A Corticothalamic Switch: Controlling the Thalamus with Dynamic Synapses

Crandall, Shane R.; Cruikshank, Scott J.; Connors, Barry W.

doi:10.1016/j.neuron.2015.03.040

Cited by 278 publications

(351 citation statements)

References 88 publications

(140 reference statements)

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“…With this in mind, feedback could certainly contribute to later phases of suppression. If so, then the influence of feedback is likely to be complex because feedback axons provide direct excitatory input onto LGN relay neurons and input onto local interneurons and GABAergic neurons in the reticular nucleus that in turn project onto relay neurons (Jones, 2006;Ulrich et al, 2007;Sherman and Guillery, 2009;Cox, 2014). Moreover, synaptic communication at all of these synapses, including retinogeniculate synapses, is dynamic and dependent on the firing rate of presynaptic neurons (Crandall et al, 2015;Usrey, 2015a,2015b).…”

Section: Discussionmentioning

confidence: 99%

Retinal and Nonretinal Contributions to Extraclassical Surround Suppression in the Lateral Geniculate Nucleus

2016

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Section: Discussionmentioning

confidence: 99%

Retinal and Nonretinal Contributions to Extraclassical Surround Suppression in the Lateral Geniculate Nucleus

2016

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“…Furthermore, current electrode recording technology limits both the recording site density and spatial coverage. Therefore, thalamo-cortical circuits have been characterized only between thalamic nuclei and directly innervated cortical regions (34,35). This characterization yields a limited understanding into widespread neural interactions beyond thalamo-cortico-thalamic networks.…”

Section: Significancementioning

confidence: 99%

“…We determined the spatiotemporal response properties of long-range excitatory thalamic projections to cortical and subcortical regions. We overcame the limitations of electrical stimulation nonspecificity (34,35) and electrode recording spatial coverage by using a multimodal approach. We used optogenetic functional MRI (fMRI) in combination with electrophysiological recordings to interrogate the vibrissae (whisker) somatosensory thalamo-cortical system.…”

Section: Significancementioning

confidence: 99%

Long-range projections coordinate distributed brain-wide neural activity with a specific spatiotemporal profile

Leong

Chan

Gao

et al. 2016

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

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One challenge in contemporary neuroscience is to achieve an integrated understanding of the large-scale brain-wide interactions, particularly the spatiotemporal patterns of neural activity that give rise to functions and behavior. At present, little is known about the spatiotemporal properties of long-range neuronal networks. We examined brain-wide neural activity patterns elicited by stimulating ventral posteromedial (VPM) thalamo-cortical excitatory neurons through combined optogenetic stimulation and functional MRI (fMRI). We detected robust optogenetically evoked fMRI activation bilaterally in primary visual, somatosensory, and auditory cortices at low (1 Hz) but not high frequencies (5-40 Hz). Subsequent electrophysiological recordings indicated interactions over long temporal windows across thalamo-cortical, cortico-cortical, and interhemispheric callosal projections at low frequencies. We further observed enhanced visually evoked fMRI activation during and after VPM stimulation in the superior colliculus, indicating that visual processing was subcortically modulated by low-frequency activity originating from VPM. Stimulating posteromedial complex thalamo-cortical excitatory neurons also evoked brain-wide bloodoxygenation-level-dependent activation, although with a distinct spatiotemporal profile. Our results directly demonstrate that lowfrequency activity governs large-scale, brain-wide connectivity and interactions through long-range excitatory projections to coordinate the functional integration of remote brain regions. This low-frequency phenomenon contributes to the neural basis of long-range functional connectivity as measured by resting-state fMRI.fMRI | optogenetic | brain connectivity | low frequency | thalamus T he brain is a highly complex, interconnected structure with parallel and hierarchical networks distributed within and between neural systems (1, 2). This integrative architecture dictates the underlying principles of how brain-wide neural connectivity supports and organizes sensory, behavioral, and cognitive processes (3). Recent advances in structural (2, 4) and functional connectivity (5-12) mapping, as well as neural circuit modulatory tools, such as optogenetics (13, 14), permit detailed, high-resolution neural examinations at unprecedented scales. In particular, functional connectivity mapping using resting-state functional MRI (rsfMRI) produces noninvasive visualization of slow and spontaneous hemodynamic fluctuations in humans (5-9) and animals (10-12). Coherent low-frequency (<1 Hz) fluctuations across functionally coupled, large-scale networks is an intriguing property, although the exact underlying neural bases and functional significance remain unclear. Previous studies integrating large-scale electrical recordings, voltage-sensitive dye (VSD), and Ca 2+ -imaging techniques (15-18) support the hypothesis that slow, oscillating neural activity constrains and elicits these hemodynamic fluctuations. Furthermore, low-frequency activity can temporally synchronize remote brain region...

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“…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.…”

mentioning

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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A Corticothalamic Switch: Controlling the Thalamus with Dynamic Synapses

Cited by 278 publications

References 88 publications

Retinal and Nonretinal Contributions to Extraclassical Surround Suppression in the Lateral Geniculate Nucleus

Retinal and Nonretinal Contributions to Extraclassical Surround Suppression in the Lateral Geniculate Nucleus

Long-range projections coordinate distributed brain-wide neural activity with a specific spatiotemporal profile

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

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