Utilizing Miniature Fluorescence Microscopy to Image Hippocampal Place Cell Ensemble Function in Thy1.GCaMP6f Transgenic Mice

Indersmitten, Tim; Berdyyeva, Tamara; Aluisio, Leah; Lovenberg, Timothy W.; Bonaventure, Pascal; Wyatt, Ryan M.

doi:10.1002/cpph.42

Cited by 4 publications

(4 citation statements)

References 30 publications

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“…Targeted SUA has been used for cell-type specific electrophysiological recording in the medial prefrontal cortex ( 56 ), and the striatum ( 57 ), but applied here for the first time in the SCN. In vivo calcium imaging has been used to measure calcium dynamics in many brain areas including the frontal cortex ( 58 ), hippocampus ( 59 ), and cerebellum ( 60 , 61 ). This technique permits the characterization of individual cells within the SCN and how they contribute to communal network behavior, and how these contributions are modulated over circadian and diurnal time.…”

Section: Discussionmentioning

confidence: 99%

Arginine–vasopressin-expressing neurons in the murine suprachiasmatic nucleus exhibit a circadian rhythm in network coherence in vivo

Stowie

Qiao

Buonfiglio

et al. 2023

Proc. Natl. Acad. Sci. U.S.A.

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The suprachiasmatic nucleus (SCN) is composed of functionally distinct subpopulations of GABAergic neurons which form a neural network responsible for synchronizing most physiological and behavioral circadian rhythms in mammals. To date, little is known regarding which aspects of SCN rhythmicity are generated by individual SCN neurons, and which aspects result from neuronal interaction within a network. Here, we utilize in vivo miniaturized microscopy to measure fluorescent GCaMP-reported calcium dynamics in arginine vasopressin (AVP)-expressing neurons in the intact SCN of awake, behaving mice. We report that SCN AVP neurons exhibit periodic, slow calcium waves which we demonstrate, using in vivo electrical recordings, likely reflect burst firing. Further, we observe substantial heterogeneity of function in that AVP neurons exhibit unstable rhythms, and relatively weak rhythmicity at the population level. Network analysis reveals that correlated cellular behavior, or coherence, among neuron pairs also exhibited stochastic rhythms with about 33% of pairs rhythmic at any time. Unlike single-cell variables, coherence exhibited a strong rhythm at the population level with time of maximal coherence among AVP neuronal pairs at CT/ZT 6 and 9, coinciding with the timing of maximal neuronal activity for the SCN as a whole. These results demonstrate robust circadian variation in the coordination between stochastically rhythmic neurons and that interactions between AVP neurons in the SCN may be more influential than single-cell activity in the regulation of circadian rhythms. Furthermore, they demonstrate that cells in this circuit, like those in many other circuits, exhibit profound heterogenicity of function over time and space.

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Section: Discussionmentioning

confidence: 99%

Arginine–vasopressin-expressing neurons in the murine suprachiasmatic nucleus exhibit a circadian rhythm in network coherence in vivo

Stowie

Qiao

Buonfiglio

et al. 2023

Proc. Natl. Acad. Sci. U.S.A.

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“…Recording sessions during which mice traversed the entirety of the linear track less than 36 times were excluded. For a more detailed protocol about surgeries and linear track training, see Indersmitten et al (2018).…”

Section: Methodsmentioning

confidence: 99%

In vivo Calcium Imaging Reveals That Cortisol Treatment Reduces the Number of Place Cells in Thy1-GCaMP6f Transgenic Mice

