Higher-Order Thalamic Circuits Channel Parallel Streams of Visual Information in Mice

Bennett, Corbett; Gale, Samuel D.; Garrett, Marina; Newton, Melissa L.; Callaway, Edward M.; Murphy, Gabe J.; Olsen, Shawn R.

doi:10.1016/j.neuron.2019.02.010

Cited by 135 publications

(162 citation statements)

References 61 publications

(85 reference statements)

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“…This effect involves the circuit formed by the tectum and the isthmic nuclei, which implements a winner-take-all mechanism for stimulus competition (Marín et al, 2007;Marín et al, 2012;Mysore & Knudsen, 2013;Wang, Luksch, Brecha, & Karten, 2006 Worthington, 1990;May, 2006). Specifically, the tectofugalrecipient cortex (area TP or POR), densely projects to the superficial layers of the SC (Bennett et al, 2019;Wang & Burkhalter, 2013) where, as we here suggest for the AI, they may contact the TGC neurons. In the case of the mouse V1, descending axons do make direct synaptic contacts upon TGC dendrites, potentiating the visual responses transmitted by the TGCs to the mouse caudal pulvinar (Fredes, Vega-Zuniga, Karten, & Mpodozis, 2012;Masterson, Zhou, Akers, Dang, & Bickford, 2018).…”

Section: Functional Considerationsmentioning

confidence: 64%

Parallel organization of the avian sensorimotor arcopallium: Tectofugal visual pathway in the pigeon (Columba livia)

Fernández

Morales

Durán

et al. 2019

J of Comparative Neurology

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The sensory–motor division of the avian arcopallium receives parallel inputs from primary and high‐order pallial areas of sensory and vocal control pathways, and sends a prominent descending projection to ascending and premotor, subpallial stages of these pathways. While this organization is well established for the auditory and trigeminal systems, the arcopallial subdivision related to the tectofugal visual system and its descending projection to the optic tectum (TeO) has been less investigated. In this study, we charted the arcopallial area displaying tectofugal visual responses and by injecting neural tracers, we traced its connectional anatomy. We found visual motion‐sensitive responses in a central region of the dorsal (AD) and intermediate (AI) arcopallium, in between previously described auditory and trigeminal zones. Blocking the ascending tectofugal sensory output, canceled these visual responses in the arcopallium, verifying their tectofugal origin. Injecting PHA‐L into the visual, but not into the auditory AI, revealed a massive projection to tectal layer 13 and other tectal related areas, sparing auditory, and trigeminal ones. Conversely, CTB injections restricted to TeO retrogradely labeled neurons confined to the visual AI. These results show that the AI zone receiving tectofugal inputs sends top‐down modulations specifically directed to tectal targets, just like the auditory and trigeminal AI zones project back to their respective subpallial sensory and premotor areas, as found by previous studies. Therefore, the arcopallium seems to be organized in a parallel fashion, such that in spite of expected cross‐modal integration, the different sensory–motor loops run through separate subdivisions of this structure.

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Section: Functional Considerationsmentioning

confidence: 64%

Parallel organization of the avian sensorimotor arcopallium: Tectofugal visual pathway in the pigeon (Columba livia)

Fernández

Morales

Durán

et al. 2019

J of Comparative Neurology

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“…We next sought to determine how the visual function of each cell type relates to its role, or lack thereof, in prey capture. In a previous study, the visual stimulus response properties of both the WF and NF cells were characterized in anesthetized mouse (Gale and Murphy, 2018) , whereas there has only been limited characterization of the WF and PV population response properties in the awake mouse (Bennett et al, 2019;Shang et al, 2015Shang et al, , 2018 . In order to provide a systematic comparison across all three cell types we quantified a range of visual response properties in awake mice by performing acute extracellular single-unit recordings with silicon multisite electrodes while applying the optogenetic approach described above to identify Cre-positive neurons during recording ( Figure 4A ).…”

Section: Visual Responses Of Identified Cell Types Are Consistent Witmentioning

confidence: 99%

“…Previous studies of LP have demonstrated that this higher-order thalamic nucleus encodes visual stimulus movement over a large region of the visual field, and provides information to cortex about when the movement of stimuli in the visual scene are not predicted by the animal's own actions (Masterson et al, 2009;Roth et al, 2016) . In addition, recent studies revealed that information carried by WF cells to LP is then relayed to specific areas of extrastriate visual cortex by circuitry that operates in parallel to the classical retino-geniculate pathway to cortex (Beltramo and Scanziani, 2019;Bennett et al, 2019) . Therefore, our findings support the idea that WF cells in sSC provide rapid initial detection of stimulus presence and can convey this information to extrastriate cortex via higher-order thalamus.…”

