Distinct recurrent versus afferent dynamics in cortical visual processing

Reinhold, Kimberly; Lien, Anthony D; Scanziani, Massimo

doi:10.1038/nn.4153

Cited by 185 publications

(239 citation statements)

References 63 publications

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“…Finally, we show (5) that synapse size correlates with physiology, with larger synapses found between neurons with similar peak orientations. Such specific connectivity is consistent with intracortical amplification of afferent signals, overcoming the strong inhibitory tone in the awake cortex 3,4,15 . As methods for automated reconstruction improve, each of these findings will come into greater focus leading to a richer understanding of network structure and function.…”

supporting

confidence: 73%

“…A model is emerging in which V1 responses arise from the selective amplification of thalamocortical signals 1,3,4 through recurrent inputs from other pyramidal neurons 2,5,14,15 . Evidence for functionally specific cortical amplification has been seen in physiological 2,3,14 and optogenetic 4 studies; however, firm anatomical evidence at the synaptic level has been lacking (but see ref.…”

mentioning

confidence: 99%

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Anatomy and function of an excitatory network in the visual cortex

Lee

Bonin

Reed

et al. 2016

Nature

487

499

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Circuits in the cerebral cortex consist of thousands of neurons connected by millions of synapses. A precise understanding of these local networks requires relating circuit activity with the underlying network structure. For pyramidal cells in superficial mouse visual cortex (V1), a consensus is emerging that neurons with similar visual response properties excite each other1–5, but the anatomical basis of this recurrent synaptic network is unknown. We combined physiological imaging and large-scale electron microscopy (EM) to study an excitatory network in V1. We found that layer 2/3 neurons organized into subnetworks defined by anatomical connectivity, with more connections within than between groups. More specifically, we found that pyramidal neurons with similar orientation selectivity preferentially formed synapses with each other, despite the fact that axons and dendrites of all orientation selectivities pass near (< 5 μm) each other with roughly equal probability. Therefore, we predict that mechanisms of functionally specific connectivity take place at the length scale of spines. Neurons with similar orientation tuning formed larger synapses, potentially enhancing the net effect of synaptic specificity. With the ability to study thousands of connections in a single circuit, functional connectomics is proving a powerful method to uncover the organizational logic of cortical networks.

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supporting

confidence: 73%

mentioning

confidence: 99%

Anatomy and function of an excitatory network in the visual cortex

Lee

Bonin

Reed

et al. 2016

Nature

487

499

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“…For this value, the input current attains a peak that is approximately three times the steady state value. Such a ratio is consistent with what has been observed in thalamic input to layer 4 cells in mouse primary visual cortex (Reinhold et al, 2015). …”

Section: Resultssupporting

confidence: 91%

Short-term depression and transient memory in sensory cortex

2017

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Persistent neuronal activity is usually studied in the context of short-term memory localized in central cortical areas. Recent studies show that early sensory areas also can have persistent representations of stimuli which emerge quickly (over tens of milliseconds) and decay slowly (over seconds). Traditional positive feedback models cannot explain sensory persistence for at least two reasons: (i) They show attractor dynamics, with transient perturbations resulting in a quasi-permanent change of system state, whereas sensory systems return to the original state after a transient. (ii) As we show, those positive feedback models which decay to baseline lose their persistence when their recurrent connections are subject to short-term depression, a common property of excitatory connections in early sensory areas. Dual time constant network behavior has also been implemented by nonlinear afferents producing a large transient input followed by much smaller steady state input. We show that such networks require unphysiologically large onset transients to produce the rise and decay observed in sensory areas. Our study explores how memory and persistence can be implemented in another model class, derivative feedback networks. We show that these networks can operate with two vastly different time courses, changing their state quickly when new information is coming in but retaining it for a long time, and that these capabilities are robust to short-term depression. Specifically, derivative feedback networks with short-term depression that acts differentially on positive and negative feedback projections are capable of dynamically changing their time constant, thus allowing fast onset and slow decay of responses without requiring unrealistically large input transients.

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“…The reduction in cortical GLT1 in both EEDY and EEST mice suggests a change in glutamate related to a motor plan based on early exposure to a complex environment, whether it changes or not. At least part of this glutamate change may involve a shift in the dynamics of glutamate input from thalamus allowing for an increase in recurrent cortical excitation [36]. But the ability to maintain the motor plan throughout the lifespan, which occurs only in EEDY mice, appears to require a corresponding increase in striatal GLT1.…”

Section: Discussionmentioning

confidence: 99%

Early exposure to dynamic environments alters patterns of motor exploration throughout the lifespan

Hong

Estrada‐Sánchez

Barton

et al. 2016

Behavioural Brain Research

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We assessed early rearing conditions on aging-related changes in mouse behavior. Two isolated-housing groups, Running Wheel (IHRW) and Empty Cage (IHEC), were compared against two enriched environments, Static (EEST) and Dynamic (EEDY), both of which included toys and other mice. For EEDY, the location of toys and sources of food and water changed daily, but remained constant for EEST. All mice, randomly assigned to one of the four groups at ~4 weeks of age, remained in their respective environments for 25 weeks followed by single housing in empty cages. Beginning at ~40 weeks of age, all mice were tested at monthly intervals in a plus-shaped maze in which we measured the number of arm entries and the probability of entering a perpendicular arm. Despite making significantly more arm entries than any other group, IHEC mice also were less likely to turn into the left or right arm, a sign of motor inflexibility. Both EEDY and EEST mice showed enhanced turning relative to IHRW and IHEC groups, but only EEDY mice maintained their turning performance for up to ~100 weeks of age. EEDY and EEST mice also were unique in showing an increase in expression of the major glutamate transporter (GLT1) in striatum, but a decrease in motor cortex, suggesting a need for further assessment of environmental manipulations on long-term changes in forebrain glutamate transmission. Our behavioral results indicate that early exposure to continually changing environments, rather than socialization or exercise alone, results in life-long changes in patterns of motor exploration.

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Distinct recurrent versus afferent dynamics in cortical visual processing

Cited by 185 publications

References 63 publications

Anatomy and function of an excitatory network in the visual cortex

Anatomy and function of an excitatory network in the visual cortex

Short-term depression and transient memory in sensory cortex

Early exposure to dynamic environments alters patterns of motor exploration throughout the lifespan

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