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

2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Caitlin Siu ◽  
Justin Balsor ◽  
Sam Merlin ◽  
Frederick Federer ◽  
Alessandra Angelucci

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.

Author(s):  
Caitlin Siu ◽  
Justin Balsor ◽  
Frederick Federer ◽  
Alessandra Angelucci

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.


Author(s):  
Caitlin Siu ◽  
Justin Balsor ◽  
Frederick Federer ◽  
Alessandra Angelucci

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.


2017 ◽  
Author(s):  
Yunyun Han ◽  
Justus M Kebschull ◽  
Robert AA Campbell ◽  
Devon Cowan ◽  
Fabia Imhof ◽  
...  

The wiring diagram of the neocortex determines how information is processed across dozens of cortical areas. Each area communicates with multiple others via extensive long-range axonal projections 1–6, but the logic of inter-area information transfer is unresolved. Specifically, the extent to which individual neurons send dedicated projections to single cortical targets or distribute their signals across multiple areas remains unclear5,7–20. Distinguishing between these possibilities has been challenging because axonal projections of only a few individual neurons have been reconstructed. Here we map the projection patterns of axonal arbors from 591 individual neurons in mouse primary visual cortex (V1) using two complementary methods: whole-brain fluorescence-based axonal tracing21,22 and high-throughput DNA sequencing of genetically barcoded neurons (MAPseq)23. Although our results confirm the existence of dedicated projections to certain cortical areas, we find these are the exception, and that the majority of V1 neurons broadcast information to multiple cortical targets. Furthermore, broadcasting cells do not project to all targets randomly, but rather comprise subpopulations that either avoid or preferentially innervate specific subsets of cortical areas. Our data argue against a model of dedicated lines of intracortical information transfer via “one neuron – one target area” mapping. Instead, long-range communication between a sensory cortical area and its targets may be based on a principle whereby individual neurons copy information to, and potentially coordinate activity across, specific subsets of cortical areas.


2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Brittany C. Clawson ◽  
Emily J. Pickup ◽  
Amy Ensing ◽  
Laura Geneseo ◽  
James Shaver ◽  
...  

AbstractLearning-activated engram neurons play a critical role in memory recall. An untested hypothesis is that these same neurons play an instructive role in offline memory consolidation. Here we show that a visually-cued fear memory is consolidated during post-conditioning sleep in mice. We then use TRAP (targeted recombination in active populations) to genetically label or optogenetically manipulate primary visual cortex (V1) neurons responsive to the visual cue. Following fear conditioning, mice respond to activation of this visual engram population in a manner similar to visual presentation of fear cues. Cue-responsive neurons are selectively reactivated in V1 during post-conditioning sleep. Mimicking visual engram reactivation optogenetically leads to increased representation of the visual cue in V1. Optogenetic inhibition of the engram population during post-conditioning sleep disrupts consolidation of fear memory. We conclude that selective sleep-associated reactivation of learning-activated sensory populations serves as a necessary instructive mechanism for memory consolidation.


2000 ◽  
Vol 17 (1) ◽  
pp. 71-76 ◽  
Author(s):  
JOHN D. ALLISON ◽  
PETER MELZER ◽  
YUCHUAN DING ◽  
A.B. BONDS ◽  
VIVIEN A. CASAGRANDE

How neurons in the primary visual cortex (V1) of primates process parallel inputs from the magnocellular (M) and parvocellular (P) layers of the lateral geniculate nucleus (LGN) is not completely understood. To investigate whether signals from the two pathways are integrated in the cortex, we recorded contrast-response functions (CRFs) from 20 bush baby V1 neurons before, during, and after pharmacologically inactivating neural activity in either the contralateral LGN M or P layers. Inactivating the M layer reduced the responses of V1 neurons (n = 10) to all stimulus contrasts and significantly elevated (t = 8.15, P < 0.01) their average contrast threshold from 8.04 (± 4.1)% contrast to 22.46 (± 6.28)% contrast. M layer inactivation also significantly reduced (t = 4.06, P < 0.01) the average peak response amplitude. Inactivating the P layer did not elevate the average contrast threshold of V1 neurons (n = 10), but significantly reduced (t = 4.34, P < 0.01) their average peak response amplitude. These data demonstrate that input from the M pathway can account for the responses of V1 neurons to low stimulus contrasts and also contributes to responses to high stimulus contrasts. The P pathway appears to influence mainly the responses of V1 neurons to high stimulus contrasts. None of the cells in our sample, which included cells in all output layers of V1, appeared to receive input from only one pathway. These findings support the view that many V1 neurons integrate information about stimulus contrast carried by the LGN M and P pathways.


