A direct interareal feedback-to-feedforward circuit in primate visual cortex

Mapping Intimacies ◽

10.21203/rs.3.rs-50399/v1 ◽

2020 ◽

Cited By ~ 1

Author(s):

Caitlin Siu ◽

Justin Balsor ◽

Frederick Federer ◽

Alessandra Angelucci

Keyword(s):

Visual Cortex ◽

Projection Neurons ◽

Cortical Areas ◽

Computational Work ◽

Primate Visual Cortex ◽

Similar Area ◽

Hierarchical Computation

Abstract The mammalian sensory neocortex consists of hierarchically organized areas reciprocally connected via feedforward (FF) and feedback (FB) circuits. Several theories of hierarchical computation ascribe the bulk of the computational work of the cortex to looped FF-FB circuits between pairs of cortical areas. However, whether such corticocortical loops exist remains unclear. In higher mammals, FF projections send afferents almost exclusively to a single higher-level area. However, it is unclear whether FB projections show similar area-specificity, and whether they influence FF-projection neurons directly or indirectly. Using viral-mediated monosynaptic circuit tracing in macaque visual cortex, we find that neurons sending FF projections to a higher-level area receive monosynaptic FB inputs exclusively from that area. We also find monosynaptic FB-to-FB neuron contacts as a second motif of FB connectivity. Our results support the existence of FF-FB loops in primate cortex, and suggest that FB can rapidly and selectively influence the activity of incoming FF signals.

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A direct interareal feedback-to-feedforward circuit in primate visual cortex

Nature Communications ◽

10.1038/s41467-021-24928-6 ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Caitlin Siu ◽

Justin Balsor ◽

Sam Merlin ◽

Frederick Federer ◽

Alessandra Angelucci

Keyword(s):

Visual Cortex ◽

Primary Visual Cortex ◽

Projection Neurons ◽

V1 Neurons ◽

Cortical Areas ◽

Area V2 ◽

Computational Work ◽

Primate Visual Cortex ◽

Similar Area ◽

Hierarchical Computation

AbstractThe mammalian sensory neocortex consists of hierarchically organized areas reciprocally connected via feedforward (FF) and feedback (FB) circuits. Several theories of hierarchical computation ascribe the bulk of the computational work of the cortex to looped FF-FB circuits between pairs of cortical areas. However, whether such corticocortical loops exist remains unclear. In higher mammals, individual FF-projection neurons send afferents almost exclusively to a single higher-level area. However, it is unclear whether FB-projection neurons show similar area-specificity, and whether they influence FF-projection neurons directly or indirectly. Using viral-mediated monosynaptic circuit tracing in macaque primary visual cortex (V1), we show that V1 neurons sending FF projections to area V2 receive monosynaptic FB inputs from V2, but not other V1-projecting areas. We also find monosynaptic FB-to-FB neuron contacts as a second motif of FB connectivity. Our results support the existence of FF-FB loops in primate cortex, and suggest that FB can rapidly and selectively influence the activity of incoming FF signals.

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A direct interareal feedback-to-feedforward circuit in primate visual cortex

10.1101/2020.07.07.192450 ◽

2020 ◽

Cited By ~ 1

Author(s):

Caitlin Siu ◽

Justin Balsor ◽

Frederick Federer ◽

Alessandra Angelucci

Keyword(s):

Visual Cortex ◽

Projection Neurons ◽

Cortical Areas ◽

Computational Work ◽

Primate Visual Cortex ◽

Similar Area ◽

Hierarchical Computation

ABSTRACTThe mammalian sensory neocortex consists of hierarchically organized areas reciprocally connected via feedforward (FF) and feedback (FB) circuits. Several theories of hierarchical computation ascribe the bulk of the computational work of the cortex to looped FF-FB circuits between pairs of cortical areas. However, whether such corticocortical loops exist remains unclear. In higher mammals, FF projections send afferents almost exclusively to a single higher-level area. However, it is unclear whether FB projections show similar area-specificity, and whether they influence FF-projection neurons directly or indirectly. Using viral-mediated monosynaptic circuit tracing in macaque visual cortex, we find that neurons sending FF projections to a higher-level area receive monosynaptic FB inputs exclusively from that area. We also find monosynaptic FB-to-FB neuron contacts as a second motif of FB connectivity. Our results support the existence of FF-FB loops in primate cortex, and suggest that FB can rapidly and selectively influence the activity of incoming FF signals.

