role of inhibitory neurotransmission in complex brain function (Griffen and Maffei, 2014; Caroni, 2015; Froemke, 2015; Letzkus et al., 2015; Tremblay et al., 2016). Studies employing optogenetic approaches demonstrate the relevance of local inhibitory networks in neural function and plasticity.
Neurons adjust their synaptic strength in a homeostatic manner following changes in network activity and connectivity. While this form of plasticity has been studied in detail for excitatory synapses, homeostatic plasticity of inhibitory synapses remains not well-understood. In the present study, we employed entorhinal cortex lesion (ECL) of organotypic entorhino-hippocampal tissue cultures to test for homeostatic changes in GABAergic neurotransmission onto partially denervated dentate granule cells. Using single and paired whole-cell patch-clamp recordings, as well as immunostainings for synaptic markers, we find that excitatory synaptic strength is robustly increased 3 days post lesion (dpl), whereas GABAergic neurotransmission is not changed after denervation. Even under conditions of pharmacological inhibition of glutamatergic neurotransmission, which prevents neurons to compensate for the loss of input via excitatory synaptic scaling, down-scaling of GABAergic synapses does not emerge 3 days after denervation. We conclude that granule cells maintain structural and functional properties of GABAergic synapses even in the face of substantial changes in network connectivity. Hence, alterations in inhibitory neurotransmission, as seen in pathological brain states, may not simply reflect a homeostatic response to disconnection.
Molecular Changes in the Brain of the Wintering Calidris pusilla in the Mangroves of the Amazon River Estuary
2023, International Journal of Molecular Sciences
Parvalbumin - Positive Neurons in the Neocortex: A Review
2023, Physiological Research
Bidirectional plasticity of GABAergic tonic inhibition in hippocampal somatostatin- and parvalbumin-containing interneurons
2023, Frontiers in Cellular Neuroscience

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ReviewRegulation of Parvalbumin Basket cell plasticity in rule learning

Abstract

Section snippets

PV Basket cell plasticity upon learning

PV Basket cell functions

Subpopulations of PV Basket cells defined by time schedule of neurogenesis

Rule learning involves plasticity in either early- or late-born PV neurons

Subpopulation cell-plasticity specifically regulated through excitation or inhibition

Early- and late-born PV Basket cells target distinct principal neurons subpopulations

Plasticity regulation through excitation or inhibition in learning

Distinct functional roles of PV Basket cell subpopulations

Conflict of interest

Neuron

Neuron

Neuron

Cell

Neuron

Neurobiol. Dis.

Reinforcement learning: a survey

J. Artif. Intell. Res.

Parvalbumin-expressing basket-cell network plasticity induced by experience regulates adult learning

Nature

Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks

Nat. Rev. Neurosci.

Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations

Science

Interneurons. Fast-spiking, parvalbumin+ GABAergic interneurons: from cellular design to microcircuit function

Science

Driving fast-spiking cells induces gamma rhythm and controls sensory responses

Nature

Maturation of GABAergic inhibition promotes strengthening of temporally coherent inputs among convergent pathways

PLoS Comput. Biol.

Local GABAcircuit control of experience-dependent plasticity in developing visual cortex

Science

Critical period plasticity in local cortical circuits

Nat. Rev. Neurosci.

Activity-dependent PSA expression regulates inhibitory maturation and onset of critical period plasticity

Nat. Neurosci.

Cortical plasticity induced by inhibitory neuron transplantation

Science

Cortical interneurons that specialize in disinhibitory control

Nature

Review
Regulation of Parvalbumin Basket cell plasticity in rule learning