VIP interneurons in mouse primary visual cortex selectively enhance responses to weak but specific stimuli

Millman, Daniel; Ocker, Gabriel Koch; Caldejon, Shiella; Kato, India; Larkin, Josh; Lee, Eric; Luviano, Jennifer; Nayan, Chelsea; Nguyen, Thuyanh V.; North, Kat; Seid, Sam; White, Casey; Lecoq, Jérôme; Reid, Clay; Buice, Michael A.; Vries, Saskia E. J. de

doi:10.7554/elife.55130

Cited by 58 publications

(99 citation statements)

References 42 publications

(59 reference statements)

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“…These neurons are also highly integrated with motor circuits, where they can reciprocally regulate activity levels 52,68 . Our study and previous ones show that upregulating VIP interneuron excitability can locally enhance sensory evoked layer 2/3 population responses in somatosensory, visual and auditory cortex [26][27][28] , as well as the tuning of specific sensory features . Conversely, interfering with VIP neuron activity impairs visual response selectivity, learning and ocular dominance plasticity 29,30 .…”

Section: A Subset Of Vip Neurons Are Highly Sensitive To the Effects supporting

confidence: 80%

“…In the present study, we reasoned that chemogenetic manipulation of cortical excitability through VIP interneurons, could provide a focal boost in periinfarct excitability in relatively non-invasive manner. VIP neurons play a powerful role in enhancing sensory responses in pyramidal neurons in visual and auditory cortex through disinhibition [26][27][28]52,53 . Consistent with previous findings, we found that increasing VIP interneuron excitability with chemogenetic stimulation could enhance forepaw evoked responses in somatosensory cortex for at least hour after CNO injection.…”

Section: Chemogenetic Stimulation Of Dis-inhibitory Vip Interneurons mentioning

confidence: 99%

“…However, the activity of PV and SOM interneurons can be regulated by inhibitory synaptic connections from VIP neurons [22][23][24] . Given that cortical VIP interneurons receive excitatory inputs from sensory nuclei in the thalamus and local cortical neurons 25 , the net effect of activating these dis-inhibitory VIP circuits is to enhance cortical responses to a sensory stimulus [26][27][28] . Not surprisingly, VIP neurons have been implicated in regulating developmental, learning and experience dependent plasticity of visual cortical circuits 29,30 .…”

Section: Introductionmentioning

confidence: 99%

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Longitudinal imaging of VIP interneurons reveals sup-population specific effects of stroke that can be rescued with chemogenetic therapy

Motaharinia

Gerrow

Boghozian

et al. 2021

Preprint

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Stroke profoundly disrupts cortical excitability which impedes recovery, but how it affects the function of specific inhibitory interneurons, or subpopulations therein, is poorly understood. Interneurons expressing vasoactive intestinal peptide (VIP) represent an intriguing stroke target because they can regulate cortical excitability through disinhibition. Here we chemogenetically augmented VIP interneuron excitability after stroke to show that it enhances somatosensory responses and improves recovery of paw function. Using longitudinal calcium imaging, we discovered that stroke primarily disrupts the fidelity (fraction of responsive trials) and predictability of sensory responses within a subset of highly active VIP neurons. Partial recovery of responses occurred largely within these active neurons and was not accompanied by the recruitment of minimally active neurons. Importantly, chemogenetic stimulation preserved sensory response fidelity and predictability in highly active neurons. These findings provide a new depth of understanding into how stroke and prospective therapies (chemogenetics), can influence subpopulations of inhibitory interneurons.

