Perineuronal nets and GABAergic cells in the inferior colliculus of guinea pigs

Foster, Nichole L; Mellott, Jeffrey G.; Schofield, Brett R.

doi:10.3389/fnana.2013.00053

Cited by 28 publications

(39 citation statements)

References 52 publications

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“…GABA‐positive neurons have been found in the IC of the rat (Roberts and Ribak, ), bat (Vater et al, ), cat (Winer et al, ), gerbil (Gleich et al, ), guinea pig (Foster et al, ), and mouse (Ono et al, ), in which they make up roughly 20–25% of both stellate and disc‐shaped neurons (cat: Oliver et al, ; bat: Winer et al, ; rat: Merchan et al, ). Our colabeling results in GAD67–EGFP mice demonstrate that GABAergic neurons in the IC do not send descending projections to the DCN in the mouse, suggesting that they are excitatory, a conclusion consistent with what has been reported for guinea pig (Ostapoff et al, ).…”

Section: Discussionmentioning

confidence: 99%

Descending projections from the inferior colliculus to the dorsal cochlear nucleus are excitatory

Milinkeviciute

Muniak

Ryugo

2016

J of Comparative Neurology

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Ascending projections of the dorsal cochlear nucleus (DCN) target primarily the contralateral inferior colliculus (IC). In turn, the IC sends bilateral descending projections back to the DCN. We sought to determine the nature of these descending axons in order to infer circuit mechanisms of signal processing at one of the earliest stages of the central auditory pathway. An anterograde tracer was injected in the IC of CBA/Ca mice to reveal terminal characteristics of the descending axons. Retrograde tracer deposits were made in the DCN of CBA/Ca and transgenic GAD67-EGFP mice to investigate the cells giving rise to these projections. A multiunit best frequency was determined for each injection site. Brains were processed by using standard histologic methods for visualization and examined by fluorescent, brightfield, and electron microscopy. Descending projections from the IC were inferred to be excitatory because the cell bodies of retrogradely labeled neurons did not colabel with EGFP expression in neurons of GAD67-EGFP mice. Furthermore, additional experiments yielded no glycinergic or cholinergic positive cells in the IC, and descending projections to the DCN were colabeled with antibodies against VGluT2, a glutamate transporter. Anterogradely labeled endings in the DCN formed asymmetric postsynaptic densities, a feature of excitatory neurotransmission. These descending projections to the DCN from the IC were topographic and suggest a feedback pathway that could underlie a frequency-specific enhancement of some acoustic signals and suppression of others. The involvement of this IC-DCN circuit is especially noteworthy when considering the gating of ascending signal streams for auditory processing. J. Comp. Neurol. 525:773-793, 2017. © 2016 Wiley Periodicals, Inc.

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Section: Discussionmentioning

confidence: 99%

Descending projections from the inferior colliculus to the dorsal cochlear nucleus are excitatory

Milinkeviciute

Muniak

Ryugo

2016

J of Comparative Neurology

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“…More recent evidence indicates that WFA-labeled PNNs are associated with more heterogeneous neuronal phenotypes than previously thought, including several subgroups of interneurons, a small subset of cortico-cortical pyramidal cells, spinal cord motor neurons and cerebellum Purkinje cells (Ajmo et al, 2008; Brauer et al, 1995; Bruckner et al, 1993; Gati and Lendvai, 2013; Hartig et al, 1995; Pantazopoulos et al, 2006; Seeger et al, 1994; Wegner et al, 2003). Among these, GABAergic neurons undoubtedly represent one of the largest populations in several brain regions, including several cortical areas, striatum, hippocampus, inferior colliculus, septum and amygdala (Foster et al, 2014; Hartig et al, 1994; Lee et al, 2012; Pantazopoulos et al, 2006; Seeger et al, 1996; Shah and Lodge, 2013). As an example, in the amygdala of rhesus monkey, the overwhelming majority of WFA-positive PNNs ensheath neurons expressing glutamic acid decarboxylase (GAD), a typical marker for GABAergic neurons, with many of these neurons also expressing PVB and/or calbindin (Hartig et al, 1995).…”

Section: Perineuronal Nets: Composition and Association With Distimentioning

confidence: 99%

Losing the sugar coating: Potential impact of perineuronal net abnormalities on interneurons in schizophrenia

