A Top-Down Cortical Circuit for Accurate Sensory Perception

Manita, Satoshi; Suzuki, Takayuki; Homma, Chihiro; Matsumoto, Takashi; Odagawa, Maya; Yamada, Kazuyuki; Ota, Ken‐ichiro; Matsubara, Chie; Inutsuka, Ayumu; Sato, Masaaki; Ohkura, Masamichi; Yamanaka, Akihiro; Yanagawa, Yuchio; Nakai, Junichi; Hayashi, Yasunori; Larkum, Matthew E.; Murayama, Miyuki

doi:10.1016/j.neuron.2015.05.006

Cited by 319 publications

(364 citation statements)

References 56 publications

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“…Studies have used visually stimuli in the upper visual field which require approach behaviors (Harvey, Collman, Dombeck, & Tank, 2009; Scott, Constantinople, Erlich, Tank, & Brody, 2015). Conversely, other studies have employed stimuli which occur in the lower visual field, and which require avoidance behaviors (Ho et al, 2015; Manita et al, 2015). However, in these studies the stimuli have usually been presented a large number of times and have been associated with either a positive or negative outcome.…”

Section: Discussionmentioning

confidence: 99%

Segregated fronto‐cortical and midbrain connections in the mouse and their relation to approach and avoidance orienting behaviors

Savage

McQuade

Thiele

2017

J of Comparative Neurology

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The orchestration of orienting behaviors requires the interaction of many cortical and subcortical areas, for example the superior colliculus (SC), as well as prefrontal areas responsible for top–down control. Orienting involves different behaviors, such as approach and avoidance. In the rat, these behaviors are at least partially mapped onto different SC subdomains, the lateral (SCl) and medial (SCm), respectively. To delineate the circuitry involved in the two types of orienting behavior in mice, we injected retrograde tracer into the intermediate and deep layers of the SCm and SCl, and thereby determined the main input structures to these subdomains. Overall the SCm receives larger numbers of afferents compared to the SCl. The prefrontal cingulate area (Cg), visual, oculomotor, and auditory areas provide strong input to the SCm, while prefrontal motor area 2 (M2), and somatosensory areas provide strong input to the SCl. The prefrontal areas Cg and M2 in turn connect to different cortical and subcortical areas, as determined by anterograde tract tracing. Even though connectivity pattern often overlap, our labeling approaches identified segregated neural circuits involving SCm, Cg, secondary visual cortices, auditory areas, and the dysgranular retrospenial cortex likely to be involved in avoidance behaviors. Conversely, SCl, M2, somatosensory cortex, and the granular retrospenial cortex comprise a network likely involved in approach/appetitive behaviors.

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Section: Discussionmentioning

confidence: 99%

Segregated fronto‐cortical and midbrain connections in the mouse and their relation to approach and avoidance orienting behaviors

Savage

McQuade

Thiele

2017

J of Comparative Neurology

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“…[3][4][5][6][9][10][11][12][13][14][15][16][17][18][19][20] The deflection of a single whisker initially evokes a highly localized sensory response, mapping onto the appropriate barrel column in the primary somatosensory cortex (S1). 3,5,11 However, the sensory response typically spreads over the next milliseconds, invading neighboring cortical barrel columns, depending upon stimulus strength, 3,6 developmental age, 21,22 ongoing spontaneous cortical activity, 4 and ongoing whisker-related behavior.…”

Section: Introductionmentioning

confidence: 99%

Voltage-sensitive dye imaging of mouse neocortex during a whisker detection task

et al. 2016

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Abstract. Sensorimotor processing occurs in a highly distributed manner in the mammalian neocortex. The spatiotemporal dynamics of electrical activity in the dorsal mouse neocortex can be imaged using voltagesensitive dyes (VSDs) with near-millisecond temporal resolution and ∼100-μm spatial resolution. Here, we trained mice to lick a water reward spout after a 1-ms deflection of the C2 whisker, and we imaged cortical dynamics during task execution with VSD RH1691. Responses to whisker deflection were highly dynamic and spatially highly distributed, exhibiting high variability from trial to trial in amplitude and spatiotemporal dynamics. We differentiated trials based on licking and whisking behavior. Hit trials, in which the mouse licked after the whisker stimulus, were accompanied by overall greater depolarization compared to miss trials, with the strongest hit versus miss differences being found in frontal cortex. Prestimulus whisking decreased behavioral performance by increasing the fraction of miss trials, and these miss trials had attenuated cortical sensorimotor responses. Our data suggest that the spatiotemporal dynamics of depolarization in mouse sensorimotor cortex evoked by a single brief whisker deflection are subject to important behavioral modulation during the execution of a simple, learned, goal-directed sensorimotor transformation.

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“…[1][2][3][4][5] Sensory information is often actively acquired through self-generated movements of sensors to specific locations to gather selected sensory input. For example, we make eye and head movements to foveate regions of interest in the world around us, and we reach out to touch objects to feel their shape and texture.…”

Section: Introductionmentioning

confidence: 99%

Parallel pathways from whisker and visual sensory cortices to distinct frontal regions of mouse neocortex

et al. 2016

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Abstract. The spatial organization of mouse frontal cortex is poorly understood. Here, we used voltage-sensitive dye to image electrical activity in the dorsal cortex of awake head-restrained mice. Whisker-deflection evoked the earliest sensory response in a localized region of primary somatosensory cortex and visual stimulation evoked the earliest responses in a localized region of primary visual cortex. Over the next milliseconds, the initial sensory response spread within the respective primary sensory cortex and into the surrounding higher order sensory cortices. In addition, secondary hotspots in the frontal cortex were evoked by whisker and visual stimulation, with the frontal hotspot for whisker deflection being more anterior and lateral compared to the frontal hotspot evoked by visual stimulation. Investigating axonal projections, we found that the somatosensory whisker cortex and the visual cortex directly innervated frontal cortex, with visual cortex axons innervating a region medial and posterior to the innervation from somatosensory cortex, consistent with the location of sensory responses in frontal cortex. In turn, the axonal outputs of these two frontal cortical areas innervate distinct regions of striatum, superior colliculus, and brainstem. Sensory input, therefore, appears to map onto modality-specific regions of frontal cortex, perhaps participating in distinct sensorimotor transformations, and directing distinct motor outputs.

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A Top-Down Cortical Circuit for Accurate Sensory Perception

Cited by 319 publications

References 56 publications

Segregated fronto‐cortical and midbrain connections in the mouse and their relation to approach and avoidance orienting behaviors

Segregated fronto‐cortical and midbrain connections in the mouse and their relation to approach and avoidance orienting behaviors

Voltage-sensitive dye imaging of mouse neocortex during a whisker detection task

Parallel pathways from whisker and visual sensory cortices to distinct frontal regions of mouse neocortex

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