Subcortical Attention


The role of the pulvinar in distractor processing and visual search

H. Strumpf and G. R. Mangun and C. N. Boehler and C. Stoppel and M. A. Schoenfeld and H.-J. Heinze and J.-M. Hopf

Hum Brain Mapp  34  1115-32  (2013)

The pulvinar nuclei of the thalamus are hypothesized to coordinate attentional selection in the visual cortex. Different models have, however, been proposed for the precise role of the pulvinar in attention. One proposal is that the pulvinar mediates shifts of spatial attention; a different proposal is that it serves the filtering of distractor information. At present, the relation between these possible operations and their relative importance in the pulvinar remains unresolved. We address this issue by contrasting these proposals in two fMRI experiments. We used a visual search paradigm that permitted us to dissociate neural activity reflecting shifts of attention from activity underlying distractor filtering. We find that distractor filtering, but not the operation of shifting attention, is associated with strong activity enhancements in dorsal and ventral regions of the pulvinar as well as in early visual cortex areas including the primary visual cortex. Our observations indicate that distractor filtering is the preponderant attentional operation subserved by the pulvinar, presumably mediated by a modulation of processing in visual areas where spatial resolution is sufficiently high to separate target from distractor input.


fMRI assessment of thalamocortical connectivity during attentional performance

J. Zhang and K.-W. Chu and E. B. Teague and R. E. Newmark and M. S. Buchsbaum

Magn Reson Imaging  31  1112-8  (2013)

Functional magnetic resonance imaging (fMRI) studies have shown dysfunction in key areas associated with the thalamocortical circuit in patients with schizophrenia. This study examined the functional connectivity involving the frontal-thalamic circuitry during a spatial focusing-of-attention task in 18 unmedicated patients with schizophrenia and 38 healthy controls. Functional connectivity was analyzed by assigning seed regions (in the thalamic nuclei (mediodorsal nucleus (MDN), pulvinar, anterior nucleus (AN)), the dorsolateral prefrontal cortex (Brodmann areas 9 and 46), and the caudate), and correlating their respective activity with that in the non-seed regions voxel-wise. Functional connectivity analysis demonstrated that functional connectivity was significantly impaired in patients, e.g., between the right pulvinar and regions such as the prefrontal and temporal cortices and the cerebellum. On the other hand, enhanced functional connectivity was found in patients, e.g., between the AN and regions such as the prefrontal and temporal cortices. In addition, the patients had significantly lower task performance and less (but non-significant) brain activation than those of controls. These results revealed disturbed functional integration in schizophrenia, and suggested that the functional connectivity abnormalities in the thalamocortical circuitry, especially the frontal-thalamic circuitry, may underlie the attention deficits in schizophrenia patients. Further, this study suggested that functional connectivity analysis might be more sensitive than brain activation analysis in detecting the functional abnormalities in schizophrenia.


Simultaneous EEG-fMRI Reveals Temporal Evolution of Coupling between Supramodal Cortical Attention Networks and the Brainstem

J. M. Walz and R. I. Goldman and M. Carapezza and J. Muraskin and T. R. Brown and P. Sajda

J Neurosci  33  19212-22  (2013)

Cortical and subcortical networks have been identified that are commonly associated with attention and task engagement, along with theories regarding their functional interaction. However, a link between these systems has not yet been demonstrated in healthy humans, primarily because of data acquisition and analysis limitations. We recorded simultaneous EEG-fMRI while subjects performed auditory and visual oddball tasks and used these data to investigate the BOLD correlates of single-trial EEG variability at latencies spanning the trial. We focused on variability along task-relevant dimensions in the EEG for identical stimuli and then combined auditory and visual data at the subject level to spatially and temporally localize brain regions involved in endogenous attentional modulations. Specifically, we found that anterior cingulate cortex (ACC) correlates strongly with both early and late EEG components, whereas brainstem, right middle frontal gyrus (rMFG), and right orbitofrontal cortex (rOFC) correlate significantly only with late components. By orthogonalizing with respect to event-related activity, we found that variability in insula and temporoparietal junction is reflected in reaction time variability, rOFC and brainstem correlate with residual EEG variability, and ACC and rMFG are significantly correlated with both. To investigate interactions between these correlates of temporally specific EEG variability, we performed dynamic causal modeling (DCM) on the fMRI data. We found strong evidence for reciprocal effective connections between the brainstem and cortical regions. Our results support the adaptive gain theory of locus ceruleus-norepinephrine (LC-NE) function and the proposed functional relationship between the LC-NE system, right-hemisphere ventral attention network, and P300 EEG response.


