Cortical connectivity and sensory coding

Harris, Kenneth D.; Mrsic-Flogel, Thomas D.

doi:10.1038/nature12654

Cited by 563 publications

(528 citation statements)

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“…Additionally, the sparse responses and localized connectivity in superficial-layer PCs compared with deep PCs underlie the weaker correlations between PCs in superficial layers compared with those in deep layers (30,42,48). Third, the density of connections among neurons in a population impacts how much sensory stimulation controls population activity; pairwise correlations in evoked and spontaneous activity are significantly more similar in heavily interconnected populations of INs than in populations of PCs with sparser connectivity (23,42). Fourth, correlations in evoked and spontaneous activity vary with anatomical distance based on the spatial extent of connectivity.…”

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

“…Sensory information from the thalamus largely targets the intermediate layer 4 and sparsely targets the layer 5/6 border (23,24). From layer 4, axonal projections go to the superficial layers 2/3 and then to the deep layers 5/6, where information is distributed to other cortical and subcortical targets (23,25). In primary auditory (A1), visual (V1), and somatosensory (S1) cortices, receptive fields are simple and separable in layer 4 and more complex and nonlinear in superficial and deep layers (26)(27)(28)(29).…”

Section: Resultsmentioning

confidence: 99%

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Coding principles of the canonical cortical microcircuit in the avian brain

Calabrese

Woolley

2015

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

113

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Mammalian neocortex is characterized by a layered architecture and a common or "canonical" microcircuit governing information flow among layers. This microcircuit is thought to underlie the computations required for complex behavior. Despite the absence of a six-layered cortex, birds are capable of complex cognition and behavior. In addition, the avian auditory pallium is composed of adjacent information-processing regions with genetically identified neuron types and projections among regions comparable with those found in the neocortex. Here, we show that the avian auditory pallium exhibits the same information-processing principles that define the canonical cortical microcircuit, long thought to have evolved only in mammals. These results suggest that the canonical cortical microcircuit evolved in a common ancestor of mammals and birds and provide a physiological explanation for the evolution of neural processes that give rise to complex behavior in the absence of cortical lamination.functional connectivity | cortex evolution | songbird | sensory coding T he cognitive abilities of birds suggest that the avian brain contains sophisticated information-processing circuitry. Recent studies have demonstrated that corvids, such as crows, rooks, and jays, exhibit innovative tool manufacture (1), referential gesturing (2), causal reasoning (3, 4), mirror self-recognition (5), and planning for future needs using recent experience (6). Other birds can perform complex pattern recognition (7), long-term recollection (8), and numerical discrimination (9), paralleling the performance of primates. Songbirds, such as zebra finches (Taeniopygia guttata, the species studied here), learn to produce and recognize complex vocalizations for social communication, with numerous parallels to speech learning and perception (10).Although cognitive skills in birds and nonhuman mammals are often comparable, avian and mammalian palliums exhibit very different anatomical organization. Although the organization of ascending sensory pathways and subpallial structures are similar in avian and mammalian brains (11), the avian pallium (referred to hereafter as the cortex) lacks the distinctive six-layered structure of the mammalian neocortex (12). Instead of a laminar structure, the avian cortex is composed of interconnected nuclei and bands of neurons that form distinct processing regions. The avian primary auditory cortex (avian A1) is organized into adjacent processing regions, collectively called the field L/CM (caudal mesopallium) complex, that are stacked in a dorsorostral to ventrocaudal orientation (13, 14) ( Fig. 1 and Fig. S1). Regions of avian A1 are delineated by differences in cytoarchitecture and connectivity (13, 15) (SI Materials and Methods) and are organized into superficial (field L1 and lateral caudal mesopallium, CML), intermediate (field L2a and -b), and deep (field L3) regions, similar to neocortical layers. A posterior region, the caudal nidopallium (NC) is referred to as "secondary" cortex here. Fig. 2A shows a schemati...

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

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Coding principles of the canonical cortical microcircuit in the avian brain

Calabrese

Woolley

2015

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

113

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“…The interaction between topdown and bottom-up signals in sensory cortices is a fast-growing and increasingly important area of research for cognitive neuroscience. At standard imaging resolutions, however, fMRI responses comprise an amalgamation of both bottom-up and top-down responses Harris & Mrsic-Flogel, 2013;Rockland & Pandya, 1979). Most research distinguishing between bottom-up and top-down functional signals has been performed on non-human primates using so-called laminar electrodes (Self et al, 2013;Van Kerkoerle, Self, & Roelfsema, 2017), where multiple contact points, spaced 100 micrometers apart, allowed for the simultaneous recording of multiunit neural activity and current-source density at different cortical depths.…”

