Learning and attention increase visual response selectivity through distinct mechanisms

Poort, Jasper; Wilmes, Katharina Anna; Blot, Antonin; Chadwick, Angus; Sahani, Maneesh; Clopath, Claudia; Mrsic-Flogel, Thomas D.; Hofer, Sonja B.; Khan, Adil G.

doi:10.1016/j.neuron.2021.11.016

Cited by 45 publications

(31 citation statements)

References 73 publications

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“…Conversely, L2/3 SOM+ cells increase their response when passively viewing a familiar stimulus (Kato et al, 2015;Makino and Komiyama, 2015). These findings can change with the presence of reward, attention, or a task (Makino and Komiyama, 2015;Fiser et al, 2016;Henschke et al, 2020;Wang et al, 2020;Poort et al, 2021). These observations in L2/3 fit well with calcium imaging in V1 L4 for principal, PV+ and SOM+ neurons (Kim et al, 2020;Hayden et al, 2021).…”

Section: Passive Viewing: Evidence Outside Of the Standard Stimulus-selective Response Plasticity Paradigmsupporting

confidence: 66%

“…However, a closer inspection of data in mouse V1 shows that, while many GABAergic neurons show no or limited orientation preference, many do have a moderate orientation preference (Kerlin et al, 2010;Ma et al, 2010;Makino and Komiyama, 2015). Learning, albeit rewarded, has also been shown to increase the stimulus selectivity of PV+ interneuron populations (Khan et al, 2018;Poort et al, 2021), and SRP experiments show that SOM+ interneurons can gain orientation selectivity simply by exposure to novel gratings of a single orientation (Hayden et al, 2021). Presumably this acquisition of selectivity reflects an increased response to a subset of excitatory inputs conveying information about the familiar stimulus.…”

Section: Stimulus-selective Response Plasticity Expression Involves Two Competing Populations Of Inhibitory Interneuronsmentioning

confidence: 99%

“…Various forms of experience-dependent plasticity have been demonstrated in L2/3 of mouse sensory cortex (Kato et al, 2015;Makino and Komiyama, 2015;Fiser et al, 2016;Garrett et al, 2020;Henschke et al, 2020;Wang et al, 2020;Gao et al, 2021;Poort et al, 2021). Of particular relevance to SRP are those studies that recorded, either by design or as a control, the changes that are caused by passive experience.…”

Section: Passive Viewing: Evidence Outside Of the Standard Stimulus-selective Response Plasticity Paradigmmentioning

confidence: 99%

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Stimulus-Selective Response Plasticity in Primary Visual Cortex: Progress and Puzzles

Montgomery

Hayden

Chaloner

et al. 2022

Front. Neural Circuits

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Stimulus-selective response plasticity (SRP) is a robust and lasting modification of primary visual cortex (V1) that occurs in response to exposure to novel visual stimuli. It is readily observed as a pronounced increase in the magnitude of visual evoked potentials (VEPs) recorded in response to phase-reversing grating stimuli in neocortical layer 4. The expression of SRP at the individual neuron level is equally robust, but the qualities vary depending on the neuronal type and how activity is measured. This form of plasticity is highly selective for stimulus features such as stimulus orientation, spatial frequency, and contrast. Several key insights into the significance and underlying mechanisms of SRP have recently been made. First, it occurs concomitantly and shares core mechanisms with behavioral habituation, indicating that SRP reflects the formation of long-term familiarity that can support recognition of innocuous stimuli. Second, SRP does not manifest within a recording session but only emerges after an off-line period of several hours that includes sleep. Third, SRP requires not only canonical molecular mechanisms of Hebbian synaptic plasticity within V1, but also the opposing engagement of two key subclasses of cortical inhibitory neuron: the parvalbumin- and somatostatin-expressing GABAergic interneurons. Fourth, pronounced shifts in the power of cortical oscillations from high frequency (gamma) to low frequency (alpha/beta) oscillations provide respective readouts of the engagement of these inhibitory neuronal subtypes following familiarization. In this article we will discuss the implications of these findings and the outstanding questions that remain to gain a deeper understanding of this striking form of experience-dependent plasticity.