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Section: A Subset Of Vip Neurons Are Highly Sensitive To the Effects supporting

confidence: 80%

Section: Chemogenetic Stimulation Of Dis-inhibitory Vip Interneurons mentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Longitudinal imaging of VIP interneurons reveals sup-population specific effects of stroke that can be rescued with chemogenetic therapy

Motaharinia

Gerrow

Boghozian

et al. 2021

Preprint

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“…The algorithm parameters were tuned to reject potential ROIs with a peak spatial SNR below 2.5, a temporal SNR below 5, or a spatial corruption index above 1.5. Fluorescence traces for both somatic and dendritic ROIs were then extracted, neuropil-subtracted, demixed, and converted to Δ F/F traces, as described in [de Vries et al, 2020; Millman et al, 2020]. Together, neuropil subtraction and the use of a 180-second (5401 sample) sliding window to calculate rolling baseline fluorescence levels F for the Δ F/F computation ensured that the Δ F/F traces obtained were robust to potential differences in background fluorescence between mice and imaging planes.…”

Section: Methodsmentioning

confidence: 99%

Learning from unexpected events in the neocortical microcircuit

Gillon

Pina

Lecoq

et al. 2021

Preprint

Self Cite

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Scientists have long conjectured that the neocortex learns the structure of the environment in a predictive, hierarchical manner. To do so, expected, predictable features are differentiated from unexpected ones by comparing bottom-up and top-down streams of data. It is theorized that the neocortex then changes the representation of incoming stimuli, guided by differences in the responses to expected and unexpected events. Such differences in cortical responses have been observed; however, it remains unknown whether these unexpected event signals govern subsequent changes in the brain’s stimulus representations, and, thus, govern learning. Here, we show that unexpected event signals predict subsequent changes in responses to expected and unexpected stimuli in individual neurons and distal apical dendrites that are tracked over a period of days. These findings were obtained by observing layer 2/3 and layer 5 pyramidal neurons in primary visual cortex of awake, behaving mice using two-photon calcium imaging. We found that many neurons in both layers 2/3 and 5 showed large differences between their responses to expected and unexpected events. These unexpected event signals also determined how the responses evolved over subsequent days, in a manner that was different between the somata and distal apical dendrites. This difference between the somata and distal apical dendrites may be important for hierarchical computation, given that these two compartments tend to receive bottom-up and top-down information, respectively. Together, our results provide novel evidence that the neocortex indeed instantiates a predictive hierarchical model in which unexpected events drive learning.

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“…It has been suggested that this visuomotor mismatch is driven by the comparison of excitatory, motor inputs with inhibitory, visual flow inputs 12,13 . However, neurons in V1 have a wide range of visual speed (or temporal frequency) preferences [14][15][16] , and running both drives V1 activity and modulates responses to visual stimuli 10,[17][18][19][20][21][22] . An alternate and untested hypothesis is that responses to sudden stops of visual flow are simply due to the convergence of motor and visual inputs, and do not arise from the precise coupling between an animals' actions and the visual stimulus.…”

Section: Introductionmentioning

confidence: 99%

Feature selectivity explains mismatch signals in mouse visual cortex

Muzzu

Saleem

2021

Preprint

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Sensory experience is often dependent on one's own actions, including self-motion. Theories of predictive coding postulate that actions are regulated by calculating prediction error, which is the difference between sensory experience and expectation based on self-generated actions. Signals consistent with prediction error have been reported in mouse visual cortex (V1) when visual flow coupled to running is unexpectedly perturbed. Here, we show that such signals can be elicited by visual stimuli uncoupled with the animal's running. We recorded the activity of mouse V1 neurons while presenting drifting gratings that unexpectedly stopped. We found strong responses to visual perturbations, which were enhanced during running. If these perturbation responses are signals about sensorimotor mismatch, they should be largest for front-to-back visual flow expected from the animals' running. Responses, however, did not show a bias for front-to-back visual flow. Instead, perturbation responses were strongest in the preferred orientation of individual neurons and perturbation responsive neurons were more likely to prefer slow visual speeds. Our results therefore indicate that prediction error signals can be explained by the convergence of known motor and sensory signals in visual cortex, providing a purely sensory and motor explanation for purported mismatch signals.

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VIP interneurons in mouse primary visual cortex selectively enhance responses to weak but specific stimuli

Cited by 58 publications

References 42 publications

Longitudinal imaging of VIP interneurons reveals sup-population specific effects of stroke that can be rescued with chemogenetic therapy

Longitudinal imaging of VIP interneurons reveals sup-population specific effects of stroke that can be rescued with chemogenetic therapy

Learning from unexpected events in the neocortical microcircuit

Feature selectivity explains mismatch signals in mouse visual cortex

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