Mechanisms underlying the basal forebrain enhancement of top-down and bottom-up attention

M. C. Avery and N. Dutt and J. L. Krichmar

Eur J Neurosci      (2013)

Both attentional signals from frontal cortex and neuromodulatory signals from basal forebrain (BF) have been shown to influence information processing in the primary visual cortex (V1). These two systems exert complementary effects on their targets, including increasing firing rates and decreasing interneuronal correlations. Interestingly, experimental research suggests that the cholinergic system is important for increasing V1's sensitivity to both sensory and attentional information. To see how the BF and top-down attention act together to modulate sensory input, we developed a spiking neural network model of V1 and thalamus that incorporated cholinergic neuromodulation and top-down attention. In our model, activation of the BF had a broad effect that decreases the efficacy of top-down projections and increased the reliance of bottom-up sensory input. In contrast, we demonstrated how local release of acetylcholine in the visual cortex, which was triggered through top-down gluatmatergic projections, could enhance top-down attention with high spatial specificity. Our model matched experimental data showing that the BF and top-down attention decrease interneuronal correlations and increase between-trial reliability. We found that decreases in correlations were primarily between excitatory-inhibitory pairs rather than excitatory-excitatory pairs and suggest that excitatory-inhibitory decorrelation is necessary for maintaining low levels of excitatory-excitatory correlations. Increased inhibitory drive via release of acetylcholine in V1 may then act as a buffer, absorbing increases in excitatory-excitatory correlations that occur with attention and BF stimulation. These findings will lead to a better understanding of the mechanisms underyling the BF's interactions with attention signals and influences on correlations.


Effects of sustained spatial attention in the human lateral geniculate nucleus and superior colliculus

K. A. Schneider and S. Kastner

J Neurosci  29  1784-95  (2009)

The role of subcortical visual structures such as the lateral geniculate nucleus (LGN) and the superior colliculus (SC) in the control of visual spatial attention remains poorly understood. Here, we used high-resolution functional magnetic resonance imaging to measure responses in the human LGN and SC during sustained spatial attention. Subjects covertly and continuously tracked one of two segments that rotated through the visual field, composed of either moving dots or transient colored shapes. Activity in both nuclei was generally enhanced by attention, independent of the stimulus type, with the voxels responding more sensitively to stimulus contrast (those dominated by magnocellular input) exhibiting greater attentional enhancement. The LGN contained clusters of voxels exhibiting attentional enhancement or weak suppression, whereas the SC exhibited predominantly attentional enhancement, which was significantly stronger than in the LGN. The spatial distribution of the attentional effects was unrelated to the retinotopic organization in either structure. The results demonstrate that each of the major subcortical visual pathways participates in attentional selection, and their differential magnitudes of modulation suggest distinct roles.


The functional logic of cortico-pulvinar connections

S. Shipp

Philos Trans R Soc Lond B Biol Sci  358  1605-24  (2003)

The pulvinar is an 'associative' thalamic nucleus, meaning that most of its input and output relationships are formed with the cerebral cortex. The function of this circuitry is little understood and its anatomy, though much investigated, is notably recondite. This is because pulvinar connection patterns disrespect the architectural subunits (anterior, medial, lateral and inferior pulvinar nuclei) that have been the traditional reference system. This article presents a simplified, global model of the organization of cortico-pulvinar connections so as to pursue their structure-function relationships. Connections between the cortex and pulvinar are topographically organized, and as a result the pulvinar contains a 'map' of the cortical sheet. However, the topography is very blurred. Hence the pulvinar connection zones of nearby cortical areas overlap, allowing indirect transcortical communication via the pulvinar. A general observation is that indirect cortico-pulvino-cortical circuits tend to mimic direct cortico-cortical pathways: this is termed 'the replication principle'. It is equally apt for certain pairs (or groups) of nearby cortical areas that happen not to connect with each other. The 'replication' of this non-connection is achieved by discontinuities and dislocations of the cortical topography within the pulvinar, such that the associated pair of connection zones do not overlap. Certain of these deformations can be used to divide the global cortical topography into specific sub-domains, which form the natural units of a connectional subdivision of the pulvinar. A substantial part of the pulvinar also expresses visual topography, reflecting visual maps in occipital cortex. There are just two well-ordered visual maps in the pulvinar, that both receive projections from area V1, and several other occipital areas; the resulting duplication of cortical topography means that each visual map also acts as a separate connection domain. In summary, the model identifies four topographically ordered connection domains, and reconciles the coexistence of visual and cortical maps in two of them. The replication principle operates at and below the level of domain structure. It is argued that cortico-pulvinar circuitry replicates the pattern of cortical circuitry but not its function, playing a more regulatory role instead. Thalamic neurons differ from cortical neurons in their inherent rhythmicity, and the pattern of cortico-thalamic connections must govern the formation of specific resonant circuits. The broad implication is that the pulvinar acts to coordinate cortical information processing by facilitating and sustaining the formation of synchronized trans-areal assemblies; a more pointed suggestion is that, owing to the considerable blurring of cortical topography in the pulvinar, rival cortical assemblies may be in competition to recruit thalamic elements in order to outlast each other in activity.


