Dissecting the circuit for blindsight to reveal the critical role of pulvinar and superior colliculus

Kinoshita, Masaharu; Katō, Risō; Isa, Kaoru; Kobayashi, Kenta; Kobayashi, Kazuto; Onoe, Hirotaka; Isa, Tadashi

doi:10.1038/s41467-018-08058-0

Cited by 98 publications

(93 citation statements)

References 53 publications

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“…These findings suggest that the SC and pulvinar constitute the subcortical visual pathway for innate face detection. Neuroanatomical, non-invasive imaging and neurophysiological studies reported existence of this subcortical pathway consisting of the SC, pulvinar, and amygdala in animals and humans (Linke et al, 1999;Day-Brown et al, 2010;Tamietto et al, 2012;Garvert et al, 2014;Rafal et al, 2015;Elorette et al, 2018;Kinoshita et al, 2019). These findings suggest that the SC is a first node in the subcortical pathway, where retinal inputs are integrated into facial information.…”

Section: Resultsmentioning

confidence: 84%

A Prototypical Template for Rapid Face Detection Is Embedded in the Monkey Superior Colliculus

Nishimaru

et al. 2020

Front. Syst. Neurosci.

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Human babies respond preferentially to faces or face-like images. It has been proposed that an innate and rapid face detection system is present at birth before the cortical visual pathway is developed in many species, including primates. However, in primates, the visual area responsible for this process is yet to be unraveled. We hypothesized that the superior colliculus (SC) that receives direct and indirect retinal visual inputs may serve as an innate rapid face-detection system in primates. To test this hypothesis, we examined the responsiveness of monkey SC neurons to first-order information of faces required for face detection (basic spatial layout of facial features including eyes, nose, and mouth), by analyzing neuronal responses to line drawing images of: (1) face-like patterns with contours and properly placed facial features; (2) non-face patterns including face contours only; and (3) nonface random patterns with contours and randomly placed face features. Here, we show that SC neurons respond stronger and faster to upright and inverted face-like patterns compared to the responses to nonface patterns, regardless of contrast polarity and contour shapes. Furthermore, SC neurons with central receptive fields (RFs) were more selective to face-like patterns. In addition, the population activity of SC neurons with central RFs can discriminate face-like patterns from nonface patterns as early as 50 ms after the stimulus onset. Our results provide strong neurophysiological evidence for the involvement of the primate SC in face detection and suggest the existence of a broadly tuned template for face detection in the subcortical visual pathway.

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Section: Resultsmentioning

confidence: 84%

A Prototypical Template for Rapid Face Detection Is Embedded in the Monkey Superior Colliculus

Nishimaru

et al. 2020

Front. Syst. Neurosci.

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“…The ventral stream extends to the temporal cortex, and contains a group of neurons responding to a specific category of visual objects (36,37). Visual information mediated via the SC projects to the higher visual cortices of the dorsal stream (11)(12)(13)(14). The excellent perception of moving grating direction in the impaired right visual field (Figure 3D) may be explained as a function of this projection.…”

Section: Discussionmentioning

confidence: 98%

“…When the V1 is damaged, the visual fields opposite to the damaged V1 are impaired, a condition known as cortical blindness (3)(4)(5). However, patients with cortical blindness have unconscious visual functions called blindsight (6,7), possibly through visual information obtained from the superior colliculus (SC), which in turn projects to the amygdala (8)(9)(10) and the higher visual cortex (11)(12)(13)(14). Fresh cortical blindness sometimes spontaneously recovers (15), and the recovery is facilitated by early rehabilitation (16,17).…”

Section: Introductionmentioning

confidence: 99%

Rapid Recovery From Cortical Blindness Caused by an Old Cerebral Infarction

Shibuki

Wakui²,

Fujimura³

et al. 2020

Front. Neurol.

