Morphological evidence for multiple distinct channels of corticogeniculate feedback originating in mid-level extrastriate visual areas of the ferret

Adusei, Matthew; Hasse, J. Michael; Briggs, Farran

doi:10.1007/s00429-021-02385-7

Cited by 4 publications

(14 citation statements)

References 63 publications

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“…Individual neuronal dendritic morphologies were reconstructed under higher magnification (20–40×). Virus-labeled extrastriate corticogeniculate neurons were verified to have their cell bodies located in layer 6, consistent with prior observations of corticogeniculate neurons in V1/area 17 and V2/area 18 in primates and carnivores ( Gilbert and Kelly, 1975 ; Lund et al, 1975 ; Lin and Kaas, 1977 ; Katz, 1987 ; Fitzpatrick et al, 1994 ; Usrey and Fitzpatrick, 1996 ; Ichida et al, 2014 ; Briggs et al, 2016 ; Hasse and Briggs, 2017a ; Hasse et al, 2019 ; Adusei et al, 2021 ). Only six (four in MT and two in MST) out of ∼4,000 virus-labeled corticogeniculate neurons across all three monkeys appeared to have cell bodies displaced outside of layer 6.…”

Section: Methodssupporting

confidence: 88%

“…Clustering algorithms, principal components analysis (PCA), and statistical methods were used to evaluate morphological differences between reconstructed corticogeniculate neurons, as described previously ( Briggs et al, 2016 ; Bragg et al, 2017 ; Bragg and Briggs, 2017 ; Hasse et al, 2019 ; Adusei et al, 2021 ). Neurolucida Explorer (MicroBrightField) was used to extract the following morphological metrics from each reconstructed corticogeniculate neuron.…”

Section: Methodsmentioning

confidence: 99%

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Parallel Streams of Direct Corticogeniculate Feedback from Mid-level Extrastriate Cortex in the Macaque Monkey

Adusei,

Callaway,

Usrey

et al. 2024

eNeuro

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First order thalamic nuclei receive feedforward signals from peripheral receptors and relay these signals to primary sensory cortex. Primary sensory cortex, in turn, provides reciprocal feedback to first order thalamus. Because the vast majority of sensory thalamocortical inputs target primary sensory cortex, their complementary corticothalamic neurons are assumed to be similarly restricted to primary sensory cortex. We upend this assumption by characterizing morphologically diverse neurons in multiple mid-level visual cortical areas of the primate (Macaca mulatta) brain that provide direct feedback to the primary visual thalamus, the dorsal lateral geniculate nucleus (LGN). Although the majority of geniculocortical neurons project to primary visual cortex (V1), a minority, located mainly in the koniocellular LGN layers, provide direct input to extrastriate visual cortex. These “V1-bypassing” projections may be implicated in blindsight. We hypothesized that geniculocortical inputs directly targeting extrastriate cortex should be complemented by reciprocal corticogeniculate circuits. Using virus-mediated circuit tracing, we discovered corticogeniculate neurons throughout three mid-level extrastriate areas: MT, MST, and V4. Quantitative morphological analyses revealed non-uniform distributions of unique cell types across areas. Many extrastriate corticogeniculate neurons had spiny stellate morphology, suggesting possible targeting of koniocellular LGN layers. Importantly though, multiple morphological types were observed across areas. Such morphological diversity could suggest parallel streams of V1-bypassing corticogeniculate feedback at multiple stages of the visual processing hierarchy. Furthermore, the presence of corticogeniculate neurons across visual cortex necessitates a reevaluation of the LGN as a hub for visual information rather than a simple relay.Significance StatementFirst order thalamic nuclei are most strongly connected in feedforward and feedback directions with primary sensory cortex. In the visual system, direct feedforward circuits link the visual thalamus with higher-order, extrastriate visual areas, although the function of these less-common pathways remains unknown. Here we demonstrate for the first time the presence of complementary direct feedback connections between multiple extrastriate visual cortical areas and the visual thalamus in the primate brain. Although sparse, extrastriate corticogeniculate circuits are consistently present and contain morphologically diverse neurons, suggesting parallel streams of extrastriate feedback. These findings indicate an evolutionary conservation of circuits that integrate information from throughout the visual processing hierarchy within the visual thalamus.