Neuron ◽  
2018 ◽  
Vol 100 (6) ◽  
pp. 1313-1321.e6 ◽  
Author(s):  
Mean-Hwan Kim ◽  
Petr Znamenskiy ◽  
Maria Florencia Iacaruso ◽  
Thomas D. Mrsic-Flogel

2007 ◽  
Vol 97 (3) ◽  
pp. 2215-2229 ◽  
Author(s):  
Allan T. Gulledge ◽  
Susanna B. Park ◽  
Yasuo Kawaguchi ◽  
Greg J. Stuart

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.


2021 ◽  
Vol 4 (1) ◽  
Author(s):  
Jan C. Frankowski ◽  
Andrzej T. Foik ◽  
Alexa Tierno ◽  
Jiana R. Machhor ◽  
David C. Lyon ◽  
...  

AbstractPrimary sensory areas of the mammalian neocortex have a remarkable degree of plasticity, allowing neural circuits to adapt to dynamic environments. However, little is known about the effects of traumatic brain injury on visual circuit function. Here we used anatomy and in vivo electrophysiological recordings in adult mice to quantify neuron responses to visual stimuli two weeks and three months after mild controlled cortical impact injury to primary visual cortex (V1). We found that, although V1 remained largely intact in brain-injured mice, there was ~35% reduction in the number of neurons that affected inhibitory cells more broadly than excitatory neurons. V1 neurons showed dramatically reduced activity, impaired responses to visual stimuli and weaker size selectivity and orientation tuning in vivo. Our results show a single, mild contusion injury produces profound and long-lasting impairments in the way V1 neurons encode visual input. These findings provide initial insight into cortical circuit dysfunction following central visual system neurotrauma.


Perception ◽  
2022 ◽  
Vol 51 (1) ◽  
pp. 60-69
Author(s):  
Li Zhaoping

Finding a target among uniformly oriented non-targets is typically faster when this target is perpendicular, rather than parallel, to the non-targets. The V1 Saliency Hypothesis (V1SH), that neurons in the primary visual cortex (V1) signal saliency for exogenous attentional attraction, predicts exactly the opposite in a special case: each target or non-target comprises two equally sized disks displaced from each other by 1.2 disk diameters center-to-center along a line defining its orientation. A target has two white or two black disks. Each non-target has one white disk and one black disk, and thus, unlike the target, activates V1 neurons less when its orientation is parallel rather than perpendicular to the neurons’ preferred orientations. When the target is parallel, rather than perpendicular, to the uniformly oriented non-targets, the target’s evoked V1 response escapes V1’s iso-orientation surround suppression, making the target more salient. I present behavioral observations confirming this prediction.


2019 ◽  
Vol 121 (6) ◽  
pp. 2202-2214 ◽  
Author(s):  
John P. McClure ◽  
Pierre-Olivier Polack

Multimodal sensory integration facilitates the generation of a unified and coherent perception of the environment. It is now well established that unimodal sensory perceptions, such as vision, are improved in multisensory contexts. Whereas multimodal integration is primarily performed by dedicated multisensory brain regions such as the association cortices or the superior colliculus, recent studies have shown that multisensory interactions also occur in primary sensory cortices. In particular, sounds were shown to modulate the responses of neurons located in layers 2/3 (L2/3) of the mouse primary visual cortex (V1). Yet, the net effect of sound modulation at the V1 population level remained unclear. In the present study, we performed two-photon calcium imaging in awake mice to compare the representation of the orientation and the direction of drifting gratings by V1 L2/3 neurons in unimodal (visual only) or multimodal (audiovisual) conditions. We found that sound modulation depended on the tuning properties (orientation and direction selectivity) and response amplitudes of V1 L2/3 neurons. Sounds potentiated the responses of neurons that were highly tuned to the cue’s orientation and direction but weakly active in the unimodal context, following the principle of inverse effectiveness of multimodal integration. Moreover, sound suppressed the responses of neurons untuned for the orientation and/or the direction of the visual cue. Altogether, sound modulation improved the representation of the orientation and direction of the visual stimulus in V1 L2/3. Namely, visual stimuli presented with auditory stimuli recruited a neuronal population better tuned to the visual stimulus orientation and direction than when presented alone. NEW & NOTEWORTHY The primary visual cortex (V1) receives direct inputs from the primary auditory cortex. Yet, the impact of sounds on visual processing in V1 remains controverted. We show that the modulation by pure tones of V1 visual responses depends on the orientation selectivity, direction selectivity, and response amplitudes of V1 neurons. Hence, audiovisual stimuli recruit a population of V1 neurons better tuned to the orientation and direction of the visual stimulus than unimodal visual stimuli.


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