Berretta

Pantazopoulos

Markota

et al. 2015

Schizophrenia Research

133

119

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Perineuronal nets (PNNs) were shown to be markedly altered in subjects with schizophrenia. In particular, decreases of PNNs have been detected in the amygdala, entorhinal cortex and prefrontal cortex. The formation of these specialized extracellular matrix (ECM) aggregates during postnatal development, their functions and association with distinct populations of GABAergic interneurons, bear great relevance to the pathophysiology of schizophrenia. PNNs gradually mature in an experience-dependent manner during late stages of postnatal development, overlapping with the prodromal period/age of onset of schizophrenia. Throughout adulthood, PNNs regulate neuronal properties, including synaptic remodeling, cell membrane compartmentalization and subsequent regulation of glutamate receptors and calcium channels, and susceptibility to oxidative stress. With the present paper, we discuss evidence for PNN abnormalities in schizophrenia, the potential functional impact of such abnormalities on inhibitory circuits and, in turn, cognitive and emotion processing. We integrate these considerations with results from recent genetic studies showing genetic susceptibility for schizophrenia associated with genes encoding for PNN components, matrix-regulating molecules and immune system factors. Notably, the composition of PNNs is regulated dynamically in response to factors such as fear, reward, stress, and immune response. This regulation occurs through families of matrix metalloproteinases that cleave ECM components, altering their functions and affecting plasticity. Several metalloproteinases have been proposed as vulnerability factors for schizophrenia. We speculate that the physiological process of PNN remodeling may be disrupted in schizophrenia as a result of interactions between matrix remodeling processes and immune system dysregulation. In turn, these mechanisms may contribute to dysfunction of GABAergic neurons.

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“…Further detailed classification of cell type would help to clarify information coding, since GLU cells appear to have a wide variety of morphological and physiological properties, and GABAergic cells can be further subdivided by the presence of perineuronal nets (Foster et al . ; Beebe et al . ).…”

Section: Discussionmentioning

confidence: 99%

“…LG cells may elicit more stable responses than GLU cells, since LG cells have fewer spines, as shown in the current study, and are covered by perineuronal nets (Foster et al . ), both of which have been suggested as leading to lower plastic abilities. IC GABAergic neurons can be classified into four types using the presence/absence of VGLUT2+ axosomatic rings and perineuronal nets (Beebe et al .…”

Section: Discussionmentioning

confidence: 99%

Different coding strategy of sound information between GABAergic and glutamatergic neurons in the auditory midbrain

Ito

2020

The Journal of Physiology

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Key points In the central nucleus of the inferior colliculus (ICC), which acts as the hub of the auditory pathways, how the sound is coded by distinct cell types is largely unknown. Large GABAergic cells are tuned broadly to pure tones and respond more strongly to frequency‐modulated sweeps than small GABAergic and glutamatergic (GLU) cells. Neurons, especially GLU cells, which share sharpness of tuning and sweep sensitivity, were spatially clustered inside the ICC. The difference in responsiveness between cell types was partially explained by the morphology of dendritic trees and the spatial distributions of excitatory and inhibitory inputs. The results suggest that each ICC cell type has a particular sound‐encoding strategy, which is partially determined by the morphological characteristics and location of cells, and contributes information coding in higher centres in different ways. Abstract The rules governing the encoding of sound information in the higher auditory centres are largely unknown. In the central nucleus of the inferior colliculus (ICC), which acts as the hub of the auditory pathways, the presence of functional maps other than tonotopicity has been suggested but not established, due to significant heterogeneity in the response properties of single microdomains. Since each ICC cell type has distinct neuronal circuitry, each cell type might encode sound information differently. Here, juxtacellular recording from rat ICC of both sexes revealed that large GABAergic (LG), small GABAergic (SG) and glutamatergic (GLU) cells encode sound information differently. LG cells are broadly tuned and respond more strongly to frequency‐modulated sweeps than SG and GLU cells. At a population level, responsiveness to sweeps is location dependent: the responsiveness to sweeps is shared in local clusters of GLU cells, whereas that to directional selectivity of sweeps is shared in local clusters of LG cells. The difference in responsiveness between cell types was partially explained by the morphology of dendritic trees and the spatial distributions of excitatory and inhibitory inputs. LG neurons had a dense local axonal plexus with projection fibres to multiple distant targets, whereas GLU projection neurons mainly aimed at a single, distant target and had less dense local collaterals. These results suggest that each ICC cell type has a particular sound‐encoding strategy, which is partially determined by the morphological characteristics and location of the cell, and the different cell types contribute information coding in higher centres in different ways.

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Perineuronal nets and GABAergic cells in the inferior colliculus of guinea pigs

Cited by 28 publications

References 52 publications

Descending projections from the inferior colliculus to the dorsal cochlear nucleus are excitatory

Descending projections from the inferior colliculus to the dorsal cochlear nucleus are excitatory

Losing the sugar coating: Potential impact of perineuronal net abnormalities on interneurons in schizophrenia

Different coding strategy of sound information between GABAergic and glutamatergic neurons in the auditory midbrain

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