Functional Imaging of the Human Lateral Geniculate Nucleus and Pulvinar

142

Patients with striate cortex damage and clinical blindness retain the ability to process certain visual properties of stimuli that they are not aware of seeing. Here we investigated the neural correlates of residual visual perception for dynamic whole-body emotional actions. Angry and neutral emotional whole-body actions were presented in the intact and blind visual hemifield of a cortically blind patient with unilateral destruction of striate cortex. Comparisons of angry vs. neutral actions performed separately in the blind and intact visual hemifield showed in both cases increased activation in primary somatosensory, motor, and premotor cortices. Activations selective for intact hemifield presentation of angry compared with neutral actions were located subcortically in the right lateral geniculate nucleus and cortically in the superior temporal sulcus, prefrontal cortex, precuneus, and intraparietal sulcus. Activations specific for blind hemifield presentation of angry compared with neutral actions were found in the bilateral superior colliculus, pulvinar nucleus of the thalamus, amygdala, and right fusiform gyrus. Direct comparison of emotional modulation in the blind vs. intact visual hemifield revealed selective activity in the right superior colliculus and bilateral pulvinar for angry expressions, thereby showing a selective involvement of these subcortical structures in nonconscious visual emotion perception.blindsight | body expressions | consciousness T he visual system encompasses a number of parallel visual pathways (1) of which the primary geniculostriate system processes a wide range of stimulus attributes. Other extrageniculostriate visual routes likely have a much more narrowly specified function, as indicated by their sensitivity to a limited range of spatial frequencies (2), spectral components (3), or motion parameters (4). However, we do not yet have a clear understanding of how these different extrageniculostriate pathways and the visual attributes they process match. Some visual attributes can also be processed by both the geniculostriate pathway and a more specialized extrageniculostriate one.One important example is movement perception. As originally discovered by Kohler and Held (5), movement perception elicits significant qualitative and quantitative differences at the neural as well as at behavioral level compared with static stimuli in the intact brain. These differences likely reflect the high evolutionary value of movement perception and may be especially important for understanding residual visual abilities in the case of striate cortex (V1) damage. In fact, after V1 damage, cortically blind patients retain a limited visual ability for movement discrimination (4, 6-9), akin to what has been previously observed in animals with V1 destruction (10,11). This spared ability to process simple movement is probably based on the extrageniculostriate connections that motion-sensitive human middle temporal/V5 complex (hMT/V5) has with subcortical structures like the lateral geniculate nucleus ...

Section: Discussionsupporting

confidence: 81%

Cortico-subcortical visual, somatosensory, and motor activations for perceiving dynamic whole-body emotional expressions with and without striate cortex (V1)

Stock

Tamietto

Sorger

et al. 2011

142

“…To test the latter hypothesis, we examined activity in the superior colliculus and the pulvinar, identified anatomically according to criteria described in ref. 36. We compared activity during between-hemisphere and within-hemisphere attention conditions.…”

Section: Resultsmentioning

confidence: 99%

Attentional integration between anatomically distinct stimulus representations in early visual cortex

Haynes

Tregellas

Rees

2005

Vision often requires attending to, and integrating information from, distant parts of the visual field. However, the neural basis for such long-range integration is not clearly understood. Here, we demonstrate a specific neural signature of attentional integration between stimuli in different parts of the visual field. Using functional MRI, we found that a task requiring the integration of information between two attended but spatially separated stimuli actively modulated the degree of functional integration (in terms of effective connectivity) between their retinotopic representations in visual cortical areas V1, V2, and V4. Spatial attention enhanced long-distance coupling between distinct neuronal populations that represented the attended visual stimuli, even at the earliest stages of cortical processing. In contrast, unattended stimulus representations were decoupled both from attended representations and particularly strongly from each other. Furthermore, enhanced functional integration between cortical representations was associated with enhanced behavioral performance. Attention may thus serve to ''bind'' together cortical loci at multiple levels of the visual hierarchy that are commonly involved in processing attended stimuli, promoting integration between otherwise functionally isolated cortical loci.attention ͉ connectivity ͉ dynamic causal modeling ͉ functional MRI ͉ vision V ision often requires integration of information from distant locations within the visual field, but how this integration is achieved is currently not well understood. Receptive field properties of visually responsive cortical neurons suggest that, in early visual cortex, information is analyzed largely (although not entirely) locally, with further processing stages combining information from successively larger portions of the visual field (1-3). In such an anatomically convergent pathway, integration of information from distant positions within the visual field might occur entirely in higher visual areas, which have large receptive fields and corresponding possibilities for interactions between distant regions (1-3). However, response properties of cells in early visual areas are also modulated by remote stimuli presented far beyond their classical receptive fields (4-7). Thus, an alternate possibility is that a neural signature reflecting integration of distant information might already be identifiable in very early visual cortex. Possible anatomical substrates for such interactions include long-range horizontal projections within visual areas (8-10), the dense and reciprocal connections between visual areas (7,(11)(12)(13)(14)(15), and subcortical pathways via pulvinar and superior colliculus (16).Here, we used functional MRI (fMRI) in humans to test whether task-dependent interactions between stimulus representations in distant parts of the visual field could be seen in early retinotopic cortex. We placed stimuli in four well separated locations of the visual field and required participants to attend to and integrate informa...

