Action and learning shape the activity of neuronal circuits in the visual cortex

Pakan, Janelle M.P.; Francioni, Valerio; Rochefort, Nathalie L.

doi:10.1016/j.conb.2018.04.020

Cited by 75 publications

(67 citation statements)

References 83 publications

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“…Moreover, our inclusion of a homeostatic inhibitory plasticity rule that precisely controls excitatory firing rate precludes us from making predictions about the dependence of a neurons average firing rate and its propensity for stimulus preference plasticity (Vogels et al, 2011). Similar links between plasticity and population dynamics could emerge in other experiments that chronically image cortical network activity (Driscoll et al, 2017;Singh et al, 2015;Peron et al, 2015) Since the majority of experiments which track stimulus preference evolution do so during visual discrimination paradigms, it is likely that top-down influences such as attention or reward modulation play significant roles in their observed dynamics (Pakan et al, 2018;Caras and Sanes, 2017;Poort et al, 2015;Schoups et al, 2001). An exception is Goltstein et al (2013), in which stimulus preference is measured in the anaesthetised state, meaning that top-down inputs are likely to be absent.…”

Section: Stability and Plasticity Of Stimulus Responsesmentioning

confidence: 83%

Population coupling predicts the plasticity of stimulus responses in cortical circuits

Sweeney

Clopath

2020

eLife

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Some neurons have stimulus responses that are stable over days, whereas other neurons have highly plastic stimulus responses. Using a recurrent network model, we explore whether this could be due to an underlying diversity in their synaptic plasticity. We find that, in a network with diverse learning rates, neurons with fast rates are more coupled to population activity than neurons with slow rates. This plasticity-coupling link predicts that neurons with high population coupling exhibit more long-term stimulus response variability than neurons with low population coupling. We substantiate this prediction using recordings from the Allen Brain Observatory, finding that a neuron’s population coupling is correlated with the plasticity of its orientation preference. Simulations of a simple perceptual learning task suggest a particular functional architecture: a stable ‘backbone’ of stimulus representation formed by neurons with low population coupling, on top of which lies a flexible substrate of neurons with high population coupling.

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Section: Stability and Plasticity Of Stimulus Responsesmentioning

confidence: 83%

Population coupling predicts the plasticity of stimulus responses in cortical circuits

Sweeney

Clopath

2020

eLife

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“…Hypothesis: Two-stage model of top-down guided microcircuit plasticity Neural responses to visual stimuli in V1 are not a simple function of bottom-up sensory inputs. They are additionally modulated by various inputs from other areas Pakan et al, 2018) and by recurrent local excitatory and inhibitory neurons (especially in layer 2/3, Cossell et al, 2015). We hypothesised that top-down inputs can induce changes in sensory representations via changes in recurrent connections in two stages.…”

Section: Resultsmentioning

confidence: 99%

Inhibitory microcircuits for top-down plasticity of sensory representations

Wilmes

Clopath

2018

Preprint

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Humans and animals are remarkable at detecting stimuli that predict rewards. While the underlying neural mechanisms are unknown, reward influences plasticity of sensory representations in early sensory areas. The underlying changes in excitatory and inhibitory circuitry are however unclear. Recently, experimental findings suggest that the inhibitory circuits can regulate learning. In addition, the inhibitory neurons in superficial layers are highly modulated by diverse long-range inputs, including reward signals. We, therefore, hypothesise that plasticity of interneuron circuits plays a major role in adjusting stimulus representations. We investigate how top-down modulation by rewards can interact with local excitatory and inhibitory plasticity to induce long-lasting changes in sensory circuitry. Using a computational model of layer 2/3 primary visual cortex, we demonstrate how interneuron networks can store information about the rewarded stimulus to instruct long-term changes in excitatory connectivity in the absence of further reward. In our model, stimulus-tuned somatostatin-positive interneurons (SSTs) develop strong connections to parvalbumin-positive interneurons (PVs) during reward presentation such that they selectively disinhibit the pyramidal layer henceforth. This triggers plasticity in the excitatory neurons, which leads to increased stimulus representation. We make specific testable predictions in terms of the activity of different neuron types. We finally show that this two-stage model allows for translation invariance of the learned representation.

