Connectional Modularity of Top-Down and Bottom-Up Multimodal Inputs to the Lateral Cortex of the Mouse Inferior Colliculus

Lesicko, Alexandria M.H.; Hristova, Teodora; Maigler, Kathleen C.; Llano, Daniel A.

doi:10.1523/jneurosci.4134-15.2016

Cited by 87 publications

(128 citation statements)

References 67 publications

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“…Adjacent sections throughout the rostrocaudal extent of the LCIC were stained to determine if the histochemical markers were in relative alignment, thus staining the same modular set. One previous experiment in P8 mice showed that GAD and CO modules are aligned (Lesicko et al, ). This study expands on this finding by examining the co‐registry of NADPH‐d with CO and AChE.…”

Section: Resultsmentioning

confidence: 99%

“…The inferior colliculus (IC) is typically portrayed as a midbrain relay hub in the ascending auditory system. This depiction, while fitting for its tonotopically‐arranged central nucleus (CNIC), does not aptly describe its surrounding shell nuclei (the lateral cortex of the IC, LCIC, and the dorsal cortex of the IC, DCIC), that receive a rich array of multimodal inputs (Coleman & Clerici, ; Gruters & Groh, ; Lesicko, Hristova, Maigler, & Llano, ). Many of these projections specifically target the LCIC and exhibit highly compartmentalized terminal distributions in a variety of species (Stebbings, Lesicko, & Llano, ).…”

Section: Introductionmentioning

confidence: 99%

“…Many of these projections specifically target the LCIC and exhibit highly compartmentalized terminal distributions in a variety of species (Stebbings, Lesicko, & Llano, ). Somatosensory and auditory afferents, in particular, appear largely segregated in the adult mouse LCIC (Lesicko et al, ). Somatosensory inputs ascending from the spinal trigeminal and dorsal column nuclei in the brainstem, along with descending projections from somatosensory cortex, terminate within a discontinuous patchy or modular LCIC layer 2 lattice.…”

Section: Introductionmentioning

confidence: 99%

“…This recently described LCIC connectional modularity appears to correlate with previous reports of an underlying neurochemical framework. A distinct set of LCIC modules that span layer 2 have been most thoroughly described in the adult rat (Chernock, Larue, & Winer, ) and mouse (Lesicko et al, ; Stebbings et al, ) for a variety of markers, including acetylcholinesterase (AChE), nicotinamide adenine dinucleotide phosphate‐diaphorase (NADPH‐d), cytochrome oxidase (CO), glutamic acid decarboxylase (GAD), and parvalbumin (PV). Analogous markers that emphasize surrounding LCIC extramodular zones, however, have yet to be identified.…”

Section: Introductionmentioning

confidence: 99%

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Modular‐extramodular organization in developing multisensory shell regions of the mouse inferior colliculus

Dillingham

Behrooz

Gabriele

2017

J of Comparative Neurology

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The complex neuroanatomical connections of the inferior colliculus (IC) and its major subdivisions offer a juxtaposition of segregated processing streams with distinct organizational features. While the tonotopically layered central nucleus is well-documented, less is known about functional compartments in the neighboring lateral cortex (LCIC). In addition to a laminar framework, LCIC afferent-efferent patterns suggest a multimodal mosaic, consisting of a patchy modular network with surrounding extramodular domains. This study utilizes several neurochemical markers that reveal an emerging LCIC modular-extramodular microarchitecture. In newborn and post-hearing C57BL/6J and CBA/CaJ mice, histochemical and immunocytochemical stains were performed for acetylcholinesterase (AChE), nicotinamide adenine dinucleotide phosphate-diaphorase (NADPH-d), glutamic acid decarboxylase (GAD), cytochrome oxidase (CO), and calretinin (CR). Discontinuous layer 2 modules are positive for AChE, NADPH-d, GAD, and CO throughout the rostrocaudal LCIC. While not readily apparent at birth, discrete cell clusters emerge over the first postnatal week, yielding an identifiable modular network prior to hearing onset. Modular boundaries continue to become increasingly distinct with age, as surrounding extramodular fields remain largely negative for each marker. Alignment of modular markers in serial sections suggests each highlight the same periodic patchy network throughout the nascent LCIC. In contrast, CR patterns appear complementary, preferentially staining extramodular LCIC zones. Double-labeling experiments confirm that NADPH-d, the most consistent developmental modular marker, and CR label separate, nonoverlapping LCIC compartments. Determining how this emerging modularity may align with similar LCIC patch-matrix-like Eph/ephrin guidance patterns, and how each interface with, and potentially influence developing multimodal LCIC projection configurations is discussed.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Modular‐extramodular organization in developing multisensory shell regions of the mouse inferior colliculus