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When the primary visual cortex (V1) is damaged, cortical blindness results. However, visual information obtained from the superior colliculus (SC) or direct thalamic afferents to higher visual cortices produces unconscious visual functions called blindsight. Alarming visual stimuli suggesting the approach of a predator are known to trigger escape behaviors via visual information mediated by the SC and amygdala in small animals, and salient and dynamic visual stimuli also produce some conscious visual experience even in patients with blindsight. Fresh cortical blindness sometimes recovers spontaneously in patients with fresh cerebral damages, and recovery can be accelerated by early rehabilitation. However, the mechanisms underlying recovery are not well-known. We analyzed a patient with cortical blindness caused by an old cerebral infarction. After repeated presentation of alarming visual stimuli, the ability to detect visual stimuli in the impaired visual field showed behavioral short-term improvement (STI) within a few minutes. Repeated behavioral STI induction was followed by behavioral long-term improvement (LTI) lasting more than several days. After behavioral LTI, the patient partially recovered the ability to read letters presented in the impaired visual field. The behavioral STI experiment, which can be performed within 10 min, may serve as a clinical screening test for anticipating recovery from cortical blindness.

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“…In rabbits, however, the inactivation of SC led to a strong attenuation of responses in lateral posterior nucleus (which is a part of the LP-pulvinar complex in non-primate species: mice, rats, rabbits, cats, and tree shrews) (Casanova and Molotchnikoff, 1990). Furthermore, selective microstimulation of the superficial layers of the SC in macaques has been shown to elicit (monosynaptic) responses in the ventral pulvinar (Kinoshita et al, 2019), in agreement with earlier work that identified the projection from SC to area MT via ventral pulvinar (Berman and Wurtz, 2011).…”

Section: Possible Sources Of Eye Position Signals In Dorsal Pulvinarmentioning

confidence: 99%

“…Extrapolating from these ventral pulvinar studies to the dorsal pulvinar, the potential influence of SC inputs to dPul (Wurtz et al, 2005) might be outweighed by more extensive cortical driving inputs (Rovó et al, 2012;Bickford, 2016). To fully elucidate complex cortico-pulvinar-cortical loops and subcortical inputs to pulvinar, it would be crucial to manipulate the specific projections from and to the pulvinar, using pathway-selective techniques, such as optogenetics and/or viral vectors (Schmitt et al, 2017;Kinoshita et al, 2019).…”

Section: Possible Sources Of Eye Position Signals In Dorsal Pulvinarmentioning

confidence: 99%

Eye position signals in the dorsal pulvinar during fixation and goal-directed saccades

Schneider

Dominguez-Vargas

Gibson

et al. 2019

Preprint

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Most sensorimotor cortical areas contain eye position information thought to ensure perceptual stability across saccades and underlie spatial transformations supporting goal-directed actions. One pathway by which eye position signals could be relayed to and across cortical areas is via the dorsal pulvinar.Several studies demonstrated saccade-related activity in the dorsal pulvinar and we have recently shown that many neurons exhibit post-saccadic spatial preference long after the saccade execution. In addition, dorsal pulvinar lesions lead to gaze-holding deficits expressed as nystagmus or ipsilesional gaze bias, prompting us to investigate the effects of eye position. We tested three starting eye positions (-15°/0°/15°) in monkeys performing a visually-cued memory saccade task. We found two main types of gaze dependence. First, ~50% of neurons showed an effect of static gaze direction during initial and post-saccadic fixation. Eccentric gaze preference was more common than straight ahead. Some of these neurons were not visually-responsive and might be primarily signaling the position of the eyes in the orbit, or coding foveal targets in a head/body/world-centered reference frame. Second, many neurons showed a combination of eye-centered and gaze-dependent modulation of visual, memory and saccadic responses to a peripheral target. A small subset showed effects consistent with eye position-dependent gain modulation. Analysis of reference frames across task epochs from visual cue to post-saccadic target fixation indicated a transition from predominantly eye-centered encoding to representation of final gaze or foveated locations in non-retinocentric coordinates. These results show that dorsal pulvinar neurons carry information about eye position, which could contribute to steady gaze during postural changes and to reference frame transformations for visually-guided eye and limb movements.

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Dissecting the circuit for blindsight to reveal the critical role of pulvinar and superior colliculus

Cited by 98 publications

References 53 publications

A Prototypical Template for Rapid Face Detection Is Embedded in the Monkey Superior Colliculus

A Prototypical Template for Rapid Face Detection Is Embedded in the Monkey Superior Colliculus

Rapid Recovery From Cortical Blindness Caused by an Old Cerebral Infarction

Eye position signals in the dorsal pulvinar during fixation and goal-directed saccades

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