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Heterogeneity of Phasic Cholinergic Signaling in Neocortical Neurons

Journal of Neurophysiology ◽

10.1152/jn.00493.2006 ◽

2007 ◽

Vol 97 (3) ◽

pp. 2215-2229 ◽

Cited By ~ 118

Author(s):

Allan T. Gulledge ◽

Susanna B. Park ◽

Yasuo Kawaguchi ◽

Greg J. Stuart

Keyword(s):

Visual Cortex ◽

Calcium Release ◽

Pyramidal Neurons ◽

Potassium Conductance ◽

Projection Neurons ◽

Sk Channels ◽

Cortical Areas ◽

Neocortical Neurons ◽

Cholinergic Signaling ◽

Nonpyramidal Neurons

Acetylcholine (ACh) is a neurotransmitter critical for normal cognition. Here we demonstrate heterogeneity of cholinergic signaling in neocortical neurons in the rat prefrontal, somatosensory, and visual cortex. Focal ACh application (100 μM) inhibited layer 5 pyramidal neurons in all cortical areas via activation of an apamin-sensitive SK-type calcium-activated potassium conductance. Cholinergic inhibition was most robust in prefrontal layer 5 neurons, where it relies on the same signal transduction mechanism (M1-like receptors, IP3-dependent calcium release, and SK-channels) as exists in somatosensory pyramidal neurons. Pyramidal neurons in layer 2/3 were less responsive to ACh, but substantial apamin-sensitive inhibitory responses occurred in deep layer 3 neurons of the visual cortex. ACh was only inhibitory when presented near the somata of layer 5 pyramidal neurons, where repetitive ACh applications generated discrete inhibitory events at frequencies of up to ∼0.5 Hz. Fast-spiking (FS) nonpyramidal neurons in all cortical areas were unresponsive to ACh. When applied to non-FS interneurons in layers 2/3 and 5, ACh generated mecamylamine-sensitive nicotinic responses (38% of cells), apamin-insensitive hyperpolarizing responses, with or without initial nicotinic depolarization (7% of neurons), or no response at all (55% of cells). Responses in interneurons were similar across cortical layers and regions but were correlated with cellular physiology and the expression of biochemical markers associated with different classes of nonpyramidal neurons. Finally, ACh generated nicotinic responses in all layer 1 neurons tested. These data demonstrate that phasic cholinergic input can directly inhibit projection neurons throughout the cortex while sculpting intracortical processing, especially in superficial layers.

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Top-Down Feedback Controls Spatial Summation and Response Gain in Primate Visual Cortex

10.1101/094680 ◽

2016 ◽

Cited By ~ 1

Author(s):

Lauri Nurminen ◽

Sam Merlin ◽

Maryam Bijanzadeh ◽

Frederick Federer ◽

Alessandra Angelucci

Keyword(s):

Visual Cortex ◽

Lower Order ◽

Image Features ◽

Field Size ◽

Cellular Mechanisms ◽

Feedback Controls ◽

Cortical Areas ◽

Visual Spatial ◽

Primate Visual Cortex ◽

Feedback Connections

ABSTRACTIn the cerebral cortex, sensory information travels along feedforward connections through a hierarchy of areas, which, in turn, send a denser network of feedback connections to lower-order areas. Feedback has been implicated in attention, expectation, and sensory context, but the cellular mechanisms underlying these diverse feedback functions are unknown. Using specific optogenetic inactivation of feedback connections in the primate visual cortex, we have identified the cellular mechanisms of feedback-mediated modulations of early sensory processing. Specifically, we found that feedback modulates receptive field size, surround suppression and response gain, similar to the modulatory effects of visual spatial attention. A recurrent network model captured these effects. These feedback-mediated modulations allow higher-order cortical areas to dynamically regulate spatial resolution, sensitivity to image features, and efficiency of coding natural images in lower-order cortical areas.

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