Section: Introductionmentioning

confidence: 99%

Laminar fMRI: Applications for cognitive neuroscience

et al. 2019

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Highlights Recent developments in high spatial resolution fMRI allow for functional imaging of human cortical layers (laminar fMRI)  Feedforward and feedback responses can be dissociated by their laminar profiles  In vivo measurements of feedforward and feedback responses in humans with laminar fMRI have many, far-reaching applications for cognitive neuroscience  We review recent laminar fMRI studies, and several areas of cognitive neuroscience that stand to benefit from this exciting technological development AbstractThe cortex is a massively recurrent network, characterised by feedforward and feedback connections between brain areas as well as lateral connections within an area. areas at a more fine-grained level than previously possible in the human species. In this review,we highlight recent studies that successfully used laminar fMRI to isolate layer-specific feedback responses in human sensory cortex. In addition, we review several areas of cognitive neuroscience that stand to benefit from this new technological development, highlighting contemporary hypotheses that yield testable predictions for laminar fMRI. We hope to encourage researchers with the opportunity to embrace this development in fMRI research, as we expect that many future advancements in our current understanding of human brain function will be gained from measuring lamina-specific brain responses.

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“…Synaptic inhibition in the cerebral cortex is fundamental for neuronal modulation (6), including gain control (7), response selectivity (8,9), and synchronized activities (10,11). Inhibition-based modulations may contribute to stimulusdriven behaviors and associative memories of sensory stimuli (12); however, it remains unclear whether neuronal silencing (i.e., a transient reduction in firing rates from their spontaneous level) by itself can serve as a memory trace and bring about behavioral expressions. In this study, we tested this possibility by optogenetically silencing auditory cortical neurons.…”

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confidence: 99%

Memory formation and retrieval of neuronal silencing in the auditory cortex

Nomura

Hara

Abe

et al. 2015

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

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Sensory stimuli not only activate specific populations of cortical neurons but can also silence other populations. However, it remains unclear whether neuronal silencing per se leads to memory formation and behavioral expression. Here we show that mice can report optogenetic inactivation of auditory neuron ensembles by exhibiting fear responses or seeking a reward. Mice receiving pairings of footshock and silencing of a neuronal ensemble exhibited a fear response selectively to the subsequent silencing of the same ensemble. The valence of the neuronal silencing was preserved for at least 30 d and was susceptible to extinction training. When we silenced an ensemble in one side of auditory cortex for conditioning, silencing of an ensemble in another side induced no fear response. We also found that mice can find a reward based on the presence or absence of the silencing. Neuronal silencing was stored as working memory. Taken together, we propose that neuronal silencing without explicit activation in the cerebral cortex is enough to elicit a cognitive behavior.fear conditioning | operant conditioning | optogenetics | neuronal inhibition | auditory cortex C ortical neurons exhibit spontaneous activity without explicit external stimuli (1-3), which may not only increase, but also be suppressed, by sensory stimuli (4, 5). For example, auditory stimuli suppress a subset of auditory cortical neurons in a frequency-dependent manner (5). Synaptic inhibition in the cerebral cortex is fundamental for neuronal modulation (6), including gain control (7), response selectivity (8, 9), and synchronized activities (10, 11). Inhibition-based modulations may contribute to stimulusdriven behaviors and associative memories of sensory stimuli (12); however, it remains unclear whether neuronal silencing (i.e., a transient reduction in firing rates from their spontaneous level) by itself can serve as a memory trace and bring about behavioral expressions. In this study, we tested this possibility by optogenetically silencing auditory cortical neurons. ResultsArchaerhodopsin Expression in the Auditory Cortex. To silence excitatory neurons in the auditory cortex, we injected an adenoassociated virus vector expressing archaerhodopsin (Arch) (13) under the control of the calcium/calmodulin-dependent protein kinase II (CaMKII) promoter (AAV-CaMKII-Arch-EYFP) into the auditory cortex of mice (Fig. 1A). Three weeks after virus injection, we observed robust expression of Arch-EYFP in the auditory cortex (Fig. 1B). We obtained whole-cell recordings from Arch-expressing neurons in auditory cortical slices and confirmed that green-light illumination induced an outward current and inhibited action potentials induced by depolarizing current injections ( Fig. 1 C and D). To confirm the inhibitory effect in vivo, we recorded multiunit activities from the auditory cortex of the anesthetized mice. The overall firing rate was reduced by 29.2 ± 7.7% during green-light illumination (eight tetrodes from two mice) (Fig. 1E).Neuronal Silencing Induces Conditio...

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Cortical connectivity and sensory coding

Cited by 563 publications

References 120 publications

Coding principles of the canonical cortical microcircuit in the avian brain

Coding principles of the canonical cortical microcircuit in the avian brain

Laminar fMRI: Applications for cognitive neuroscience

Memory formation and retrieval of neuronal silencing in the auditory cortex

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