Divergent topographic projection of cerebral cortical areas to overlapping cerebellar lobules through distinct regions of the pontine nuclei

Wu, Xuanjing; Sarpong, Gideon A.; Zhang, Jingyun; Sugihara, Izumi

doi:10.1016/j.heliyon.2023.e14352

Cited by 5 publications

(4 citation statements)

References 83 publications

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“…These lobules have orofacial representation in the mossy fiber responses (Welker, 1987) and have been implicated in the sensorimotor coordination in the orofacial areas such as licking (Welsh et al., 1995) and eye blink reflex (Van Ham & Yeo, 1992). These lobules are also the target of the pontocerebellar projection from the central part of the pontine nucleus (Biswas et al., 2019), which relays the projection from the orofacial somatosensory and motor cortices (Wu et al., 2023) and additionally the projection from the Sp5I (Swenson et al., 1984). Thus, direct trigeminal inputs and indirect pontine inputs, both of which mediate signals of orofacial sensorimotor information merge in these cerebellar lobules.…”

Section: Discussionmentioning

confidence: 99%

Single axonal characterization of trigeminocerebellar projection patterns in the mouse

Wang,

Numata,

et al. 2024

J of Comparative Neurology

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The cerebellar projection from the trigeminal nuclear complex is one of the major populations of the cerebellar inputs. Although this projection is essential in cerebellar functional processing and organization, its morphological organization has not been systematically clarified. The present study addressed this issue by lobule‐specific retrograde neuronal labeling and single axonal reconstruction with anterograde labeling. The cerebellar projection arose mainly from the interpolaris subdivision of the spinal trigeminal nucleus (Sp5I) and the principal trigeminal sensory nucleus (Pr5). Although crus II, paramedian lobule, lobule IX, and simple lobule were the major targets, paraflocculus, and other lobules received some projections. Reconstructed single trigeminocerebellar axons showed 77.8 mossy fiber terminals on average often in multiple lobules but no nuclear collaterals. More terminals were located in zebrin‐negative or lightly‐positive compartments than in zebrin‐positive compartments. While Pr5 axons predominantly projected to ipsilateral crus II, Sp5I axons projected either predominantly to crus II and paramedian lobule often bilaterally, or predominantly to lobule IX always ipsilaterally. Lobule IX‐predominant‐type Sp5I neurons specifically expressed Gpr26. Gpr26‐tagged neuronal labeling produced a peculiar mossy fiber distribution, which was dense in the dorsolateral lobule IX and extending transversely to the dorsal median apex in lobule IX. The projection to the cerebellar nuclei was observed in collaterals of ascending Sp5I axons that project to the diencephalon. In sum, multiple populations of trigeminocerebellar projections showed divergent projections to cerebellar lobules. The projection was generally complementary with the pontine projection and partly matched with the reported orofacial receptive field arrangement.

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Section: Discussionmentioning

confidence: 99%

Single axonal characterization of trigeminocerebellar projection patterns in the mouse

Wang,

Numata,

et al. 2024

J of Comparative Neurology

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“…The superior colliculus (homologous to the TeO), GLv, and NOT (homologous to LM) have all been shown to project to the pontine nuclei in mammals (Kratochwil et al., 2017; Ramnani, 2006). Additionally, most regions of the cortex project to the pontine nuclei (Henschke & Pakan, 2020; Kratochwil et al., 2017; Ramnani, 2006; Wu et al., 2023). In birds, both the Wulst and arcopallium, the two main outputs of the pallium, project to the pontine nuclei; however, it is unclear whether the projections from the pallium to the pontine nuclei in birds are as widespread as in mammals.…”

Section: Discussionmentioning

confidence: 99%

Topography of visual and somatosensory inputs to the pontine nuclei in zebra finches (Taeniopygia guttata)