Gating and control of primary visual cortex by pulvinar

G. Purushothaman and R. Marion and K. Li and V. A. Casagrande

Nat Neurosci  15  905-12  (2012)

The primary visual cortex (V1) receives its driving input from the eyes via the lateral geniculate nucleus (LGN) of the thalamus. The lateral pulvinar nucleus of the thalamus also projects to V1, but this input is not well understood. We manipulated lateral pulvinar neural activity in prosimian primates and assessed the effect on supra-granular layers of V1 that project to higher visual cortex. Reversibly inactivating lateral pulvinar prevented supra-granular V1 neurons from responding to visual stimulation. Reversible, focal excitation of lateral pulvinar receptive fields increased the visual responses in coincident V1 receptive fields fourfold and shifted partially overlapping V1 receptive fields toward the center of excitation. V1 responses to regions surrounding the excited lateral pulvinar receptive fields were suppressed. LGN responses were unaffected by these lateral pulvinar manipulations. Excitation of lateral pulvinar after LGN lesion activated supra-granular layer V1 neurons. Thus, lateral pulvinar is able to powerfully control and gate information outflow from V1.


The thalamus interrupts top-down attentional control for permitting exploratory shiftings to sensory signals

G. A. Michael and M. Boucart and J. F. Degreef and O. Godefroy

Neuroreport  12  2041-8  (2001)

When attention is involuntarily drawn in a direction different to that of the target, slower motor response times are observed (i.e. the meridian effect). Previous data suggested that the thalamus might participate in the generation of visual salience. What may be the role of the thalamus in the capture by luminance transients when attentional control is in action? A single experiment was administrated in a group of ten healthy volunteers as well as in a group of three patients with unilateral thalamic infarcts. Subjects participated in a task where attentional control was interrupted by a distractor. The meridian effect was present only in the performance of the healthy volunteers and when distractors occurred in the ipsilesional (intact) hemifield of the thalamic patients. These results suggest that when an important signal appears during attentional focalization, the thalamus interrupts current focalization and permits the compilation of an attentional program in the midbrain aiming at generating an orienting response towards the source of this signal.


An object-based frame of reference within the human pulvinar

R. Ward and I. Arend

Brain  130  2462-9  (2007)

The pulvinar nucleus of the thalamus is massively interconnected to cortical areas which translate spatial visual information into coordinate systems defined by multiple reference frames [Grieve et al. (The primate pulvinar nuclei: vision and action. Trends in Neurosciences 2000; 23(1): 35-39)]. Here we report the first evidence that spatial coding in the pulvinar is defined by an object-based frame. We evaluated the efficiency of spatial coding in two patients with damage to spatial maps within the pulvinar. Patients located targets within a 2 x 2 (up/down x left/right) search array, which was itself located within a 2 x 2 retinotopic space. For both patients, spatial deficits were defined in both a retinotopic and an object-based frame. For example, targets in the contralesional side of the array were poorly localized whether the array appeared in contra or ipsilesional retinotopic space. We conclude that spatial processing bias following pulvinar damage can be defined by coordinate systems based on both object-based and retinotopic spaces.


Pulvinar contributions to the dorsal and ventral streams of visual processing in primates

J. H. Kaas and D. C. Lyon

Brain Res Rev  55  285-96  (2007)

The visual pulvinar is part of the dorsal thalamus, and in primates it is especially well developed. Recently, our understanding of how the visual pulvinar is subdivided into nuclei has greatly improved as a number of histological procedures have revealed marked architectonic differences within the pulvinar complex. At the same time, there have been unparalleled advances in understanding of how visual cortex of primates is subdivided into areas and how these areas interconnect. In addition, considerable evidence supports the view that the hierarchy of interconnected visual areas is divided into two major processing streams, a ventral stream for object vision and a dorsal stream for visually guided actions. In this review, we present evidence that a subset of medial nuclei in the inferior pulvinar function predominantly as a subcortical component of the dorsal stream while the most lateral nucleus of the inferior pulvinar and the adjoining ventrolateral nucleus of the lateral pulvinar are more devoted to the ventral stream of cortical processing. These nuclei provide cortico-pulvinar-cortical interactions that spread information across areas within streams, as well as information relayed from the superior colliculus via inferior pulvinar nuclei to largely dorsal stream areas.


