Differential excitatory control of 2 parallel basket cell networks in amygdala microcircuits

Andrási, Tibor; Veres, Judit M.; Rovira-Esteban, Laura; Kozma, Richárd; Vikór, Attila; Gregori, Erzsébet; Hájos, Norbert

doi:10.1371/journal.pbio.2001421

Cited by 34 publications

(65 citation statements)

References 76 publications

(123 reference statements)

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“…The dendritic shafts of VIP+ INs were the main subcellular domain targeted by glutamatergic inputs, with similar density on both the proximal and distal compartments. However, the density of excitatory inputs received by VIP+ INs appears much lower compared with other INs, such as those expressing PV ( Smith et al, 1998 ; Gulyás et al, 1999 ; Andrási et al, 2017 ). One EM study of CR+ INs in the rat hippocampus revealed that they share a similar density of excitatory inputs to VIP+ INs ( Gulyás et al, 1999 ), thus suggesting that the glutamatergic innervation of VIP+ and CR+ INs significantly differs at least from PV+ INs.…”

Section: Discussionmentioning

confidence: 93%

“…One characteristic of BLA INs that has not been fully explored is its diversity. BLA INs vary significantly in their firing, molecular, and morphological properties, including axonal projections ( Spampanato et al, 2011 ; Capogna, 2014 ; Vereczki et al, 2016 ; Andrási et al, 2017 ). Similar to their neocortical and hippocampal counterparts, BLA IN subtypes may serve profoundly different roles in the spatiotemporal control of local network activity associated with different brain states and behavioral contexts ( Tremblay et al, 2016 ).…”

Section: Introductionmentioning

confidence: 99%

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Vasoactive Intestinal Polypeptide-Immunoreactive Interneurons within Circuits of the Mouse Basolateral Amygdala

et al. 2018

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In cortical structures, principal cell activity is tightly regulated by different GABAergic interneurons (INs). Among these INs are vasoactive intestinal polypeptide-expressing (VIP+) INs, which innervate preferentially other INs, providing a structural basis for temporal disinhibition of principal cells. However, relatively little is known about VIP+ INs in the amygdaloid basolateral complex (BLA). In this study, we report that VIP+ INs have a variable density in the distinct subdivisions of the mouse BLA. Based on different anatomical, neurochemical, and electrophysiological criteria, VIP+ INs could be identified as IN-selective INs (IS-INs) and basket cells expressing CB1 cannabinoid receptors. Whole-cell recordings of VIP+ IS-INs revealed three different spiking patterns, none of which was associated with the expression of calretinin. Genetic targeting combined with optogenetics and in vitro recordings enabled us to identify several types of BLA INs innervated by VIP+ INs, including other IS-INs, basket and neurogliaform cells. Moreover, light stimulation of VIP+ basket cell axon terminals, characterized by CB1 sensitivity, evoked IPSPs in ∼20% of principal neurons. Finally, we show that VIP+ INs receive a dense innervation from both GABAergic inputs (although only 10% from other VIP+ INs) and distinct glutamatergic inputs, identified by their expression of different vesicular glutamate transporters.In conclusion, our study provides a wide-range analysis of single-cell properties of VIP+ INs in the mouse BLA and of their intrinsic and extrinsic connectivity. Our results reinforce the evidence that VIP+ INs are structurally and functionally heterogeneous and that this heterogeneity could mediate different roles in amygdala-dependent functions.SIGNIFICANCE STATEMENT We provide the first comprehensive analysis of the distribution of vasoactive intestinal polypeptide-expressing (VIP+) interneurons (INs) across the entire mouse amygdaloid basolateral complex (BLA), as well as of their morphological and physiological properties. VIP+ INs in the neocortex preferentially target other INs to form a disinhibitory network that facilitates principal cell firing. Our study is the first to demonstrate the presence of such a disinhibitory circuitry in the BLA. We observed structural and functional heterogeneity of these INs and characterized their input/output connectivity. We also identified several types of BLA INs that, when inhibited, may provide a temporal window for principal cell firing and facilitate associative plasticity, e.g., in fear learning.

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Section: Discussionmentioning

confidence: 93%

Section: Introductionmentioning

confidence: 99%

Vasoactive Intestinal Polypeptide-Immunoreactive Interneurons within Circuits of the Mouse Basolateral Amygdala

et al. 2018

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“…The neurons of this cortical CCK+ network are connected by both GABAergic synapses and electrical synapses, and this network is distinct from other interneuronal networks of PV+ and neurogliaform neurons (Hestrin & Galarreta, ). Likewise, networks of distinct subtypes of PV+ neurons interconnected by GABAergic synapses and electrical synapses have been described in the rodent BNC (Andrási et al, ; Muller et al, ; Woodruff & Sah, ). Since these amygdalar and cortical networks are always interconnected by both chemical and electrical synapses, it seems likely that CCK+ neurons in the monkey BNC may also be interconnected by both types of synapses.…”

