Descending Axonal Projections from the Inferior Colliculus Target Nearly All Excitatory and Inhibitory Cell Types of the Dorsal Cochlear Nucleus

Balmer, Timothy S.; Trussell, Laurence O.

doi:10.1523/jneurosci.1190-21.2022

“…UBCs are also present in the dorsal cochlear nucleus, a cerebellum-like circuit in the auditory brainstem of mammals. Like granule cells in the dorsal cochlear nucleus, UBCs receive multisensory signals from various sources ( Ryugo et al, 2003 ; Balmer and Trussell, 2021b ; Balmer and Trussell, 2022 ). In order to test whether our findings about the identity of UBCs labeled in GRP-cre and P079 mice are generalizable across UBC populations, we examined their distribution in the dorsal cochlear nucleus.…”

Section: Resultsmentioning

confidence: 99%

A system of feed-forward cerebellar circuits that extend and diversify sensory signaling

Hariani,

Algstam,

Candler

et al. 2024

eLife

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Sensory signals are processed by the cerebellum to coordinate movements. Numerous cerebellar functions are thought to require the maintenance of a sensory representation that extends beyond the input signal. Granule cells receive sensory input, but they do not prolong the signal and are thus unlikely to maintain a sensory representation for much longer than the inputs themselves. Unipolar brush cells (UBCs) are excitatory interneurons that project to granule cells and transform sensory input into prolonged increases or decreases in firing, depending on their ON or OFF UBC subtype. Further extension and diversification of the input signal could be produced by UBCs that project to one another, but whether this circuitry exists is unclear. Here we test whether UBCs innervate one another and explore how these small networks of UBCs could transform spiking patterns. We characterized two transgenic mouse lines electrophysiologically and immunohistochemically to confirm that they label ON and OFF UBC subtypes and crossed them together, revealing that ON and OFF UBCs innervate one another. A Brainbow reporter was used to label UBCs of the same ON or OFF subtype with different fluorescent proteins, which showed that UBCs innervate their own subtypes as well. Computational models predict that these feed-forward networks of UBCs extend the length of bursts or pauses and introduce delays—transformations that may be necessary for cerebellar functions from modulation of eye movements to adaptive learning across time scales. The cerebellum is essential for the accurate performance of behaviors ranging in complexity from stabilizing an image on the retina to playing a piano or performing a gymnastics routine. Cerebellar dysfunction disrupts the ability to produce smooth movements and leads to a disorder called ataxia. Damage to the vestibular cerebellum occurs in various disorders including medulloblastoma and leads to nystagmus, involuntary movements of the eyes that prevent normal vision. Treating disorders of motor control such as nystagmus, requires a better understanding of how representations of movements are maintained in the firing patterns of neurons in the cerebellar circuit. Here we use transgenic mice to label a type of neuron called the unipolar brush cell and revealed that these cells innervate one another and are likely to increase the length and diversity of spiking patterns in the cerebellum. These transformations may be necessary for numerous functions from controlling eye movements to learning new behaviors.

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“…UBCs are also present in the dorsal cochlear nucleus, a cerebellum-like circuit in the auditory brainstem of mammals. Like granule cells in the dorsal cochlear nucleus, UBCs receive multisensory signals from various sources (Ryugo et al, 2003; Balmer and Trussell, 2021, 2022). In order to test whether our findings about the identity of UBCs labeled in GRP-cre and P079 mice is generalizable across UBC populations, we examined their distribution in the dorsal cochlear nucleus.…”

Section: Resultsmentioning

confidence: 99%

A system of feed-forward cerebellar circuits that extend and diversify sensory signaling