et al. 2019

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The hippocampus, a structure essential for spatial navigation and memory undergoes anatomical and functional changes during chronic stress. Here, we investigate the effects of chronic stress on the ability of place cells to encode the neural representation of a linear track. To model physiological conditions of chronic stress on hippocampal function, transgenic mice expressing the genetically encoded calcium indicator GCaMP6f in CA1 pyramidal neurons were chronically administered with 40 μg/ml of cortisol for 8 weeks. Cortisol-treated mice exhibited symptoms typically observed during chronic stress, including diminished reward seeking behavior and reduced adrenal gland and spleen weights. In vivo imaging of hippocampal cellular activity during linear track running behavior revealed a reduced number of cells that could be recruited to encode spatial position, despite an unchanged overall number of active cells, in cortisol-treated mice. The properties of the remaining place cells that could be recruited to encode spatial information, however, was unperturbed. Bayesian decoders trained to estimate the mouse’s position on the track using single neuron activity data demonstrated reduced performance in a cue richness-dependent fashion in cortisol-treated animals. The performance of decoders utilizing data from the entire neuronal ensemble was unaffected by cortisol treatment. Finally, to test the hypothesis that an antidepressant drug could prevent the effects of cortisol, we orally administered a group of mice with 10 mg/kg citalopram during cortisol administration. Citalopram prevented the cortisol-induced decrease in single-neuron decoder performance but failed to significantly prevent anhedonia and the cortisol-induced reduction in the proportion place cells. The dysfunction observed at the single-neuron level indicates that chronic stress may impair the ability of the hippocampus to encode individual neural representations of the mouse’s spatial position, a function pivotal to forming an accurate navigational map of the mouse’s external environment; however, the hippocampal ensemble as a whole is resilient to any cortisol-induced insults to single neuronal place cell function on the linear track.

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“…Using miniature microscopes for intravital microscopy is also a specialized topic, and it is not covered in this review paper. Readers wishing to investigate this topic are advised to refer to the Current Protocols paper by Indersmitten et al (2018) as well as Aharoni and Hoogland (2019), de Groot et al (2020), andGuinto et al (2022).…”

Section: Intravital Microscopymentioning

confidence: 99%

“…Readers wishing to investigate this topic are advised to refer to the Current Protocols paper by Indersmitten et al. (2018) as well as Aharoni and Hoogland (2019), de Groot et al. (2020), and Guinto et al.…”

Section: Commentarymentioning

confidence: 99%

Multi‐Photon Microscopy

Sanderson

2023

Current Protocols

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In this series of papers on light microscopy imaging, we have covered the fundamentals of microscopy, super-resolution microscopy, and lightsheet microscopy. This last review covers multi-photon microscopy with a brief reference to intravital imaging and Brainbow labeling. Multi-photon microscopy is often referred to as two-photon microscopy. Indeed, using two-photon microscopy is by far the most common way of imaging thick tissues; however, it is theoretically possible to use a higher number of photons, and three-photon microscopy is possible. Therefore, this review is titled "multi-photon microscopy." Another term for describing multi-photon microscopy is "non-linear" microscopy because fluorescence intensity at the focal spot depends upon the average squared intensity rather than the squared average intensity; hence, non-linear optics (NLO) is an alternative name for multi-photon microscopy. It is this non-linear relationship (or third exponential power in the case of three-photon excitation) that determines the axial optical sectioning capability of multi-photon imaging. In this paper, the necessity for two-photon or multi-photon imaging is explained, and the method of optical sectioning by multi-photon microscopy is described. Advice is also given on what fluorescent markers to use and other practical aspects of imaging thick tissues. The technique of Brainbow imaging is discussed. The review concludes with a description of intravital imaging of the mouse.

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Utilizing Miniature Fluorescence Microscopy to Image Hippocampal Place Cell Ensemble Function in Thy1.GCaMP6f Transgenic Mice

Cited by 4 publications

References 30 publications

Arginine–vasopressin-expressing neurons in the murine suprachiasmatic nucleus exhibit a circadian rhythm in network coherence in vivo

Arginine–vasopressin-expressing neurons in the murine suprachiasmatic nucleus exhibit a circadian rhythm in network coherence in vivo

In vivo Calcium Imaging Reveals That Cortisol Treatment Reduces the Number of Place Cells in Thy1-GCaMP6f Transgenic Mice

Multi‐Photon Microscopy

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