The role of the dorsal thalamus in visual processing and object selection: a case of an attentional system in amphibians

T. Ruhl and U. Dicke

Eur J Neurosci  36  3459-70  (2012)

In amphibians, the midbrain tectum is regarded as the visual centre for object recognition but the functional role of forebrain centres in visual information processing is less clear. In order to address this question, the dorsal thalamus was lesioned in the salamander Plethodon shermani, and the effects on orienting behaviour or on visual processing in the tectum were investigated. In a two-alternative-choice task, the average number of orienting responses toward one of two competing prey or simple configural stimuli was significantly decreased in lesioned animals compared to that of controls and sham-lesioned animals. When stimuli were presented during recording from tectal neurons, the number of spikes on presentation of a stimulus in the excitatory receptive field and a second salient stimulus in the surround was significantly reduced in controls and sham-lesioned salamanders compared to single presentation of the stimulus in the excitatory receptive field, while this inhibitory effect on the number of spikes of tectal neurons was absent in thalamus-lesioned animals. In amphibians, the dorsal thalamus is part of the second visual pathway which extends from the tectum via the thalamus to the telencephalon. A feedback loop to the tectum is assumed to modulate visual processing in the tectum and to ensure orienting behaviour toward visual objects. It is concluded that the tectum-thalamus-telencephalon pathway contributes to the recognition and evaluation of objects and enables spatial attention in object selection. This attentional system in amphibians resembles that found in mammals and illustrates the essential role of attention for goal-directed visuomotor action.


Gating of attentional effort through the central thalamus

N. D. Schiff and S. A. Shah and A. E. Hudson and T. Nauvel and S. F. Kalik and K. P. Purpura

J Neurophysiol  109  1152-63  (2013)

The central thalamus plays an important role in the regulation of arousal and allocation of attentional resources in the performance of even simple tasks. To assess the contribution of central thalamic neurons to short-term adjustments of attentional effort, we analyzed 166 microelectrode recordings obtained from two rhesus monkeys performing a visuomotor simple reaction time task with a variable foreperiod. Multiunit responses showed maintained firing rate elevations during the variable delay period of the task in 24% of recording sites. Simultaneously recorded local field potentials demonstrated significant decreases in power at 10-20 Hz and increases in power at 30-100 Hz during the delay period when compared against precue baselines. Comparison of the spectral power of local field potentials during the delay period of correct and incorrect trials showed that, during incorrect trials, similar, but reduced, shifts of spectral power occurred within the same frequency bands. Sustained performance of even simple tasks requires regulation of arousal and attention that combine in the concept of "attentional effort". Our findings suggest that central thalamic neurons regulate task performance through brief changes in firing rates and spectral power changes during task-relevant short-term shifts of attentional effort. Increases in attentional effort may be reflected in changes within the central thalamic local populations, where correct task performance associates with more robust maintenance of firing rates during the delay period. Such ongoing fluctuations of central thalamic activity likely reflect a mix of influences, including variations in moment-to-moment levels of motivation, arousal, and availability of cognitive resources.


Effect of attentive fixation in macaque thalamus and cortex

D. B. Bender and M. Youakim

J Neurophysiol  85  219-34  (2001)


Attentional modulation of neuronal responsiveness is common in many areas of visual cortex. We examined whether attentional modulation in the visual thalamus was quantitatively similar to that in cortex. Identical procedures and apparatus were used to compare attentional modulation of single neurons in seven different areas of the visual system: the lateral geniculate, three visual subdivisions of the pulvinar [inferior, lateral, dorsomedial part of lateral pulvinar (Pdm)], and three areas of extrastriate cortex representing early, intermediate, and late stages of cortical processing (V2, V4/PM, area 7a). A simple fixation task controlled transitions among three attentive states. The animal waited for a fixation point to appear (ready state), fixated the point until it dimmed (fixation state), and then waited idly to begin the next trial (idle state). Attentional modulation was estimated by flashing an identical, irrelevant stimulus in a neuron's receptive field during each of the three states; the three responses defined a "response vector" whose deviation from the line of equal response in all three states (the main diagonal) indicated the character and magnitude of attentional modulation. Attentional modulation was present in all visual areas except the lateral geniculate, indicating that modulation was of central origin. Prevalence of modulation was modest (26%) in pulvinar, and increased from 21% in V2 to 43% in 7a. Modulation had a push-pull character (as many cells facilitated as suppressed) with respect to the fixation state in all areas except Pdm where all cells were suppressed during fixation. The absolute magnitude of attentional modulation, measured by the angle between response vector and main diagonal expressed as a percent of the maximum possible angle, differed among brain areas. Magnitude of modulation was modest in the pulvinar (19-26%), and increased from 22% in V2 to 41% in 7a. However, average trial-to-trial variability of response, measured by the coefficient of variation, also increased across brain areas so that its difference among areas accounted for more than 90% of the difference in modulation magnitude among areas. We also measured attentional modulation by the ratio of cell discharge due to attention divided by discharge variability. The resulting signal-to-noise ratio of attention was small and constant, 1.3 +/- 10%, across all areas of pulvinar and cortex. We conclude that the pulvinar, but not the lateral geniculate, is as strongly affected by attentional state as any area of visual cortex we studied and that attentional modulation amplitude is closely tied to intrinsic variability of response.