Hariani

¹

,

Algstam

²

,

Candler

³

et al. 2023

Preprint

Self Cite

0

View full text Add to dashboard Cite

Sensory signals are processed by the cerebellum to coordinate movements. Numerous cerebellar functions are thought to require the maintenance of a sensory representation that extends beyond the input signal. Granule cells receive sensory input, but they do not prolong the signal and are thus unlikely to maintain a sensory representation for much longer than the inputs themselves. Unipolar brush cells (UBCs) are excitatory interneurons that project to granule cells and transform sensory input into prolonged increases or decreases in firing, depending on their ON or OFF UBC subtype. Further extension and diversification of the input signal could be produced by UBCs that project to one another, but whether this circuitry exists is unclear. Here we test whether UBCs innervate one another and explore how these small networks of UBCs could transform spiking patterns. We characterized two transgenic mouse lines electrophysiologically and immunohistochemically to confirm that they label ON and OFF UBC subtypes and crossed them together, revealing that ON and OFF UBCs innervate one another. A Brainbow reporter was used to label UBCs of the same ON or OFF subtype with different fluorescent proteins, which showed that UBCs innervate their own subtypes as well. Computational models predict that these feed-forward networks of UBCs extend the length of bursts or pauses and introduce delays—transformations that may be necessary for cerebellar functions from modulation of eye movements to adaptive learning across time scales.

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“…For example, the superior colliculus, a brain region involved in controlling eye movements, projects to the inferior colliculus (IC), an auditory structure (Coleman and Clerici, 1987; Sparks and Hartwich-Young, 1989). Auditory signals in both the SC and the IC are sensitive to changes in eye position (SC: (Jay and Sparks, 1984, 1987b, a; Hartline et al, 1995; Zella et al, 2001; Populin et al, 2004; Lee and Groh, 2012); IC: (Groh et al, 2001; Zwiers et al, 2004; Porter et al, 2006; Bulkin and Groh, 2012b, a; Willett et al, 2019), and the IC conveys descending projections to both the superior olivary complex (Faye-Lund, 1986), the source of descending input to the outer hair cells (Guinan, 2006; Ciuman, 2010) and the cochlear nucleus (Milinkeviciute et al, 2017; Balmer and Trussell, 2022) which in turn projects to the facial and trigeminal nerves that innervate the stapedius and tensor tympani respectively (Mukerji et al, 2010). Preliminary findings from our group are consistent with a role for all three of these types of motor actuators in the generation of EMREOs (King et al, 2023).…”

Section: Discussionmentioning

confidence: 99%

Conserved features of eye movement related eardrum oscillations (EMREOs) across humans and monkeys

Lovich

¹

,

King

²

,

Murphy

³

et al. 2023

Preprint

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Auditory and visual information involve different coordinate systems, with auditory spatial cues anchored to the head and visual spatial cues anchored to the eyes. Information about eye movements is therefore critical for reconciling visual and auditory spatial signals. The recent discovery of eye movement-related eardrum oscillations (EMREOs) suggests that this process could begin as early as the auditory periphery. How this reconciliation might happen remains poorly understood. Because humans and monkeys both have mobile eyes and therefore both must perform this shift of reference frames, comparison of the EMREO across species can provide insights to shared and therefore important parameters of the signal. Here we show that rhesus monkeys, like humans, have a consistent, significant EMREO signal that carries parametric information about eye displacement as well as onset times of eye movements. The dependence of the EMREO on the horizontal displacement of the eye is its most consistent feature, and is shared across behavioral tasks, subjects, and species. Differences chiefly involve the waveform frequency, and may relate at least in part to differences in the speed of eye movements across species.

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Descending Axonal Projections from the Inferior Colliculus Target Nearly All Excitatory and Inhibitory Cell Types of the Dorsal Cochlear Nucleus

Cited by 17 publications

References 45 publications

A system of feed-forward cerebellar circuits that extend and diversify sensory signaling

A system of feed-forward cerebellar circuits that extend and diversify sensory signaling

A system of feed-forward cerebellar circuits that extend and diversify sensory signaling

Conserved features of eye movement related eardrum oscillations (EMREOs) across humans and monkeys

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