Gaede,

Gutiérrez‐Ibáñez,

et al. 2023

J of Comparative Neurology

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Birds have a comprehensive network of sensorimotor projections extending from the forebrain and midbrain to the cerebellum via the pontine nuclei, but the organization of these circuits in the pons is not thoroughly described. Inputs to the pontine nuclei include two retinorecipient areas, nucleus lentiformis mesencephali (LM) and nucleus of the basal optic root (nBOR), which are important structures for analyzing optic flow. Other crucial regions for visuomotor control include the retinorecipient ventral lateral geniculate nucleus (GLv), and optic tectum (TeO). These visual areas, together with the somatosensory area of the anterior (rostral) Wulst, which is homologous to the primary somatosensory cortex in mammals, project to the medial and lateral pontine nuclei (PM, PL). In this study, we used injections of fluorescent tracers to study the organization of these visual and somatosensory inputs to the pontine nuclei in zebra finches. We found a topographic organization of inputs to PM and PL. The PM has a lateral subdivision that predominantly receives projections from the ipsilateral anterior Wulst. The medial PM receives bands of inputs from the ipsilateral GLv and the nucleus laminaris precommisulis, located medial to LM. We also found that the lateral PL receives a strong ipsilateral projection from TeO, while the medial PL and region between the PM and PL receive less prominent projections from nBOR, bilaterally. We discuss these results in the context of the organization of pontine inputs to the cerebellum and possible functional implications of diverse somato‐motor and visuomotor inputs and parcellation in the pontine nuclei.

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“…Regarding the relationship between the cerebral cortex and cerebellum, it has been reported that the topography of the cortex is maintained particularly in the outputs from the pontine nuclei (Wu, Sarpong et al 2023). However, this topography may be largely disrupted from granule cells to PCs (Pisano, Dhanerawala et al 2021).…”

Section: Spiking Neural Network Reproducing Representative Activity O...mentioning

confidence: 99%

“…3). Conversely, although recent studies have provided essential knowledge (Kebschull, Richman et al 2020, Pisano, Dhanerawala et al 2021, Wu, Sarpong et al 2023, because of limited projectome data of the cerebro-cerebellar loop circuit at a subdivision level (for instance, at the level of the microzone (Sugihara, Fujita et al 2009)), we modeled only a part of the cerebellar network with known anatomical connections. We set the conduction delay of each connection as shown in Extended Data As an input from the cerebral cortex, we simulated a Poisson spike train as a spiking activity of association cortex (N = 600 neurons).…”

Section: Simulation Of a Spiking Neural Networkmentioning

confidence: 99%

Synergistic reinforcement learning by cooperation of the cerebellum and basal ganglia

Yoshida,

Sugino,

Yamamoto

et al. 2024

Preprint

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The cerebral cortex, cerebellum, and basal ganglia play a central role in flexible learning in mammals. However, how these three structures work together is not fully understood. Recently, it has been suggested that reinforcement learning may be implemented not only in the basal ganglia but also in the cerebellum, as the activity of cerebellar climbing fibers represents reward prediction error. If the same learning mechanism via reward prediction error occurs simultaneously in the basal ganglia and cerebellum, it remains unclear how these two regions co-function. Here, we recorded neuronal activity in the output of cerebellum and basal ganglia, the cerebellar nuclei and substantia nigra pars reticulata, respectively, from ChR2 transgenic rats with high-density Neuropixels probes while optogenetically stimulating the cerebral cortex point-by-point. The temporal response patterns could be categorized into two classes in both cerebellar nuclei and substantia nigra pars reticulata. Among them, the fast excitatory response of the cerebellar nuclei due to the input of mossy fibers and the inhibitory response of the substantia nigra pars reticulata via the direct pathway were synchronized. This coincidence, reproduced in a spiking network simulation based on connectome data, was expected to synchronously activate the cerebral cortex via the thalamus. To further investigate the significance of this synchronous positive feedback, we constructed a reservoir model that mimics the time course of the activity dynamics of cerebral cortex and temporal responses of cerebellar nuclei and substantia nigra pars reticulata. Plasticity of both parallel fiber inputs to Purkinje cell and corticostriatal synapses onto the striatal neurons of the direct pathway was essential for successful learning of a reinforcement learning task. Notably, learning was inhibited when the timing of the cerebellar or basal ganglia output was delayed from the real data by 10 ms; the larger this delay, the slower the learning rate. This necessary temporal precision was observed only when the cerebral cortex operated in the β-to-γ frequency range. These results indicate that coordinated output of the cerebellum and basal ganglia, with input from the cerebral cortex in a narrow frequency band, facilitates brain-wide synergistic reinforcement learning. Thus, our findings contribute to a holistic understanding of the interactions among the cerebellum, basal ganglia, and cerebral cortex.

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Divergent topographic projection of cerebral cortical areas to overlapping cerebellar lobules through distinct regions of the pontine nuclei

Cited by 5 publications

References 83 publications

Single axonal characterization of trigeminocerebellar projection patterns in the mouse

Single axonal characterization of trigeminocerebellar projection patterns in the mouse

Topography of visual and somatosensory inputs to the pontine nuclei in zebra finches (Taeniopygia guttata)

Synergistic reinforcement learning by cooperation of the cerebellum and basal ganglia

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