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Section: Methodssupporting

confidence: 88%

Section: Methodsmentioning

confidence: 99%

Parallel Streams of Direct Corticogeniculate Feedback from Mid-level Extrastriate Cortex in the Macaque Monkey

Adusei,

Callaway,

Usrey

et al. 2024

eNeuro

Self Cite

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show abstract

“…LGN cells are largely monocular ( Casagrande and Boyd, 1996 ), organized in layers based on cell type (magno- parvo-cellular layers with intermixed konio-cells) and eye-of-origin (ipsi- and contralateral). However, there are indications that interocular interactions are possible in LGN ( Dougherty et al, 2021 ; Zeater et al, 2015 ), either due to local interthalamic circuits ( Dougherty et al, 2019 ) or to the large contingent of corticothalamic fibers that feedback into LGN from striate and extrastriate visual areas ( Adusei et al, 2021 ; Briggs and Usrey, 2011 ; Fitzpatrick et al, 2009 ; Hendrickson et al, 1978 ; Lund et al, 1975 ). Whichever their origin, these interocular interactions could account for the oscillations of LGN BOLD responses during binocular rivalry, shown in seminal work by Wunderlich et al, 2005 and Haynes et al, 2005 .…”

Section: Introductionmentioning

confidence: 99%

Short-term plasticity in the human visual thalamus

Kurzawski

Lunghi

Biagi

et al. 2022

eLife

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While there is evidence that the visual cortex retains a potential for plasticity in adulthood, less is known about the subcortical stages of visual processing. Here we asked whether short-term ocular dominance plasticity affects the human visual thalamus. We addressed this question in normally sighted adult humans, using ultra-high field (7T) magnetic resonance imaging combined with the paradigm of short-term monocular deprivation. With this approach, we previously demonstrated transient shifts of perceptual eye dominance and ocular dominance in visual cortex (Binda et al., 2018). Here we report evidence for short-term plasticity in the ventral division of the pulvinar (vPulv), where the deprived eye representation was enhanced over the non-deprived eye. This ventral-pulvinar plasticity was similar as previously seen in visual cortex and it was correlated with the ocular dominance shift measured behaviorally. In contrast, there was no effect of monocular deprivation in two adjacent thalamic regions: dorsal pulvinar (dPulv), and Lateral Geniculate Nucleus (LGN). We conclude that the visual thalamus retains potential for short-term plasticity in adulthood; the plasticity effect differs across thalamic subregions, possibly reflecting differences in their cortico-fugal connectivity.

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“…Most surprising, however, was the strong, inverse coupling of face patch neurons with the entire LGN of both hemispheres. While anatomical projections linking the temporal cortex and LGN have been reported, current evidence suggests that they are extremely sparse, particularly in the adult ( 43 , 45 ), although this is an active topic of investigation ( 46 , 47 ). A more likely explanation is that the LGN correlations stem from changes in brain states conferred to the thalamus by neuromodulation, such as cholinergic modulation stemming from the PPT ( 48 , 49 ).…”

Section: Discussionmentioning

confidence: 99%

Brain-wide functional connectivity of face patch neurons during rest

Zaldívar

Koyano

et al. 2022

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

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The brain is a highly organized, dynamic system whose network architecture is often assessed through resting functional magnetic resonance imaging (fMRI) functional connectivity. The functional interactions between brain areas, including those observed during rest, are assumed to stem from the collective influence of action potentials carried by long-range neural projections. However, the contribution of individual neurons to brain-wide functional connectivity has not been systematically assessed. Here we developed a method to concurrently measure and compare the spiking activity of local neurons with fMRI signals measured across the brain during rest. We recorded spontaneous activity from neural populations in cortical face patches in the macaque during fMRI scanning sessions. Individual cells exhibited prominent, bilateral coupling with fMRI fluctuations in a restricted set of cortical areas inside and outside the face patch network, partially matching the pattern of known anatomical projections. Within each face patch population, a subset of neurons was positively coupled with the face patch network and another was negatively coupled. The same cells showed inverse correlations with distinct subcortical structures, most notably the lateral geniculate nucleus and brainstem neuromodulatory centers. Corresponding connectivity maps derived from fMRI seeds and local field potentials differed from the single unit maps, particularly in subcortical areas. Together, the results demonstrate that the spiking fluctuations of neurons are selectively coupled with discrete brain regions, with the coupling governed in part by anatomical network connections and in part by indirect neuromodulatory pathways.

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Morphological evidence for multiple distinct channels of corticogeniculate feedback originating in mid-level extrastriate visual areas of the ferret

Cited by 4 publications

References 63 publications

Parallel Streams of Direct Corticogeniculate Feedback from Mid-level Extrastriate Cortex in the Macaque Monkey

Parallel Streams of Direct Corticogeniculate Feedback from Mid-level Extrastriate Cortex in the Macaque Monkey

Short-term plasticity in the human visual thalamus

Brain-wide functional connectivity of face patch neurons during rest

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