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“…In the visual cortex, pyramidal cells respond with increased firing rates during locomotion, but the network mechanisms of this effect are not fully understood 30 . Using ASAP3-Kv, we investigated whether locomotion influences synaptic inputs in different neuronal types in visual cortex.…”

Section: Modulation Of Network Activity By Locomotion In the Visual Cmentioning

confidence: 99%

Fast two-photon volumetric imaging of an improved voltage indicator reveals electrical activity in deeply located neurons in the awake brain

Chavarha

Villette

Dimov

et al. 2018

Preprint

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Imaging of transmembrane voltage deep in brain tissue with cellular resolution has the potential to reveal information processing by neuronal circuits in living animals with minimal perturbation. Multi-photon voltage imaging in vivo, however, is currently limited by speed and sensitivity of both indicators and imaging methods. Here, we report the engineering of an improved genetically encoded voltage indicator, ASAP3, which exhibits up to 51% fluorescence responses in the physiological voltage range, sub-millisecond activation kinetics, and full responsivity under two-photon illumination. We also introduce an ultrafast local volume excitation (ULOVE) two-photon scanning method to sample ASAP3 signals in awake mice at kilohertz rates with increased stability and sensitivity. ASAP3 and ULOVE allowed continuous single-trial tracking of spikes and subthreshold events for minutes in deep locations, with subcellular resolution, and with repeated sampling over multiple days. By imaging voltage in visual cortex neurons, we found evidence for cell type-dependent subthreshold modulation by locomotion. Thus, ASAP3 and ULOVE enable continuous high-speed highresolution imaging of electrical activity in deeply located genetically defined neurons during awake behavior.shaping 7,8 . However, parallel excitation is problematic for imaging, as scattered fluorescence signals from simultaneously excited cells would become intermixed, hindering detection of small responses. Furthermore, as GEVIs reside in the membrane rather than the cytosol, the number of indicator molecules that can be excited in an optical section through a mammalian cell body is typically smaller for GEVIs than for GECIs 4,6 .Given these limitations, the development of GEVIs with larger two-photon responses to electrical events of interest is highly desirable. Currently, the GEVIs with the largest responses to both subthreshold changes and APs are based on two types of voltage-sensing domains: seven-transmembrane helix opsins and four-transemembrane helix voltage-sensing domains (VSDs). Opsin-based GEVIs have been used in vivo with one-photon excitation to report electrical activity of superficially located neurons 9,10 , but their responsivity is severely attenuated under twophoton excitation 4,11 . In contrast, ASAP-family GEVIs, composed of a circularly permuted green fluorescent protein variant inserted within the VSD of G. gallus voltage-sensing phosphatase (Fig. 1a), are fully responsive under twophoton excitation 11 . In particular, ASAP2s demonstrates the largest response per AP of fluorescent protein-based GEVIs, but its kinetics are actually slower than earlier ASAP variants 11 . If ASAP-family kinetics and/or overall responsivity could be improved, then electrical events could be more easily detected by two-photon imaging.Here we report an improved indicator, ASAP3, resulting from novel methods for generation and screening of GEVI libraries in mammalian cells. ASAP3 features the largest responses of fluorescent GEVIs to either steady-state voltages or ...

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Action and learning shape the activity of neuronal circuits in the visual cortex

Cited by 75 publications

References 83 publications

Population coupling predicts the plasticity of stimulus responses in cortical circuits

Population coupling predicts the plasticity of stimulus responses in cortical circuits

Inhibitory microcircuits for top-down plasticity of sensory representations

Fast two-photon volumetric imaging of an improved voltage indicator reveals electrical activity in deeply located neurons in the awake brain

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