The human pulvinar and attentional processing of visual distractors

G. A. Michael and S. Desmedt

Neurosci Lett  362  176-81  (2004)

The processing of a target is degraded when noise is present in proximity, and performance increases as the target-noise distance increases. We tested a group of healthy volunteers and a group of patients, who suffered strokes in the posterior thalamus, in a task where the target-noise distance was manipulated. Whilst controls exhibited the expected pattern of results, thalamic patients exhibited little signs of noise interference. Interference occurred when the target-noise distance was 0 degrees (the target and noise were superimposed), but it was absent for distances equal to and bigger than 1 degree. The results suggest that the coarse grain of visual attention reported previously might be due to some aspects of attention processing underlain by the pulvinar and acting to grab the visual context or background of a target.


Corticocortical and thalamocortical information flow in the primate visual system

D. C. Van Essen

Prog Brain Res  149  173-85  (2005)

Visual cortex in primates contains a mosaic of several dozen visual areas that collectively occupy a large fraction of cerebral cortex (approximately 50% in the macaque; approximately 25% in humans). These areas are richly interconnected by hundreds of reciprocal corticocortical pathways that underlie an anatomically based hierarchy containing multiple processing streams. In addition, there is a complex pattern of reciprocal connections with the pulvinar, which itself contains about 10 architectonically distinct subdivisions. Information flow through these corticocortical and corticothalamic circuits is regulated very dynamically by top-down as well as bottom-up processes, including directed visual attention. This chapter evaluates current hypotheses and evidence relating to the interaction between thalamocortical and corticocortical circuitry in the dynamic regulation of information flow.


Thalamocortical circuits: fMRI assessment of the pulvinar and medial dorsal nucleus in normal volunteers

M. S. Buchsbaum and B. R. Buchsbaum and S. Chokron and C. Tang and T.-C. Wei and W. Byne

Neurosci Lett  404  282-7  (2006)

This fMRI study investigates the activation of the thalamic nuclei in a spatial focusing-of-attention task previously shown to activate the pulvinar with FDG-PET and assesses the connectivity of the thalamic nuclei with cortical areas. Normal right-handed subjects (eight men, eight women, average age=32 years) viewed four types of stimuli positioned to the right or left of the central fixation point (left hemifield-large letter, left hemifield-small letter display with flanking letters; right hemifield-large letter, right hemifield-small letter display with flankers). BOLD responses to small letters surrounded by flankers were compared with responses to large isolated letters. To examine maximum functional regional connectivity, we modeled "subject" as a random effect and attained fixed effect parameter estimates and t-statistics for functional connectivity between each of the thalamic nuclei (pulvinar, medial dorsal, and anterior) as the seed region and each non-seed voxel. Greater BOLD activation for letters surrounded by flankers than for large letters was observed in the pulvinar as anticipated and was also marked in the medial dorsal nucleus (MDN), anterior and superior cingulate (BA24 and BA24'), dorsolateral prefrontal cortex, and frontal operculum and insula. For the MDN, maximal functional connectivity was with the dorsolateral prefrontal cortex; correlations with left superior temporal, parietal, posterior frontal, and occipital regions were also observed. For the pulvinar, maximal functional connectivity was with parietal BA39; for anterior thalamus, with anterior cingulate.


The human pulvinar and stimulus-driven attentional control

G. A. Michael and V. Buron

Behav Neurosci  119  1353-67  (2005)

The present study compared the behavioral effects of sudden motion onsets or color changes (i.e., featural changes) with the effects of new objects (i.e., multiple changes). Experiments 1 and 2 showed that lesions of the pulvinar affect stimulus-driven attentional control only when it is triggered by featural changes, but not by new objects. Experiment 3 revealed that when appended on a new object, a featural change is processed as a part of a more massive new object: Its attentional effects are larger and remain undisturbed by lesions of the pulvinar. In Experiment 4 a temporal superiority effect was found for featural changes, but not for new objects in healthy subjects. These results suggest that featural changes and new objects may be processed through different pathways and that the pulvinar may be particularly involved in stimulus-driven attentional control by sudden events entailing featural changes.