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Section: Passive Viewing: Evidence Outside Of the Standard Stimulus-selective Response Plasticity Paradigmsupporting

confidence: 66%

Section: Stimulus-selective Response Plasticity Expression Involves Two Competing Populations Of Inhibitory Interneuronsmentioning

confidence: 99%

Section: Passive Viewing: Evidence Outside Of the Standard Stimulus-selective Response Plasticity Paradigmmentioning

confidence: 99%

See 1 more Smart Citation

Stimulus-Selective Response Plasticity in Primary Visual Cortex: Progress and Puzzles

Montgomery

Hayden

Chaloner

et al. 2022

Front. Neural Circuits

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show abstract

“…The BCI task used in this study was multimodal in nature. To determine whether our results generalize to a single-modality task, we trained mice in a visual discrimination task in which it was previously established that V1 activity is required for improved behavioral performance 16 , 50 , 51 . Converging evidence indicates visual discrimination training enhances the neural representation of rewarded stimuli by increasing selectivity for the stimuli experienced during training 16 , 21 and in some cases improving response reliability 16 , and at the same time suppresses responses to non-relevant stimuli 16 .…”

Section: Resultsmentioning

confidence: 99%

Existing function in primary visual cortex is not perturbed by new skill acquisition of a non-matched sensory task

et al. 2022

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Acquisition of new skills has the potential to disturb existing network function. To directly assess whether previously acquired cortical function is altered during learning, mice were trained in an abstract task in which selected activity patterns were rewarded using an optical brain-computer interface device coupled to primary visual cortex (V1) neurons. Excitatory neurons were longitudinally recorded using 2-photon calcium imaging. Despite significant changes in local neural activity during task performance, tuning properties and stimulus encoding assessed outside of the trained context were not perturbed. Similarly, stimulus tuning was stable in neurons that remained responsive following a different, visual discrimination training task. However, visual discrimination training increased the rate of representational drift. Our results indicate that while some forms of perceptual learning may modify the contribution of individual neurons to stimulus encoding, new skill learning is not inherently disruptive to the quality of stimulus representation in adult V1.

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“…Hence, one possibility is that L2/3 PNs in M1 encode reward signals during the naive stage, but after associative learning, they habituate and become unresponsive to the reward stimulus. In addition, in the sensory cortices, the flexibility to either respond to or ignore sensory stimuli is based on the stimulus’ behavioral relevance and is gated by local SOM-INs ( Kato et al, 2015 ; Makino and Komiyama, 2015 ; Poort et al, 2021 ). In line with these findings, we found that SOM-INs became more reliably responsive to both the CS and the reward with associative learning.…”

Section: Discussionmentioning

confidence: 99%

Cell-type-specific responses to associative learning in the primary motor cortex

Lee

Harkin

Yin

et al. 2022

eLife

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The primary motor cortex (M1) is known to be a critical site for movement initiation and motor learning. Surprisingly, it has also been shown to possess reward-related activity, presumably to facilitate reward-based learning of new movements. However, whether reward-related signals are represented among different cell types in M1, and whether their response properties change after cue-reward conditioning remains unclear. Here, we performed longitudinal in vivo two-photon Ca2+ imaging to monitor the activity of different neuronal cell types in M1 while mice engaged in a classical conditioning task. Our results demonstrate that most of the major neuronal cell types in M1 showed robust but differential responses to both the conditioned cue stimulus (CS) and reward, and their response properties undergo cell-type specific modifications after associative learning. PV-INs' responses became more reliable to the CS, while VIP-INs' responses became more reliable to reward. PNs only showed robust responses to novel reward, and they habituated to it after associative learning. Lastly, SOM-INs' responses emerged and became more reliable to both the CS and reward after conditioning. These observations suggest that cue- and reward-related signals are preferentially represented among different neuronal cell types in M1, and the distinct modifications they undergo during associative learning could be essential in triggering different aspects of local circuit reorganization in M1 during reward-based motor skill learning.

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Learning and attention increase visual response selectivity through distinct mechanisms

Cited by 45 publications

References 73 publications

Stimulus-Selective Response Plasticity in Primary Visual Cortex: Progress and Puzzles

Stimulus-Selective Response Plasticity in Primary Visual Cortex: Progress and Puzzles

Existing function in primary visual cortex is not perturbed by new skill acquisition of a non-matched sensory task

Cell-type-specific responses to associative learning in the primary motor cortex

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