Cortex-wide response mode of VIP-expressing inhibitory neurons by reward and punishment
- Laboratory of 3D functional network and dendritic imaging, Institute of Experimental Medicine, Hungary
- MTA-PPKE ITK-NAP B – 2p Measurement Technology Group, The Faculty of Information Technology, Pázmány Péter Catholic University, Hungary
- János Szentágothai Doctoral School of Neurosciences, Semmelweis University, Hungary
- BrainVisionCenter, Hungary
- Cold Spring Harbor Laboratory, United States
- Volen Center for Complex Systems, Biology Department, Brandeis University, United States
- Departments of Neuroscience and Psychiatry, Washington University School of Medicine, United States
- Computational Systems Neuroscience Lab, Wigner Research Centre for Physics, Hungary
- Department of Mathematical Geometry, Institute of Mathematics, Budapest University of Technology and Economics, Hungary
Figures
Figure 1 with 3 supplements
Three-dimensional (3D) random access two-photon imaging of vasoactive intestinal polypeptide (VIP) neurons in an auditory discrimination task.
(A) Schematic of the combined fast 3D acousto-optical (AO) imaging and behavior experiments. Head-restrained mice were trained to perform a sensory discrimination, an auditory go-no-go task during …
Figure 1—figure supplement 1
Three-dimensional random access two-photon imaging and fiber photometry of vasoactive intestinal polypeptide (VIP) neurons in an auditory discrimination task.
(A) The somatic Ca2+ responses in Figure 1C shown in transient form. (B) The same somatic Ca2+ responses as in Figure 1C but ordered according to their cortical depth (left) and cell diameter …
Figure 1—video 1
Recording sparse interneuronal population in large volume.
Z-stack from half mm3 neocortical volume was obtained in the parietal cortex. Then small squares containing the vasoactive intestinal polypeptide interneurons’ somata were selected as regions of …
Figure 1—video 2
Vasoactive intestinal polypeptide (VIP) population activity during an auditory discrimination task.
Example, false alarm trial of an imaging session with pupillometry, velocity recording, and motion-corrected calcium imaging of 52 VIP interneurons. Flashing white speaker and red air cloud icons …
Figure 2 with 3 supplements
Reward and punishment recruit vasoactive intestinal polypeptide (VIP) neuronal activity across the dorsal cortex (A) Ca2+ responses of individual VIP interneurons recorded separately from 18 different cortical regions from 16 mice using fast three-dimensional acousto-optical imaging were averaged for Hit (thick green), false alarm (FA; thick red), Miss (dark blue), and correct rejection (CR; light blue).
Fiber photometry data were recorded simultaneously from medial prefrontal cortex (mPFC) and auditory cortex (ACx) regions and are shown in gray boxes. Functional map (Pankhurst et al., 2012) used …
Figure 2—figure supplement 1
Quantification of the activity of vasoactive intestinal polypeptide (VIP) neurons across the dorsal cortex.
(A) Raster plot of the trial-to-trial activation of the responsive VIP neurons in Hit and false alarm (FA) trials during the two-photon imaging sessions (n=18 sessions, n=16 mice, n=746 cells). (B) …
Figure 2—figure supplement 2
Heterogeneity in vasoactive intestinal polypeptide (VIP) neuronal responses across the dorsal cortex.
(A) Left, explained variance. We used five principal components (PCs), explaining >90% of the variance of our data for the k-means clustering. Right, neurons from individual recording sessions are …
Figure 2—figure supplement 3
Cell diameter distribution of the recorded vasoactive intestinal polypeptide (VIP) interneuron population and its relation to the activity.
(A) Left, maximal intensity projection of the GCaMP6f-labeled VIP interneuron population imaged by fast three-dimensional acousto-optical scanning in one of the sessions. Thin yellow lines symbolize …
Figure 3 with 2 supplements
Arousal states modulate vasoactive intestinal polypeptide (VIP) neural responses to sensory cues and reinforcers.
(A) Upper left, schematic of measurements. Pupil and movement were simultaneously monitored during three-dimensional (3D) imaging in the auditory go-no-go task. Upper right, high (orange) and low …
Figure 3—figure supplement 1
The baseline and the change in pupil diameter, and the change of speed additionally modulate vasoactive intestinal polypeptide neuronal activity on top of activation by cues and outcomes.
(A) Population averages for Miss and correct rejection (CR; left and middle) during high and low arousal change in the somatosensory (SS) and motor (Mtr) regions (left), and auditory cortex (ACx) …
Figure 3—figure supplement 2
Arousal and reinforcement can make distinct contributions to vasoactive intestinal polypeptide (VIP) interneuronal activity.
(A) Pupil diameter, locomotion speed, and activity of multiple VIP interneurons in an example trial where reinforcement did not trigger any increase in arousal. (B) Top, relative change in pupil …
Figure 4 with 1 supplement
Visual cortex vasoactive intestinal polypeptide (VIP) neurons respond to both visual stimuli and reinforcers (A) Schematic of the measurement.
Orientation tuning was mapped in a first set of experiments (Exp. 1) which was followed by recordings of the same neurons during the auditory go-no-go task (Exp. 2). Both set of recordings were …
Figure 4—figure supplement 1
Quantification of the connection of visual tuning parameters and reinforcement-related responses.
(A) Scatter plot of reinforcement- vs visual stimulation-induced responses of the same vasoactive intestinal polypeptide (VIP) cells. (B) Scatter plot of reinforcement-induced responses vs …
Author response image 1
Comparison of peak amplitudes of pupil trace averages split according to their baseline amplitudes in Hit & FA.
Author response image 2
Comparison of peak amplitudes of pupil trace averages split according to their baseline amplitudes in Miss & CR.
Author response image 3
Comparison of peak amplitudes of pupil trace averages split according to the pupil change in Miss & CR and Hit & FA (see Figure 3—figure supplement 1A).
Author response image 4
Left, correlation of locomotion and VIP activity (median=0.11). Right, three example mice with low (red) and high (purple and green) running speeds. Right top, average running speed during Hit & FA. Right bottom, corresponding average VIP activity.
Tables
Key resources table
| Reagent type (species) or resource | Designation | Source or reference | Identifiers | Additional information |
|---|---|---|---|---|
| Recombinant DNA reagent | AAV9.Syn.Flex. GCaMP6f.WPRE.SV40 | Penn Vector Core | Cat# AV-1-PV2819 | |
| Biological sample (Mus musculus) | Viptm.1(cre)Zjh/J, B6.129P2-Pvalbtm1(cre)Arbr/J, FVB/N-Tg(Thy1-cre)1Vln/J, | The Jackson Laboratory | RRID: IMSR_JAX:010908 RRID: IMSR_JAX:017320 RRID: IMSR_JAX:006143 | |
| Software, algorithm | MATLAB | MathWorks | ||
| Software, algorithm | MES | Femtonics |
Additional files
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Supplementary file 1
Comparison of different scanning methods.
Scanning speed was calculated according to the equations in the column ‘calculation of scanning speed’. Ratio of collected photons was calculated from relative pixel dwell times. All parameters used for calculations are listed in the bottom field. Note, that chessboard scanning provides 170-fold faster measurement speed and 244-fold higher photon collection compared to volume scanning with resonant mirrors.
- https://cdn.elifesciences.org/articles/78815/elife-78815-supp1-v1.docx
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Supplementary file 2
Calculation of ratio of responsive neurons following reward.
- https://cdn.elifesciences.org/articles/78815/elife-78815-supp2-v1.docx
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MDAR checklist
- https://cdn.elifesciences.org/articles/78815/elife-78815-mdarchecklist1-v1.pdf