Two streams of attention-dependent beta activity in the striate recipient zone of cat's lateral posterior-pulvinar complex

A. Wróbel and A. Ghazaryan and M. Bekisz and W. Bogdan and J. Kamiński

J Neurosci  27  2230-40  (2007)

Local field potentials from different visual cortical areas and subdivisions of the cat's lateral posterior-pulvinar complex of the thalamus (LP-P) were recorded during a behavioral task based on delayed spatial discrimination of visual or auditory stimuli. During visual but not auditory attentive tasks, we observed an increase of beta activity (12-25 Hz) as calculated from signals recorded from the caudal part of the lateral zone of the LP-P (LPl-c) as well as from cortical areas 17 and 18 and the complex located at the middle suprasylvian sulcus (MSS). This beta activity appeared only in the trials that ended with a successful response, proving its relationship to the mechanism of visual attention. In contrast, no enhanced beta activity was observed in the rostral part of the lateral zone of the LP-P and in the pulvinar proper. Two subregions of LPl-c (ventromedial and dorsolateral) were distinguished by visually related, attentional beta activity of low (12-18 Hz) and high (18-25 Hz) frequencies, respectively. At the same time, area 17 exhibited attentional activation in the whole beta range, and an increase of power in low-frequency beta was observed in the medial bank of MSS, whereas cortical area 18 and the lateral bank of the MSS were activated in the high beta range. Phase-correlation analysis revealed that two distinct corticothalamic systems were synchronized by the beta activity of different frequencies. One comprised of cortical area 17, ventromedial region of LPl-c, and medial MSS, the second involved area 18 and the dorsolateral LPl-c. Our observations suggest that LPl-c belongs to the wide corticothalamic attentional system, which is functionally segregated by distinct streams of beta activity.


The role of the human pulvinar in visual attention and action: evidence from temporal-order judgment, saccade decision, and antisaccade tasks

I. Arend and L. Machado and R. Ward and M. McGrath and T. Ro and R. D. Rafal

Prog Brain Res  171  475-83  (2008)

The pulvinar nucleus of the thalamus has been considered as a key structure for visual attention functions (Grieve, K.L. et al. (2000). Trends Neurosci., 23: 35-39; Shipp, S. (2003). Philos. Trans. R. Soc. Lond. B Biol. Sci., 358(1438): 1605-1624). During the past several years, we have studied the role of the human pulvinar in visual attention and oculomotor behaviour by testing a small group of patients with unilateral pulvinar lesions. Here we summarize some of these findings, and present new evidence for the role of this structure in both eye movements and visual attention through two versions of a temporal-order judgment task and an antisaccade task. Pulvinar damage induces an ipsilesional bias in perceptual temporal-order judgments and in saccadic decision, and also increases the latency of antisaccades away from contralesional targets. The demonstration that pulvinar damage affects both attention and oculomotor behaviour highlights the role of this structure in the integration of visual and oculomotor signals and, more generally, its role in flexibly linking visual stimuli with context-specific motor responses.


Dissociating vision and visual attention in the human pulvinar

A. T. Smith and P. L. Cotton and A. Bruno and C. Moutsiana

J Neurophysiol  101  917-25  (2009)

The pulvinar region of the thalamus has repeatedly been linked with the control of attention. However, the functions of the pulvinar remain poorly characterized, both in human and in nonhuman primates. In a functional MRI study, we examined the relative contributions to activity in the human posterior pulvinar made by visual drive (the presence of an unattended visual stimulus) and attention (covert spatial attention to the stimulus). In an event-related design, large optic flow stimuli were presented to the left and/or right of a central fixation point. When unattended, the stimuli robustly activated two regions of the pulvinar, one medial and one dorsal with respect to the lateral geniculate. The activity in both regions shows a strong contralateral bias, suggesting retinotopic organization. Primate physiology suggests that the two regions could be two portions of the same double map of the visual field. In our paradigm, attending to the stimulus enhanced the response by about 20%. Thus attention is not necessary to activate the human pulvinar and the degree of attentional enhancement matches, but does not exceed, that seen in the cortical regions with which the posterior pulvinar connects.


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

J. C. Snow and H. A. Allen and R. D. Rafal and G. W. Humphreys

Proc Natl Acad Sci U S A  106  4054-9  (2009)

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.