“…Chemical tracer studies in the monkey brain indicate that although ventral pulvinar neurons predominantly represent the contralateral hemifield (13,19,39) neurons with large, bilateral receptive fields have been recorded from cells within macaque lateral (ventral) pulvinar (40). Similarly, fMRI evidence in healthy humans (27,30) suggests that, as in the monkey, human pulvinar may have neurons with large receptive fields that can influence attentional competition across the entire visual field. However, a more recent fMRI study reported activation within ventral pulvinar only for contralateral events (41).…”

Section: Discussionmentioning

confidence: 99%

“…Heretofore, neuropsychological studies in patients with pulvinar damage have found no evidence that distracters interfere with performance (22-24), and one study reports reduced flanker interference from contralesional distracters (25). Pulvinar activation has nevertheless been reported using fMRI or positron emission tomography in healthy human observers during filtering tasks or other attentional paradigms (8,(26)(27)(28)(29)(30). The lack of distracter interference effects in human neuropsychological studies may reflect the use of behavioral tasks that measured the effects of response conflict, rather than perceptual selection of stimuli based on their behavioral salience.…”

mentioning

confidence: 99%

Impaired attentional selection following lesions to human pulvinar: Evidence for homology between human and monkey

Snow

Allen

Rafal

et al. 2009

174

113

We examined the contributions of the human pulvinar to goal directed selection of visual targets in 3 patients with chronic, unilateral lesions involving topographic maps in the ventral pulvinar. Observers completed 2 psychophysical tasks in which they discriminated the orientation of a lateralized target grating in the presence of vertically-aligned distracters. In experiment 1, where distracter contrast was varied while target contrast remained constant, the patients' contralesional contrast thresholds for discriminating the orientation of grating stimuli were elevated only when the task required selection of a visual target in the face of competition from a salient distracter. Attentional selectivity was restored in the patients in experiment 2 where target contrast was varied while distracter contrast remained constant. These observations provide the first evidence that the human pulvinar plays a necessary role in modulating physical saliency in attentional selection, and supports a homology in global pulvinar structure between humans and monkey.salience ͉ visual attention M ultiple items within a visual scene compete for our focal attention. This competition is resolved on the basis of both the perceptual salience of the stimulus and its behavioral salience in relation to the goals of ongoing behavior (1). Visual items can compete for representation in ventral occipito-temporal brain areas, with this competition varying according to the physical distinctiveness of the items and according to whether they demand processing through the same receptive fields (2, 3). The competition can also be biased in favor of less conspicuous objects if they are nonetheless more relevant for behavior (2,4,5). These ''goaldriven'' attentional control signals arise within dorsal frontoparietal networks (6-8) and they lead to behavioral improvements in discriminating the features of the attended object (9, 10). What remains unclear is how such ''dorsal'' attentional signals are communicated to ventral occipital and temporal areas to bias visual analysis. Here, we report the first direct behavioral evidence in humans for the role of the pulvinar in coordinating these goaldriven and stimulus-driven interactions. We used a sensitive psychophysical task to examine target selection in a special group of patients with well documented chronic, unilateral lesions involving topographic maps in the ventral pulvinar. Our findings demonstrate that the pulvinar plays an important role in filtering irrelevant but salient visual distracters.The pulvinar nucleus of the thalamus has been hypothesized to play a central role in coordinating attentional effects on visual processing (11,12). Most of our current knowledge on patterns of connectivity of the pulvinar stems from anatomical studies in non-human primates. The primate pulvinar has extensive connectivity with the cortex. Based on this connectivity, several general organising principles within the pulvinar have been suggested: a global dorsal/ventral division, and an anterior/ posterior org...