Olfactory stimulation induces cerebellar vermis activation during sexual learning in male rats

Hernández-Briones, Z.S.; García-Bañuelos, Paulina; Hernández, Marı́a Elena; López, María-Leonor; Chacón, Armando Martínez; Carrillo, Porfirio; Coria-Ávila, Genaro A.; Manzo, Jorge; García, Luis I.

doi:10.1016/j.nlm.2017.11.003

Cited by 7 publications

(4 citation statements)

References 40 publications

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“…Interestingly, odorant responses have been reported in the cerebellum. Studies in sexually trained male rats found that female bedding or almond smell elicited increased cFos immunoreactive GCs in the vermis compared to rats exposed to clean air 55 . Furthermore, sexual experience increased the number of cFos positive GCs.…”

Section: Discussionmentioning

confidence: 95%

Molecular layer interneurons in the cerebellum encode for valence in associative learning

Futia

Souza

et al. 2020

Nat Commun

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The cerebellum plays a crucial role in sensorimotor and associative learning. However, the contribution of molecular layer interneurons (MLIs) to these processes is not well understood. We used two-photon microscopy to study the role of ensembles of cerebellar MLIs in a go-no go task where mice obtain a sugar water reward if they lick a spout in the presence of the rewarded odorant and avoid a timeout when they refrain from licking for the unrewarded odorant. In naive animals the MLI responses did not differ between the odorants. With learning, the rewarded odorant elicited a large increase in MLI calcium responses, and the identity of the odorant could be decoded from the differential response. Importantly, MLIs switched odorant responses when the valence of the stimuli was reversed. Finally, mice took a longer time to refrain from licking in the presence of the unrewarded odorant and had difficulty becoming proficient when MLIs were inhibited by chemogenetic intervention. Our findings support a role for MLIs in learning valence in the cerebellum.

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Section: Discussionmentioning

confidence: 95%

Molecular layer interneurons in the cerebellum encode for valence in associative learning

Futia

Souza

et al. 2020

Nat Commun

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“…Interestingly, odorant responses have been reported in the cerebellum in rodents and humans. Studies of c-Fos expression found that when sexually trained male rats were exposed to female bedding or almond smell they displayed higher levels of cFos immunoreactive GCs in the vermis compared to rats exposed to clean air 47 . In addition, sexual experience increased the number of cFos positive GCs.…”

Section: Discussionmentioning

confidence: 97%

Molecular layer interneurons in the cerebellum encode for valence in associative learning

Ma¹,

Futia

Ozbay

et al. 2019

Preprint

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24We used two-photon microscopy to study the role of ensembles of cerebellar molecular 25 layer interneurons (MLIs) in a go-no go task where mice obtain a sugar water reward if 26 they lick a spout in the presence of the rewarded odorant and avoid punishment when they 27 restrain from licking for the unrewarded odorant. When the animal was naï ve to the valence 28 of the stimulus (is the odorant rewarded?) responses of the MLIs did not differ between 29 odorants. However, as the animal became proficient, the rewarded odorant elicited a large 30 increase in Ca 2+ in MLIs, and the identity of the odorant could be decoded from the 31 differential response. Importantly, MLIs switched odorant responses when the valence of 32 the stimuli was reversed. Finally, licks diverged more slowly and mice did not become 33 proficient when MLIs were inhibited by chemogenetic intervention. Our findings support 34 a role for MLIs in learning valence in the cerebellum. 35 109response returned to basal levels shortly after the odorant was applied. Fig. 2f shows the 110 mean F/F (+CI) for the last second of odorant application for trials falling within different 111 percent correct performance ranges ( Supplementary Fig. 4). A generalized linear model 112 (GLM) analysis finds a statistically significant interaction between performance and the 113 odorant (S+ vs. S-) (p<0.001, 44 d.f., 4 mice). Therefore, as the animal learns the change 114 in Ca 2+ in MLIs diverges between S+ and S-odorants, suggesting a possible role for MLIs 115 in associative learning. 116 117Finally, we calculated the dimensionality of F/F responses for the MLI cell ensemble. 118The plots in Fig. 1c indicate that odorant responses are fairly uniform for the ROIs in the 119 FOV. In order to provide an estimate of the number of independent components comprising 120 the F/F responsiveness of the ensemble we calculated a quantitative measure of 121 dimensionality 27 (see Methods). Fig. 2g shows the dimensionality for four sessions with a 122 total number of ROIs ranging from 103 to 136. The dimensionality ranged from 2 to 6 and 123 was higher for the pre-odorant period compared to the odorant or reinforcement periods 124 (GLM p<0.01, 18 d.f.). This indicates that Ca 2+ ensemble activity becomes more uniform 125 after addition of the odorant. 126 127 The identity of the stimulus can be decoded from MLI activity after mice learn to 128 differentiate odorants. The finding that the MLIs developed divergent responses for S+ 129 vs. S-trials following learning raised the question whether ensemble neural activity 130 encodes for the identity of the stimulus when the animal becomes proficient differentiating 131 the odorants. The learning curve for a session where the mouse achieves >80% ~60 trials 132 is shown in Fig. 3a. Fig. 3b shows for this session plots of the first two principal 133 components for a principal component analysis (PCA) of F/F values for all MLIs for a 134 subset of trials with percent correct <65% (top, naï ve) or >80% (bottom, proficient) 135 calcul...

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“…Second, the conceptualized network model of SRM inevitably embeds other information, such as the sensory and motor processing during the social recognition task as well as environmental factors, e.g., fear or stress from experimental handlings. While the cerebellum was taken for examining the distribution of fluorescent proteins and not used for c-Fos staining, c-Fos in the vermis can be reactive to external stimuli including odorants 78 . To minimize the variables, all groups were tested under the same conditions and c-Fos counts were normalized to the average value of the control group for each brain region (Figs.…”

Section: Discussionmentioning

confidence: 99%

Social memory deficit caused by dysregulation of the cerebellar vermis

Chao,

Pathak,

Zhang

et al. 2023

Nat Commun

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Social recognition memory (SRM) is a key determinant of social interactions. While the cerebellum emerges as an important region for social behavior, how cerebellar activity affects social functions remains unclear. We selectively increased the excitability of molecular layer interneurons (MLIs) to suppress Purkinje cell firing in the mouse cerebellar vermis. Chemogenetic perturbation of MLIs impaired SRM without affecting sociability, anxiety levels, motor coordination or object recognition. Optogenetic interference of MLIs during distinct phases of a social recognition test revealed the cerebellar engagement in the retrieval, but not encoding, of social information. c-Fos mapping after the social recognition test showed that cerebellar manipulation decreased brain-wide interregional correlations and altered network structure from medial prefrontal cortex and hippocampus-centered to amygdala-centered modules. Anatomical tracing demonstrated hierarchical projections from the central cerebellum to the social brain network integrating amygdalar connections. Our findings suggest that the cerebellum organizes the neural matrix necessary for SRM.

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Olfactory stimulation induces cerebellar vermis activation during sexual learning in male rats

Cited by 7 publications

References 40 publications

Molecular layer interneurons in the cerebellum encode for valence in associative learning

Molecular layer interneurons in the cerebellum encode for valence in associative learning

Molecular layer interneurons in the cerebellum encode for valence in associative learning

Social memory deficit caused by dysregulation of the cerebellar vermis

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