Neural activity in the visual thalamus reflects perceptual suppression

M. Wilke and K.-M. Mueller and D. A. Leopold

Proc Natl Acad Sci U S A  106  9465-70  (2009)

To examine the role of the visual thalamus in perception, we recorded neural activity in the lateral geniculate nucleus (LGN) and pulvinar of 2 macaque monkeys during a visual illusion that induced the intermittent perceptual suppression of a bright luminance patch. Neural responses were sorted on the basis of the trial-to-trial visibility of the stimulus, as reported by the animals. We found that neurons in the dorsal and ventral pulvinar, but not the LGN, showed changes in spiking rate according to stimulus visibility. Passive viewing control sessions showed such modulation to be independent of the monkeys' active report. Perceptual suppression was also accompanied by a marked drop in low-frequency power (9-30 Hz) of the local field potential (LFP) throughout the visual thalamus, but this modulation was not observed during passive viewing. Our findings demonstrate that visual responses of pulvinar neurons reflect the perceptual awareness of a stimulus, while those of LGN neurons do not.


Gain control in the visual thalamus during perception and cognition

Y. B. Saalmann and S. Kastner

Curr Opin Neurobiol  19  408-14  (2009)

The thalamus has traditionally been thought to passively relay sensory information to the cortex. By showing that responses in visual thalamus are modulated by perceptual and cognitive tasks, recent fMRI and physiology studies have helped revise this view. The modulatory input to the visual thalamus derives from functionally distinct cortical and subcortical feedback pathways. These pathways enable the lateral geniculate nucleus and pulvinar to regulate the information transmitted to cortical areas according to cognitive requirements. Emerging evidence suggests that such regulation involves changing the degree of synchrony between neurons as well as changing the magnitude of thalamic activity. These findings support a role for the thalamus that extends as far as contributing to the control of visual attention and awareness.


Pulvinar inactivation disrupts selection of movement plans

M. Wilke and J. Turchi and K. Smith and M. Mishkin and D. A. Leopold

J Neurosci  30  8650-9  (2010)

The coordinated movement of the eyes and hands under visual guidance is an essential part of goal-directed behavior. Several cortical areas known to be involved in this process exchange projections with the dorsal aspect of the thalamic pulvinar nucleus, suggesting that this structure may play a central role in visuomotor behavior. Here, we used reversible inactivation to investigate the role of the dorsal pulvinar in the selection and execution of visually guided manual and saccadic eye movements in macaque monkeys. We found that unilateral pulvinar inactivation resulted in a spatial neglect syndrome accompanied by visuomotor deficits including optic ataxia during visually guided limb movements. Monkeys were severely disrupted in their visually guided behavior regarding space contralateral to the side of the injection in several domains, including the following: (1) target selection in both manual and oculomotor tasks, (2) limb usage in a manual retrieval task, and (3) spontaneous visual exploration. In addition, saccades into the ipsilesional field had abnormally short latencies and tended to overshoot their mark. None of the deficits could be explained by a visual field defect or primary motor deficit. These findings highlight the importance of the dorsal aspect of the pulvinar nucleus as a critical hub for spatial attention and selection of visually guided actions.


Spatially distributed encoding of covert attentional shifts in human thalamus

O. J. Hulme and L. Whiteley and S. Shipp

J Neurophysiol  104  3644-56  (2010)

Spatial attention modulates signal processing within visual nuclei of the thalamus--but do other nuclei govern the locus of attention in top-down mode? We examined functional MRI (fMRI) data from three subjects performing a task requiring covert attention to 1 of 16 positions in a circular array. Target position was cued after stimulus offset, requiring subjects to perform target detection from iconic visual memory. We found positionally specific responses at multiple thalamic sites, with individual voxels activating at more than one direction of attentional shift. Voxel clusters at anatomically equivalent sites across subjects revealed a broad range of directional tuning at each site, with little sign of contralateral bias. By reference to a thalamic atlas, we identified the nuclear correspondence of the four most reliably activated sites across subjects: mediodorsal/central-intralaminar (oculomotor thalamus), caudal intralaminar/parafascicular, suprageniculate/limitans, and medial pulvinar/lateral posterior. Hence, the cortical network generating a top-down control signal for relocating attention acts in concert with a spatially selective thalamic apparatus-the set of active nuclei mirroring the thalamic territory of cortical "eye-field" areas, thus supporting theories which propose the visuomotor origins of covert attentional selection.