Section: Discussionmentioning

confidence: 99%

“…In the present study, synapse‐like contacts of CCK+ axon terminals with somata and dendrites of other CCK+ neurons were common, indicating that there is a network of interconnected CCK+ neurons in the monkey BNC. These contacts have not been described in anatomical studies in rodents, although presumptive CCK to CCK synapses have been seen using antibodies to CB1Rs (Andrási et al, ). A similar interconnected network of large CCK+/CB1R+ basket cells has been described in the rodent neocortex (Galarreta, Erdélyi, Szabó, & Hestrin, ).…”

Section: Discussionmentioning

confidence: 99%

Cholecystokinin immunoreactive neurons in the basolateral amygdala of the rhesus monkey (Macaca mulatta)

McDonald

Mascagni

2019

J of Comparative Neurology

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Several distinct subpopulations of interneurons (INs) in the amygdalar basolateral nuclear complex (BNC) of the rat can be recognized on the basis of their expression of calcium‐binding proteins and neuropeptides, including parvalbumin (PV), somatostatin (SOM), calretinin (CR), and cholecystokinin (CCK). In the rat BNC CCK is expressed in two separate IN subpopulations, termed large (CCKL) and small (CCKS). These subpopulations exhibit distinct connections indicative of discrete functional roles in the circuitry of the BNC. Although there have been several studies of PV+, SOM+, and CR+ INs in the primate BNC, there is almost no information regarding CCK+ INs in these species. Therefore, in the present study the distribution and morphology of CCK+ INs and their axon terminals in the BNC of the monkey was investigated. CCK immunoreactivity in the BNC was observed in somata and proximal dendrites of nonpyramidal neurons, as well as in axon terminals. A moderate density of CCK+ INs was found in all nuclei of the BNC. CCK+ INs in the BNC were morphologically heterogeneous, with both small and large varieties observed. All CCK+ somata gave rise to 2–4 dendrites that branched sparingly and were aspiny. CCK+ axon terminals in the BNC were found both in the neuropil and forming pericellular baskets contacting somata of pyramidal cells. In addition, many CCK+ neurons were contacted by multiple CCK+ terminals, indicative of the existence of a CCK interneuronal network. These data indicate that the morphology of CCK+ INs in the monkey is very similar to that of the rat.

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“…Both ultrastructural and electrophysiological studies have shown that the rodent BNC contains a network of PV+ interneurons interconnected by chemical and gap‐junctional electrical synapses (Muller et al, ; Woodruff & Sah, ). Applying a combination of optogenetics, electrophysiology, and high‐resolution microscopy allowed Andrási et al () to demonstrate that actually both PV+ and CCK+ basket cells form separate networks that are interconnected by chemical synapses and gap junctions. However, both types of basket cells synapse with PV+ AACs.…”

Section: Discussionmentioning

confidence: 99%

Nonpyramidal neurons in the primate basolateral amygdala: A Golgi study in the baboon (Papio cynocephalus) and long‐tailed macaque (Macaca fascicularis)

McDonald

Augustine

2019

J of Comparative Neurology

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Nonpyramidal GABAergic interneurons in the basolateral nuclear complex (BNC) of the amygdala are critical for the regulation of emotion. Remarkably, there have been no Golgi studies of these neurons in nonhuman primates. Therefore, in the present study we investigated the morphology of nonpyramidal neurons (NPNs) in the BNC of the baboon and monkey using the Golgi technique. NPNs were scattered throughout all nuclei of the BNC and had aspiny or spine‐sparse dendrites. NPNs were morphologically heterogeneous and could be divided into small, medium, large, and giant types based on the size of their somata. NPNs could be further divided on the basis of their somatodendritic morphology into four types: multipolar, bitufted, bipolar, and irregular. NPN axons, when stained, formed dense local arborizations that overlapped their dendritic fields to varying extents. These axons always exhibited varying numbers of varicosities representing axon terminals. Three specialized NPN subtypes were recognized because of their unique anatomical features: axo‐axonic cells, neurogliaform cells, and giant cells. The axons of axo‐axonic cells formed “axonal cartridges,” with clustered varicosities that contacted the axon initial segments of pyramidal neurons (PNs). Neurogliaform cells had small somata and numerous short dendrites that formed a dense dendritic arborization; they also exhibited a very dense axonal arborization that overlapped the dendritic field. Giant cells had very large irregular somata and long, thick dendrites; their distal dendrites often branched extensively and had long appendages. In general, the NPNs of the baboon and monkey BNC, including the specialized subtypes, were similar to those of rodents.

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Differential excitatory control of 2 parallel basket cell networks in amygdala microcircuits

Cited by 34 publications

References 76 publications

Vasoactive Intestinal Polypeptide-Immunoreactive Interneurons within Circuits of the Mouse Basolateral Amygdala

Vasoactive Intestinal Polypeptide-Immunoreactive Interneurons within Circuits of the Mouse Basolateral Amygdala

Cholecystokinin immunoreactive neurons in the basolateral amygdala of the rhesus monkey (Macaca mulatta)

Nonpyramidal neurons in the primate basolateral amygdala: A Golgi study in the baboon (Papio cynocephalus) and long‐tailed macaque (Macaca fascicularis)

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