Structural and functional organization of visual responses in the inferior olive of larval zebrafish

Félix, Rita; Markov, Daniil A.; Renninger, Sabine L.; Tomas, Raquel; Laborde, Alexandre; Carey, Megan R.; Orger, Michael B.; Portugues, Rubén

doi:10.1101/2021.11.29.470378

Cited by 4 publications

(5 citation statements)

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“…Here, we undertook a large-scale investigation of the representations of a simple visual stimulus in the olivo-cerebellar system of larval zebrafish at the single-cell level. Previous reports from our lab have been exploring the responses of individual cell types in the cerebellar circuitry (Knogler et al, 2017, 2019; Harmon et al, 2020; Felix et al, 2021). Building on this previous work, we have systematically explored the responses of IONs and GCs to changes in luminance.…”

Section: Discussionmentioning

confidence: 99%

“…Three types of transgenic lines in a nacre ( mitf -/-) (Lister et al, 1999) genetic background were used for functional imaging experiments. For GCs and IONs imaging, a modified fast calcium indicator under the UAS promoter UAS:GCaMP6fEF05, see (Felix et al, 2021)) was expressed either under a GC-specific Tg(gSA2AzGFF152B) (Takeuchi et al, 2015)) or ION-specific (Tg(hspGFFDMC28C), (Takeuchi et al, 2015)) Gal4 promoter. For PC imaging, GCaMP6s was expressed under a direct PC promoter (Tg(PC:GCaMP6f), (Knogler et al, 2019).…”

Section: Methodsmentioning

confidence: 99%

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Comparing the representation of a simple visual stimulus across the cerebellar network

Petrucco

Prat

Portugues

et al. 2022

Preprint

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The cerebellum is a highly conserved structure of the vertebrate central nervous system that plays a role in the timing and calibration of motor sequences. Its function is supported by the convergence of fibers from granule cells (GCs) and inferior olive neurons (IONs) onto Purkinje cells (PCs). Theories of cerebellar function postulate that IONs convey error signals to PCs that, paired with the contextual information provided by GCs, can be used as a teaching signal to guide motor learning. Here, we use the larval zebrafish to investigate (i) how sensory representations of the same stimulus vary across GCs and IONs and (ii) how PC activity reflects these two different input streams. We use population calcium imaging to measure the cell responses to flashes of diverse luminance and duration to show that IONs and GCs encode different stimulus properties. First, most GCs show tonic and graded responses, as opposed to IONs, whose activity peaks only at on and off luminance transitions, in agreement with the notion that GCs and IONs encode context and error information, respectively. Secondly, we show that GC activity is patterned over time: some neurons had sustained responses for the entire duration of the stimulus, while in others activity was ramping up with slow time constants. This suggests that, by performing temporal integration, GCs could provide a basis that PCs may use to decode time. Finally, we show how PC activity can be largely reconstructed by a linear combination of granule cells and inferior olive neurons. Together, our observations give support to the notion of an error signal coming from IONs, and provide the first experimental evidence for a temporal patterning of GC activity over many seconds.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Comparing the representation of a simple visual stimulus across the cerebellar network

Petrucco

Prat

Portugues

et al. 2022

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…Here, we undertook a large-scale investigation of the representations of a simple visual stimulus in the olivocerebellar system of larval zebrafish at the single-cell level. Previous reports have been exploring the responses of individual cell types in the cerebellar circuitry ( Knogler et al, 2017 , 2019 ; Harmon et al, 2020 ; Felix et al, 2021 ). Building on this previous work, we have systematically explored the responses of IONs and GCs to changes in luminance.…”

Section: Discussionmentioning

confidence: 99%

“…Three types of transgenic lines in a nacre ( mitf −/−; Lister et al, 1999 ) genetic background were used for functional imaging experiments. For GC and ION imaging, a modified fast calcium indicator under the UAS promoter UAS:GCaMP6fEF05 ( Felix et al, 2021 ) was expressed either under a GC-specific Tg(gSA2AzGFF152B) ( Takeuchi et al, 2015 ) or ION-specific Tg(hspGFFDMC28C) ( Takeuchi et al, 2015 ) Gal4 promoter. For PC imaging, GCaMP6s was expressed under a direct PC promoter Tg(PC:GCaMP6f) ( Knogler et al, 2019 ).…”