Dillingham

Behrooz

Gabriele

2017

J of Comparative Neurology

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“…Interestingly, the nBIC/ECIC comprises GAD67‐positive neurochemical modules, which are thought to receive axonal terminations predominantly from somatosensory structures (somatosensory cortex and dorsal column nuclei), while the auditory inputs (from the auditory cortex and the ICc) terminate in the extramodular zones (Lesicko et al . ). Furthermore, a recent study identified an excitatory auditory pathway from the ECIC extramodular zones to the SC in the mouse (Lesicko & Llano, ).…”

Section: Discussionmentioning

confidence: 97%

Complex and spatially segregated auditory inputs of the mouse superior colliculus

Bednárová

Grothe

Myoga

2018

The Journal of Physiology

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Key points Although the visual circuits in the superior colliculus (SC) have been thoroughly examined, the auditory circuits lack equivalent scrutiny.SC neurons receiving auditory inputs in mice were characterized and three distinguishable types of neurons were found.The auditory pathways from external nuclei of the inferior colliculus (IC) were characterized, and a novel direct inhibitory connection and an excitation that drives feed‐forward inhibitory circuits within the SC were found.The direct excitatory and inhibitory inputs exhibited distinct arbourization patterns in the SC.These findings suggest functional differences between excitatory and inhibitory sensory information that targets the auditory SC. AbstractThe superior colliculus (SC) is a midbrain structure that integrates auditory, somatosensory and visual inputs to drive orientation movements. While much is known about how visual information is processed in the superficial layers of the SC, little is known about the SC circuits in the deep layers that process auditory inputs. We therefore characterized intrinsic neuronal properties in the auditory‐recipient layer of the SC (stratum griseum profundum; SGP) and confirmed three electrophysiologically defined clusters of neurons, consistent with literature from other SC layers. To determine the types of inputs to the SGP, we expressed Channelrhodopsin‐2 in the nucleus of the brachium of the inferior colliculus (nBIC) and external cortex of the inferior colliculus (ECIC) and optically stimulated these pathways while recording from SGP neurons. Probing the connections in this manner, we described a monosynaptic excitation that additionally drives feed‐forward inhibition via circuits intrinsic to the SC. Moreover, we found a profound long‐range monosynaptic inhibition in 100% of recorded SGP neurons, a surprising finding considering that only about 15% of SGP‐projecting neurons in the nBIC/ECIC are inhibitory. Furthermore, we found spatial differences in the cell body locations as well as axon trajectories between the monosynaptic excitatory and inhibitory inputs, suggesting that these inputs may be functionally distinct. Taking this together with recent anatomical evidence suggesting an auditory excitation from the nBIC and a GABAergic multimodal inhibition from the ECIC, we propose that sensory integration in the SGP is more multifaceted than previously thought.

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Approaches to Understanding Multisensory Dysfunction in Autism Spectrum Disorder

2020

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Abnormal sensory responses are a DSM‐5 symptom of autism spectrum disorder (ASD), and research findings demonstrate altered sensory processing in ASD. Beyond difficulties with processing information within single sensory domains, including both hypersensitivity and hyposensitivity, difficulties in multisensory processing are becoming a core issue of focus in ASD. These difficulties may be targeted by treatment approaches such as “sensory integration,” which is frequently applied in autism treatment but not yet based on clear evidence. Recently, psychophysical data have emerged to demonstrate multisensory deficits in some children with ASD. Unlike deficits in social communication, which are best understood in humans, sensory and multisensory changes offer a tractable marker of circuit dysfunction that is more easily translated into animal model systems to probe the underlying neurobiological mechanisms. Paralleling experimental paradigms that were previously applied in humans and larger mammals, we and others have demonstrated that multisensory function can also be examined behaviorally in rodents. Here, we review the sensory and multisensory difficulties commonly found in ASD, examining laboratory findings that relate these findings across species. Next, we discuss the known neurobiology of multisensory integration, drawing largely on experimental work in larger mammals, and extensions of these paradigms into rodents. Finally, we describe emerging investigations into multisensory processing in genetic mouse models related to autism risk. By detailing findings from humans to mice, we highlight the advantage of multisensory paradigms that can be easily translated across species, as well as the potential for rodent experimental systems to reveal opportunities for novel treatments. Lay Summary Sensory and multisensory deficits are commonly found in ASD and may result in cascading effects that impact social communication. By using similar experiments to those in humans, we discuss how studies in animal models may allow an understanding of the brain mechanisms that underlie difficulties in multisensory integration, with the ultimate goal of developing new treatments. Autism Res 2020, 13: 1430–1449. © 2020 International Society for Autism Research, Wiley Periodicals, Inc.

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Connectional Modularity of Top-Down and Bottom-Up Multimodal Inputs to the Lateral Cortex of the Mouse Inferior Colliculus

Cited by 87 publications

References 67 publications

Modular‐extramodular organization in developing multisensory shell regions of the mouse inferior colliculus

Modular‐extramodular organization in developing multisensory shell regions of the mouse inferior colliculus

Complex and spatially segregated auditory inputs of the mouse superior colliculus

Approaches to Understanding Multisensory Dysfunction in Autism Spectrum Disorder

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