Differential properties of cells in the feline primary visual cortex providing the corticofugal feedback to the lateral geniculate nucleus and visual claustrum

Grieve, K. L.; Sillito, Adam M.

doi:10.1523/jneurosci.15-07-04868.1995

Cited by 100 publications

(73 citation statements)

References 34 publications

(52 reference statements)

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“…Past studies in cats, ferrets, and rabbits have subdivided corticogeniculate neurons on the basis of antidromic activation latency (Tsumoto and Suda, 1980;Swadlow and Weyand, 1987;Briggs and Usrey, 2005) and/or visual responses (Tsumoto and Suda, 1980;Greive and Sillito, 1995;Hirsch et al, 1998). Our results from the monkey support the view that there are functionally distinct groups of corticogeniculate neurons.…”

Section: Functional Diversity Of Corticogeniculate Neurons and Implicsupporting

confidence: 82%

A Fast, Reciprocal Pathway between the Lateral Geniculate Nucleus and Visual Cortex in the Macaque Monkey

Briggs¹,

Usrey²

2007

J. Neurosci.

106

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Neurons in the lateral geniculate nucleus (LGN) not only provide feedforward input to primary visual cortex (V1), but also receive robust feedback from the cortex. Accordingly, visual processing in the LGN is continuously influenced by previous patterns of activity. This study examines the temporal properties of feedforward and feedback pathways between the LGN and V1 in the macaque monkey to provide a lower bound on how quickly the cortex can influence the LGN. In so doing, we identified a subclass of corticogeniculate neurons that receives direct, suprathreshold input from the LGN that is similar in latency to that directed to other recipient neurons (4.2 Ϯ 0.4 vs 4.0 Ϯ 0.2 ms). These neurons also provide feedback to the LGN that is significantly shorter in latency than that supplied by corticogeniculate neurons lacking LGN input (5.1 Ϯ 1.3 vs 11.1 Ϯ 2.3 ms, respectively). Across our sample of corticogeniculate neurons, the shortest combined visual response latency and feedback latency was 37 ms (mean, 52.5 Ϯ 3.8 ms), indicating that visual signals can rapidly travel from the periphery to the cortex and back to the LGN.

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Section: Functional Diversity Of Corticogeniculate Neurons and Implicsupporting

confidence: 82%

A Fast, Reciprocal Pathway between the Lateral Geniculate Nucleus and Visual Cortex in the Macaque Monkey

Briggs¹,

Usrey²

2007

J. Neurosci.

106

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“…Thus, particular features of a visual scene could trigger CG activation, causing streamspecific feedback activation of LGN ensembles via the circuit mechanism described above. Interestingly, CG feedback in a variety of species is known to operate on different timescales due to differential axon conduction velocities among the diverse CG neuronal types (35,44,(47)(48)(49)(50)(51). The large variation in axon conduction times suggests that different CG neurons may have shorter or longer timescales over which they can integrate incoming information.…”

Section: Discussionmentioning

confidence: 99%

Corticogeniculate feedback sharpens the temporal precision and spatial resolution of visual signals in the ferret

Hasse

Briggs

2017

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

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The corticogeniculate (CG) pathway connects the visual cortex with the visual thalamus (LGN) in the feedback direction and enables the cortex to directly influence its own input. Despite numerous investigations, the role of this feedback circuit in visual perception remained elusive. To probe the function of CG feedback in a causal manner, we selectively and reversibly manipulated the activity of CG neurons in anesthetized ferrets in vivo using a combined viral-infection and optogenetics approach to drive expression of channelrhodopsin2 (ChR2) in CG neurons. We observed significant increases in temporal precision and spatial resolution of LGN neuronal responses to drifting grating and white noise stimuli when CG neurons expressing ChR2 were light activated. Enhancing CG feedback reduced visually evoked response latencies, increased spike-timing precision, and reduced classical receptive field size. Increased precision among LGN neurons led to increased spike-timing precision among granular layer V1 neurons as well. Together, our findings suggest that the function of CG feedback is to control the timing and precision of thalamic responses to incoming visual signals.T he feedforward progression of sensory information from peripheral receptors through nuclei in the sensory thalamus to the primary sensory cortex is well understood. For example, much is known about how neurons in the primary sensory cortex represent elementary sensory features based on the inputs they receive from peripheral and thalamic neurons with well-defined receptive field properties. In addition to these feedforward circuits, mammalian sensory systems include a substantial feedback projection from the primary sensory cortex to the sensory thalamus (1). Despite a rich history of investigation, the functional role of corticothalamic feedback circuits in sensory perception remains a fundamental mystery in neuroscience.Our goal was to determine the functional contribution of corticothalamic feedback to vision. Corticogeniculate (CG) circuits link the primary visual cortex (V1) with the lateral geniculate nucleus of the thalamus (LGN) and constitute the first cortical feedback connection in the visual processing hierarchy (2). CG axons target LGN relay neurons, local interneurons within the LGN, and neurons in the visual portion of the thalamic reticular nucleus (TRN) that inhibit LGN relay neurons (3-5) (Fig. 1A). Based on this pattern of axonal innervation, CG modulation of LGN neurons could include both monosynaptic excitation and disynaptic inhibition of LGN relay neurons via TRN and/or local LGN inhibitory circuitry. The CG circuit is anatomically robust-cortical synapses onto LGN relay neurons far outnumber retinal synapses (4); however, the receptive fields of LGN relay neurons reflect their retinal and not their cortical inputs (6). In part due to its subtle influence on LGN responses, the function of CG feedback has remained elusive.There have been numerous experimental examinations of CG function-using methods with varying degrees of sele...