Section: Methodsmentioning

confidence: 99%

Comparing the Representation of a Simple Visual Stimulus across the Cerebellar Network

Prat,

Petrucco,

Štih

et al. 2024

eNeuro

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The cerebellum is a conserved structure of the vertebrate brain involved in the timing and calibration of movements. Its function is supported by the convergence of fibers from granule cells (GCs) and inferior olive neurons (IONs) onto Purkinje cells (PCs). Theories of cerebellar function postulate that IONs convey error signals to PCs that, paired with the contextual information provided by GCs, can instruct motor learning.Here, we use the larval zebrafish to investigate (i) how sensory representations of the same stimulus vary across GCs and IONs and (ii) how PC activity reflects these two different input streams. We use population calcium imaging to measure IONs and GCs responses to flashes of diverse luminance and duration. First, we observe that GCs show tonic and graded responses, as opposed to IONs, whose activity peaks mostly at luminance transitions, consistently with the notion that GCs and IONs encode context and error information, respectively. Secondly, we show that GC activity is patterned over time: some neurons exhibit sustained responses for the entire duration of the stimulus, while in others activity ramps up with slow time constants. This activity could provide a substrate for time representation in the cerebellum. Together, our observations give support to the notion of an error signal coming from IONs and provide the first experimental evidence for a temporal patterning of GC activity over many seconds.Significance statementThe cerebellum is an important brain structure shared by all vertebrates, playing a crucial role in sensorimotor behavior. By using calcium imaging in larval zebrafish, we investigated sensory responses across granule cells (GCs), Purkinje cells. (PCs), and inferior olive neurons (IONs). We describe how GCs show tonic and graded responses, as opposed to IONs, more active at stimulus transition times, confirming the notion that GCs and IONs encode context and error information, respectively. We also show how time could be represented in the cerebellum by patterned activity in GCs. Together, our observations support to the notion of an error signal coming from IONs and provide the first experimental evidence for a temporal patterning of GC activity over many seconds.

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“…PFs, via the modulation of simple spiking and CFs, by triggering calcium influx into PC dendrites, contribute to transient peaks in dF/F signals in PCs (33)(34)(35). CFs are tuned for specific optic flow directions (36) implying that PCs might also show directional tuning when forward or backward optic flow stimuli are presented.…”

Section: Pcs Exhibit Direction-tuned Responses To Optic Flowmentioning

confidence: 99%

Predictive neural computations in the cerebellum contribute to motor planning and faster behavioral responses in larval zebrafish

Narayanan,

Varma,

Thirumalai

2024

Sci. Adv.

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The ability to predict the future based on past experience lies at the core of the brain’s ability to adapt behavior. However, the neural mechanisms that participate in generating and updating predictions are not clearly understood. Further, the evolutionary antecedents and the prevalence of predictive processing among vertebrates are even less explored. Here, we show evidence of predictive processing via the involvement of cerebellar circuits in larval zebrafish. We presented stereotyped optic flow stimuli to larval zebrafish to evoke swims and discovered that lesioning the cerebellum abolished prediction-dependent modulation of swim latency. When expectations of optic flow direction did not match with reality, error signals arrive at Purkinje cells via the olivary climbing fibers, whereas granule cells and Purkinje cells encode signals of expectation. Strong neural representations of expectation correlate with faster swim responses and vice versa. In sum, our results show evidence for predictive processing in nonmammalian vertebrates with the involvement of cerebellum, an evolutionarily conserved brain structure.

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Structural and functional organization of visual responses in the inferior olive of larval zebrafish

Cited by 4 publications

References 48 publications

Comparing the representation of a simple visual stimulus across the cerebellar network

Comparing the representation of a simple visual stimulus across the cerebellar network

Comparing the Representation of a Simple Visual Stimulus across the Cerebellar Network

Predictive neural computations in the cerebellum contribute to motor planning and faster behavioral responses in larval zebrafish

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