Inhibitory Projections from the Inferior Colliculus to the Medial Geniculate body Originate from Four Subtypes of GABAergic Cells

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

doi:10.1523/eneuro.0406-18.2018

Cited by 21 publications

(14 citation statements)

References 43 publications

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“…In many brain regions, GABAergic neurons are interneurons (Tremblay et al, 2016), but in the IC, GABAergic cells contribute substantially to long-range projections to the MG and other targets (Winer et al, 1996;Peruzzi et al, 1997;St. Marie et al, 1997;Ito et al, 2009;Mellott et al, 2014Mellott et al, , 2018Beebe et al, 2018). The projection to MG is particularly interesting because other regions of primary sensory thalamus do not receive ascending inhibitory input (Halassa and Acsády, 2016).…”

Section: Npy Neurons Include Gabaergic Projection Neuronsmentioning

confidence: 99%

Neuropeptide Y Expression Defines a Novel Class of GABAergic Projection Neuron in the Inferior Colliculus

et al. 2020

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Located in the midbrain, the inferior colliculus (IC) integrates information from numerous auditory nuclei and is an important hub for sound processing. Despite its importance, little is known about the molecular identity and functional roles of defined neuron types in the IC. Using a multifaceted approach in mice of both sexes, we found that neuropeptide Y (NPY) expression identifies a major class of inhibitory neurons, accounting for approximately one-third of GABAergic neurons in the IC. Retrograde tracing showed that NPY neurons are principal neurons that can project to the medial geniculate nucleus. In brain slice recordings, many NPY neurons fired spontaneously, suggesting that NPY neurons may drive tonic inhibition onto postsynaptic targets. Morphologic reconstructions showed that NPY neurons are stellate cells, and the dendrites of NPY neurons in the tonotopically organized central nucleus of the IC cross isofrequency laminae. Immunostaining confirmed that NPY neurons express NPY, and we therefore hypothesized that NPY signaling regulates activity in the IC. In crosses between Npy1r cre and Ai14 Cre-reporter mice, we found that NPY Y 1 receptor (Y 1 R)-expressing neurons are glutamatergic and were broadly distributed throughout the rostrocaudal extent of the IC. In whole-cell recordings, application of a high-affinity Y 1 R agonist led to hyperpolarization in most Y 1 R-expressing IC neurons. Thus, NPY neurons represent a novel class of inhibitory principal neurons that are well poised to use GABAergic and NPY signaling to regulate the excitability of circuits in the IC and auditory thalamus.

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Section: Npy Neurons Include Gabaergic Projection Neuronsmentioning

confidence: 99%

Neuropeptide Y Expression Defines a Novel Class of GABAergic Projection Neuron in the Inferior Colliculus

et al. 2020

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“…Around one-fourth of neurons in the IC are GABAergic (Schofield and Beebe, 2019). In particular the large GABAergic neurons seem to form a distinct subclass (Ito et al, 2009; Ito and Oliver, 2012; Geis and Borst, 2013), but based on histology, at least four different subclasses of GABAergic neurons can be discriminated, which all contribute to the ascending projections to the medial geniculate body of the thalamus (Beebe et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Tonotopic and non-auditory organization of the mouse dorsal inferior colliculus revealed by two-photon imaging

Wong

Borst

2019

eLife

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The dorsal (DCIC) and lateral cortices (LCIC) of the inferior colliculus are major targets of the auditory and non-auditory cortical areas, suggesting a role in complex multimodal information processing. However, relatively little is known about their functional organization. We utilized in vivo two-photon Ca2+ imaging in awake mice expressing GCaMP6s in GABAergic or non-GABAergic neurons in the IC to investigate their spatial organization. We found different classes of temporal responses, which we confirmed with simultaneous juxtacellular electrophysiology. Both GABAergic and non-GABAergic neurons showed spatial microheterogeneity in their temporal responses. In contrast, a robust, double rostromedial-caudolateral gradient of frequency tuning was conserved between the two groups, and even among the subclasses. This, together with the existence of a subset of neurons sensitive to spontaneous movements, provides functional evidence for redefining the border between DCIC and LCIC.

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“…13B). However, it must be noted about the possibility that the latter type ('local' neurons) may also contain projection neurons with insufficient TMR labelling, since not only LG and GLU cells but also SG cells project to thalamus (Beebe et al 2018). There were no significant differences in any of the physiological response parameters (jitter to noise, jitter to CF tones, peak-trough interval, spike width, latency to CF tones, latency to noise, MT, sweep index and DSI) between the former and latter types of GLU cells (P > 0.05, Student's t test).…”

Section: The Spatial Distribution Of Axons Is Different Between Lg Anmentioning

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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Inhibitory Projections from the Inferior Colliculus to the Medial Geniculate body Originate from Four Subtypes of GABAergic Cells

Cited by 21 publications

References 43 publications

Neuropeptide Y Expression Defines a Novel Class of GABAergic Projection Neuron in the Inferior Colliculus

Neuropeptide Y Expression Defines a Novel Class of GABAergic Projection Neuron in the Inferior Colliculus

Tonotopic and non-auditory organization of the mouse dorsal inferior colliculus revealed by two-photon imaging

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

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