Complex Effects on In Vivo Visual Responses by Specific Projections from Mouse Cortical Layer 6 to Dorsal Lateral Geniculate Nucleus

Denman, Daniel J.; Contreras, Diego

doi:10.1523/jneurosci.0027-15.2015

Cited by 87 publications

(115 citation statements)

References 75 publications

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“…Indeed, numerous studies using a variety of experimental techniques to manipulate CG feedback have documented changes in the magnitude of LGN responses (7)(8)(9)(10)(11)(12)(13)(14). Our results are consistent with some, but not all, of these observations.…”

Section: Discussionsupporting

confidence: 90%

“…The notion that CG feedback sharpens the spatial resolution of LGN responses is further supported by computational models of LGN-V1-TRN circuits in which stimulation of retinotopically aligned V1/LGN neurons led to enhanced activity in LGN relay neurons with aligned receptive fields and suppressed activity in neighboring relay neurons (33). Interestingly, CG feedback in the mouse visual system does not appear to modulate the size of the classical receptive field or the influence of the surround among LGN neurons (8). Although species differences could explain these contradictory findings, the prediction that CG feedback enhances surround suppression in a highly visual mammal remains to be tested using selective methods.…”

Section: Discussionmentioning

confidence: 99%

“…First, we determined that the vast majority of LGN neurons in our dataset (all but four) had spike waveforms matching regular spiking neurons (SI Appendix, Fig. S2D) based on peak-to-trough time and amplitude, suggesting that we recorded mainly from LGN relay neurons (8). We observed a low incidence of thalamic bursts (5) among recorded LGN neurons (<1% of spikes).…”

Section: Influence Of Cg Feedback On Lgn Neuronal Receptive Field Sizmentioning

confidence: 90%

“…Some have proposed that CG feedback modulates the gain (7)(8)(9)(10)(11)(12)(13)(14) and/or the spatiotemporal properties of LGN neurons (15)(16)(17). Others have proposed that corticothalamic feedback controls whether thalamic neurons are in a state of net excitation or inhibition (8,12), depending upon oscillatory activity in corticothalamic networks (18). Our goal was to conduct a causal and comprehensive examination of CG function using a combination of virus-mediated gene delivery and optogenetic strategies to selectively and reversibly manipulate the activity of CG neurons in vivo.…”

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confidence: 99%

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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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Section: Discussionsupporting

confidence: 90%

Section: Discussionmentioning

confidence: 99%

Section: Influence Of Cg Feedback On Lgn Neuronal Receptive Field Sizmentioning

confidence: 90%

mentioning

confidence: 99%

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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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“…Examples of such modulation by class 2 inputs include control of tonic versus burst firing mode of thalamic relay cells (29,30) and affecting the EPSP amplitudes of class 1 inputs (1,(31)(32)(33)(34)(35). Also consistent with this modulatory role for class 2 inputs are in vivo studies showing that optogenetic manipulation of the class 2 corticogeniculate pathway from cortical layer 6 shows that gain control is one of its main roles (36,37). The effect of class 2 inputs, whether inhibition or excitation, did not alter the orientation tuning of the postsynaptic cells in these studies.…”

Section: Discussionmentioning

confidence: 82%

Synaptic properties of the lemniscal and paralemniscal pathways to the mouse somatosensory thalamus

Petrof

Viaene

et al. 2017

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

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Somatosensory information is thought to arrive in thalamus through two glutamatergic routes called the lemniscal and paralemniscal pathways via the ventral posterior medial (VPm) and posterior medial (POm) nuclei. Here we challenge the view that these pathways functionally represent parallel information routes. Using electrical stimulation and an optogenetic approach in brain slices from the mouse, we investigated the synaptic properties of the lemniscal and paralemniscal input to VPm and POm. Stimulation of the lemniscal pathway produced class 1, or "driver," responses in VPm relay cells, which is consistent with this being an informationbearing channel. However, stimulation of the paralemniscal pathway produced two distinct types of responses in POm relay cells: class 1 (driver) responses in 29% of the cells, and class 2, or "modulator," responses in the rest. Our data suggest that, unlike the lemniscal pathway, the paralemniscal one is not homogenous and that it is primarily modulatory. This finding requires major rethinking regarding the routes of somatosensory information to cortex and suggests that the paralemniscal route is chiefly involved in modulatory functions rather than simply being an information route parallel to the lemniscal channel.driver | modulator | glutamatergic | ventral posterior medial nucleus | posterior medial nucleus B efore reaching the cortex, all sensory information except olfaction is relayed by the thalamus. For somatosensory information, there appear to be two potential routes of such information flow, which have been termed "lemniscal" and "paralemniscal." Regarding the trigeminal components of these, the lemniscal route is represented by the pathway from the principal and spinal nuclei of the Vth nerve (PrV and SpV, respectively) via the medial lemniscus (ML) through VPm, whereas the paralemniscal route is represented by the pathway originating mostly from SpV through POm. However, exactly how these circuits function depends critically on the nature of the underlying synapses. These inputs to thalamus and from thalamus to cortex are glutamatergic, meaning that they use glutamate as a neurotransmitter. Recent work has made it clear that glutamatergic inputs in thalamus and cortex are heterogeneous and can be divided into at least two types, known as class 1 (or driver) and class 2 (or modulator) (1-3). It has been suggested that the class 1 inputs carry the main information between neuronal regions and that the class 2 inputs provide a modulatory role, mainly affecting how class 1 inputs are processed (reviewed in refs. 4-6; see also Discussion). Thus, identifying which type of glutamatergic synapses are involved in the lemniscal and paralemniscal pathways could help clarify whether they represent parallel information routes or whether some other functional explanation is more plausible.To this end, we used slice preparations in which we could use a combination of electrical stimulation and optogenetics to activate lemniscal or paralemniscal inputs to patched cells in VPm and P...

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Cre‐expressing neurons in visual cortex of Ntsr1‐Cre GN220 mice are corticothalamic and are depolarized by acetylcholine

Sundberg

Lindström

Sanchez

et al. 2017

J of Comparative Neurology

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The Ntsr1-Cre GN220 mouse expresses Cre-recombinase in corticothalamic (CT) neurons in neocortical layer 6. It is not known if the other major types of pyramidal neurons in this layer also express this enzyme. By electrophysiological recordings in slices and histological analysis of the uptake of retrogradely transported beads we show that Cre-positive neurons are CT and not corticocortical or corticoclaustral types. Furthermore, we show that Ntsr1-Cre-positive cells are immuno-positive for the nuclear transcription factor Forkhead box protein P2 (FoxP2). We conclude that Cre-expression is limited to a specific type of pyramidal neuron: CT. However, it appears as not all CT neurons are Cre-expressing; there are indications that the penetrance of the gene is about 90%. We demonstrate the utility of assigning a specific identity to individual neurons by determining that the CT neurons are potently modulated by acetylcholine acting on both nicotinic and muscarinic acetylcholine receptors. These results corroborate the suggested function of these neurons in regulating the gain of thalamocortical transfer of sensory information depending on attentional demand and state of arousal.

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Complex Effects on In Vivo Visual Responses by Specific Projections from Mouse Cortical Layer 6 to Dorsal Lateral Geniculate Nucleus

Cited by 87 publications

References 75 publications

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

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

Synaptic properties of the lemniscal and paralemniscal pathways to the mouse somatosensory thalamus

Cre‐expressing neurons in visual cortex of Ntsr1‐Cre GN220 mice are corticothalamic and are depolarized by acetylcholine

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