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“…In attempting to make sense of the influence of the feedback, it is important to consider the response properties of layer 6 feedback cells. They exhibit low spontaneous activity, have mainly ''simple'' type receptive fields, and are sensitive to stimulus orientation and direction of motion (54). Thus, feedback effects will be evoked by stimuli that drive layer 6 cells and will be seen only when the cortex is functional.…”

Section: Discussionmentioning

confidence: 99%

Corticothalamic feedback enhances stimulus response precision in the visual system

Andolina

Jones

Wang

et al. 2007

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

109

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There is a tightly coupled bidirectional interaction between visual cortex and visual thalamus [lateral geniculate nucleus (LGN)]. Using drifting sinusoidal grating stimuli, we compared the response of cells in the LGN with and without feedback from the visual cortex. Raster plots revealed a striking difference in the response pattern of cells with and without feedback. This difference was reflected in the results from computing vector sum plots and the ratio of zero harmonic to the fundamental harmonic of the fast Fourier transform (FFT) for these responses. The variability of responses assessed by using the Fano factor was also different for the two groups, with the cells without feedback showing higher variability. We examined the covariance of these measures between pairs of simultaneously recorded cells with and without feedback, and they were much more strongly positively correlated with feedback. We constructed orientation tuning curves from the central 5 ms in the raw cross-correlograms of the outputs of pairs of LGN cells, and these curves revealed much sharper tuning with feedback. We discuss the significance of these data for cortical function and suggest that the precision in stimulus-linked firing in the LGN appears as an emergent factor from the corticothalamic interaction.corticofugal feedback ͉ lateral geniculate nucleus ͉ synchronization ͉ visual processing T he patterning of activity in the brain, whether by the grouping of action potentials or synchronization of firing across sets of neurons, can have a major impact on the effectiveness with which information is transferred to other brain areas (1, 2). Common to many sensory pathways, both burst firing and tightly timed monoand/or heterosynaptic inputs have been argued to increase the effectiveness with which thalamic input can drive the cortex (3-7). In the visual system heterosynaptic thalamic inputs from the dorsal lateral geniculate nucleus (LGN) that fall within 5 ms of each other exhibit a supralinear enhancement of transmission to visual cortical simple cells (7). The ability of visual stimuli to generate heterosynaptic facilitation from the convergent inputs of LGN cells on cortical cells will depend on the precision in the way the LGN cells respond to visual stimuli. We know that the corticofugal feedback to the thalamus has a strong influence on this patterning via direct connections to the thalamus and thalamic reticular nucleus (8)(9)(10)(11)(12)(13)(14). In many ways the thalamus, thalamic reticular nucleus, and cortex form part of a circuit rather than distinct steps in an ascending system. How does this interaction serve to refine the way the thalamus accesses the cortex?Clearly, the precision in the timing and structure of the firing pattern to visual stimuli is critically important in understanding their neural representation and impact. One can hypothesize that the contrast edges of a complex object moving through visual space could provoke synchronous firing in groups of thalamic cells that optimally drive the representation...

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Differential properties of cells in the feline primary visual cortex providing the corticofugal feedback to the lateral geniculate nucleus and visual claustrum

Cited by 100 publications

References 34 publications

A Fast, Reciprocal Pathway between the Lateral Geniculate Nucleus and Visual Cortex in the Macaque Monkey

A Fast, Reciprocal Pathway between the Lateral Geniculate Nucleus and Visual Cortex in the Macaque Monkey

Corticogeniculate feedback sharpens the temporal precision and spatial resolution of visual signals in the ferret

Corticothalamic feedback enhances stimulus response precision in the visual system

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