The spatiotemporal organization of experience dictates hippocampal involvement in primary visual cortical plasticity

Finnie, Peter S.B.; Komorowski, Robert W.; Bear, Mark F.

doi:10.1016/j.cub.2021.06.079

Cited by 33 publications

(33 citation statements)

References 83 publications

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“…In fact, we previously speculated that cue-triggered reactivation of simple sequences might be driven by an automatic pattern completion-like mechanism that reactivates all associated items based on partial input (Ekman et al, 2017). This idea is in line with the finding that predictive representations in V1 correlated with pattern completion-like activity in the hippocampus (Hindy et al, 2016;Kok & Turk-Browne, 2018) that might be driving V1 activity (Finnie et al, 2021;Ji & Wilson, 2007).…”

Section: Discussionsupporting

confidence: 67%

“…On a conceptual level, navigation (in memory and space) and processing visual events both involve abstraction of the relational structure between events to enable forward planning and predictions. Similar to navigational space, visual space can be represented in terms of its relational structure like direction and distance, and it has been suggested that similar mechanisms might underlie spatial and non-spatial representations (Nau, Julian, et al, 2018), especially if there is sequential structure present (Finnie et al, 2021). Supporting this notion, recently, a conceptual link between representations for visual understanding and spatial navigation has been proposed that suggests a common underlying map-like representation of visual and navigational task structure (Schwartenbeck et al, 2021).…”

Section: Discussionmentioning

confidence: 99%

“…Anticipation and planning of future visual input require knowledge of the relational structure between events. The relational structure, for instance that stimulus B usually follows stimulus A, is learned through exposure during past experiences (Behrens et al, 2018;Finnie et al, 2021;Gavornik & Bear, 2014) and can be used to build a model or cognitive map (Tolman, 1948) that enables us to generate inferences in situation with noisy or partial input (Ekman et al, 2017;Momennejad, 2020;Schwartenbeck et al, 2021).…”

Section: Introductionmentioning

confidence: 99%

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Successor-like representation guides the prediction of future events in human visual cortex and hippocampus

Ekman

Kusch

Lange

2022

Preprint

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Human agents build models of their environment, which enable them to anticipate and plan upcoming events. However, little is known about the properties of such predictive models. Recently, it has been proposed that hippocampal representations take the form of a predictive map-like structure, the so-called successor representation. Here we used human fMRI to probe whether activity in the early visual cortex (V1) and hippocampus adhere to the postulated properties of the successor representation after visual sequence learning. Participants were exposed to an arbitrary spatiotemporal sequence consisting of four items (A-B-C-D). We found that after repeated exposure to the sequence, merely presenting single sequence items (e.g., - B - -) resulted in V1 activation at the successor locations of the full sequence (e.g., C-D), but not at the predecessor locations (e.g., A). This highlights that visual representations are skewed toward future states, in line with the successor representation. Similar results were also found in the hippocampus. Moreover, the hippocampus developed a tuning profile that showed sensitivity to the temporal distance in sequence-space, with fading representations for sequence events in the more distant past and future. V1, in contrast, showed a tuning profile that was only sensitive to spatial distance in stimulus-space. Together, these results provide empirical evidence for the proposition that both visual and hippocampal cortex represent a predictive map of the visual world akin to the successor representation.

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Section: Discussionsupporting

confidence: 67%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Successor-like representation guides the prediction of future events in human visual cortex and hippocampus

Ekman

Kusch

Lange

2022

Preprint

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“…When first presented with an oriented grating stimulus, mice produce an easily measured visually evoked fidgeting behavior (Figure 2A) that subsides with increasing familiarity via a process we have termed orientation-selective habituation (OSH). With a similar degree of selectivity to SRP, OSH is reversed and movement re-emerges upon presentation of a novel stimulus (Figure 2B) Kaplan et al, 2016;Fong et al, 2020;Finnie et al, 2021). VEP recordings from these headfixed mice reveal that these behavioral changes occur along a comparable timecourse to SRP (Figure 2C).…”

Section: Orientation-selective Habituationmentioning

confidence: 82%

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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“…In fact, the structure of the adaptive subunit model suggests that this memory could be primarily encoded by synaptic and cellular variables of neurons within V1. At the same time, recent results have shown that responses in V1 can be influenced by activity in the hippocampus ( 77 , 78 ), so it would be premature to rule out any such involvement.…”

Section: Discussionmentioning

confidence: 99%

Novel stimuli evoke excess activity in the mouse primary visual cortex

Homann

Koay

Chen

et al. 2022

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

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To explore how neural circuits represent novel versus familiar inputs, we presented mice with repeated sets of images with novel images sparsely substituted. Using two-photon calcium imaging to record from layer 2/3 neurons in the mouse primary visual cortex, we found that novel images evoked excess activity in the majority of neurons. This novelty response rapidly emerged, arising with a time constant of 2.6 ± 0.9 s. When a new image set was repeatedly presented, a majority of neurons had similarly elevated activity for the first few presentations, which decayed to steady state with a time constant of 1.4 ± 0.4 s. When we increased the number of images in the set, the novelty response’s amplitude decreased, defining a capacity to store ∼15 familiar images under our conditions. These results could be explained quantitatively using an adaptive subunit model in which presynaptic neurons have individual tuning and gain control. This result shows that local neural circuits can create different representations for novel versus familiar inputs using generic, widely available mechanisms.

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The spatiotemporal organization of experience dictates hippocampal involvement in primary visual cortical plasticity

Cited by 33 publications

References 83 publications

Successor-like representation guides the prediction of future events in human visual cortex and hippocampus

Successor-like representation guides the prediction of future events in human visual cortex and hippocampus

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

Novel stimuli evoke excess activity in the mouse primary visual cortex

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