Section: Specific Cell Types and Circuits Within The Ssc Contribute Tmentioning

confidence: 99%

Defined cell types in superior colliculus make distinct contributions to prey capture behavior in the mouse

Hoy

Bishop

Niell

2019

Preprint

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The superior colliculus (SC) mediates rapid orienting to visual stimuli across species. To determine the specific circuits within the SC that drive orienting and approach behavior toward appetitive stimuli, we explored the role of three genetically defined cell types in mediating prey capture in mice. Chemogenetic inactivation of two classically defined cell types, the wide-field (WF) and narrow-field (NF) vertical neurons, revealed that they are involved in distinct aspects of prey capture. WF neurons were required for rapid prey detection and distant approach initiation, whereas NF neurons were required for continuous and accurate orienting during pursuit. In contrast, prey capture did not require parvalbumin-expressing (PV) neurons that have previously been implicated in fear responses. The visual coding of WF and NF cells in the awake mouse and their projection targets were consistent with their roles in prey detection versus pursuit. Thus, our studies link specific neural circuit connectivity and function with stimulus detection and orienting behavior, providing insight into visuomotor and attentional mechanisms mediated by superior colliculus. Highlights• This study provides the first demonstration of the role of specific cell populations in the superior colliculus in orienting and approach behavior.• A genetically targeted population of wide-field vertical neurons in the superior colliculus is required for rapid prey detection and initiation of long-distance approaches.• A genetically targeted population of narrow-field vertical neurons is required for approach initiation, accurate targeting, and approach continuity.• Visual response properties and projection targets of these cells are consistent with their role in prey capture, linking neural circuit connectivity and function with behavior.

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“…This is especially true for rodent models where little has been reported on receptive field properties of mouse pulvinar (a.k.a. lateral posterior nucleus; LP; Roth et al, 2015;Ahmadlou et al, 2018;Bennett et al, 2019), and even less so in rats (Montero et al, 1968).…”

Section: Introductionmentioning

confidence: 99%

Visual response characteristics in lateral and medial subdivisions of the rat pulvinar

Foik¹,

Scholl²,

Lean³

et al. 2020

Preprint

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The pulvinar is a higher-order thalamic relay and a central component of the extrageniculate visual pathway, with input from the superior colliculus and visual cortex and output to all of visual cortex. Rodent pulvinar, more commonly called the lateral posterior nucleus (LP), consists of three highly-conserved subdivisions, and offers the advantage of simplicity in its study compared to more subdivided primate pulvinar. Little is known about receptive field properties of LP, let alone whether functional differences exist between different LP subdivisions, making it difficult to understand what visual information is relayed and what kinds of computations the pulvinar might support. Here, we characterized single-cell response properties in two V1 recipient subdivisions of rat pulvinar, the rostromedial (LPrm) and lateral (LPl), and found that a fourth of the cells were selective for orientation, compared to half in V1, and that LP tuning widths were significantly broader. Response latencies were also significantly longer and preferred size more than three times larger on average than in V1; the latter suggesting pulvinar as a source of spatial context to V1. Between subdivisons, LPl cells preferred higher temporal frequencies, whereas LPrm showed a greater degree of direction selectivity and pattern motion detection. Taken together with known differences in connectivity patterns, these results suggest two separate visual feature processing channels in the pulvinar, one in LPl related to higher speed processing which likely derives from superior colliculus input, and the other in LPrm for motion processing derived through input from visual cortex. Significance StatementThe pulvinar has a perplexing role in visual cognition as no clear link has been found between the functional properties of its neurons and behavioral deficits that arise when it is damaged. The pulvinar, called the lateral posterior nucleus (LP) in rats, is a higher order thalamic relay with input from the superior colliculus and visual cortex and output to all of visual cortex. By characterizing single-cell response properties in anatomically distinct subdivisions we found two separate visual feature processing channels in the pulvinar, one in lateral LP related to higher speed processing which likely derives from superior colliculus input, and the other in rostromedial LP for motion processing derived through input from visual cortex.

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Higher-Order Thalamic Circuits Channel Parallel Streams of Visual Information in Mice

Cited by 135 publications

References 61 publications

Parallel organization of the avian sensorimotor arcopallium: Tectofugal visual pathway in the pigeon (Columba livia)

Parallel organization of the avian sensorimotor arcopallium: Tectofugal visual pathway in the pigeon (Columba livia)

Defined cell types in superior colliculus make distinct contributions to prey capture behavior in the mouse

Visual response characteristics in lateral and medial subdivisions of the rat pulvinar

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