Neuronal mechanisms for visual stability: progress and problems

R. H. Wurtz and W. M. Joiner and R. A. Berman

Philos Trans R Soc Lond B Biol Sci  366  492-503  (2011)

How our vision remains stable in spite of the interruptions produced by saccadic eye movements has been a repeatedly revisited perceptual puzzle. The major hypothesis is that a corollary discharge (CD) or efference copy signal provides information that the eye has moved, and this information is used to compensate for the motion. There has been progress in the search for neuronal correlates of such a CD in the monkey brain, the best animal model of the human visual system. In this article, we briefly summarize the evidence for a CD pathway to frontal cortex, and then consider four questions on the relation of neuronal mechanisms in the monkey brain to stable visual perception. First, how can we determine whether the neuronal activity is related to stable visual perception? Second, is the activity a possible neuronal correlate of the proposed transsaccadic memory hypothesis of visual stability? Third, are the neuronal mechanisms modified by visual attention and does our perceived visual stability actually result from neuronal mechanisms related primarily to the central visual field? Fourth, does the pathway from superior colliculus through the pulvinar nucleus to visual cortex contribute to visual stability through suppression of the visual blur produced by saccades?


Subcortical mechanisms of feature-based attention

K. A. Schneider

J Neurosci  31  8643-53  (2011)

The degree to which spatial and feature-based attention are governed by similar control mechanisms is not clear. To explore this issue, I measured, during conditions of spatial or feature-based attention, activity in the human subcortical visual nuclei, which have precise retinotopic maps and are known to play important roles in the regulation of spatial attention but have limited selectivity of nonspatial features. Subjects attended to and detected changes in separate fields of moving or colored dots. When the fields were disjoint, spatially attending to one field enhanced hemodynamic responses in the superior colliculus (SC), lateral geniculate nucleus (LGN), and two retinotopic pulvinar nuclei. When the two dot fields were spatially overlapping, feature-based attention to the moving versus colored dots enhanced responses in the pulvinar nuclei and the majority of the LGN, including the magnocellular layers, and suppressed activity in some areas within the parvocellular layers; the SC was inconsistently modulated among subjects. The results demonstrate that feature-based attention operates throughout the visual system by prioritizing neurons encoding the attended information, including broadly tuned thalamic neurons. I conclude that spatial and feature-based attention operate via a common principle, but that spatial location is a special feature in that it is widely encoded in the brain, is used for overt orienting, and uses a specialized structure, the SC.


Attentional modulation of primary interoceptive and exteroceptive cortices

N. A. S. Farb and Z. V. Segal and A. K. Anderson

Cereb Cortex  23  114-26  (2013)

How exteroceptive attention (EA) alters neural representations of the external world is well characterized, yet little is known about how interoceptive attention (IA) alters neural representations of the body's internal state. We contrasted visual EA against IA toward respiration. Visual EA modulated striate and extrastriate cortices and a lateral frontoparietal "executive" network. By contrast, respiratory IA modulated a posterior insula region sensitive to respiratory frequency, consistent with primary interoceptive cortex, and a posterior limbic and medial parietal network, including the hippocampus, precuneus, and midcingulate cortex. Further distinguishing between EA and IA networks, attention-dependent connectivity analyses revealed that EA enhanced visual cortex connectivity with the inferior parietal lobule and pulvinar of the thalamus, while IA enhanced insula connectivity with the posterior ventromedial thalamus, a relay of the laminar I spinothalamocortical pathway supporting interoceptive afference. Despite strong connectivity between the posterior and the anterior insula, anatomical parcellation of the insula revealed a gradient of IA to EA recruitment along its posterior-anterior axis. These results suggest that distinct networks may support EA and IA. Furthermore, the anterior insula is not an area of pure body awareness but may link representations of the outside world with the body's internal state--a potential basis for emotional experience.


The pulvinar regulates information transmission between cortical areas based on attention demands

Y. B. Saalmann and M. A. Pinsk and L. Wang and X. Li and S. Kastner

Science  337  753-6  (2012)

Selective attention mechanisms route behaviorally relevant information through large-scale cortical networks. Although evidence suggests that populations of cortical neurons synchronize their activity to preferentially transmit information about attentional priorities, it is unclear how cortical synchrony across a network is accomplished. Based on its anatomical connectivity with the cortex, we hypothesized that the pulvinar, a thalamic nucleus, regulates cortical synchrony. We mapped pulvino-cortical networks within the visual system, using diffusion tensor imaging, and simultaneously recorded spikes and field potentials from these interconnected network sites in monkeys performing a visuospatial attention task. The pulvinar synchronized activity between interconnected cortical areas according to attentional allocation, suggesting a critical role for the thalamus not only in attentional selection but more generally in regulating information transmission across the visual cortex.


Attention gates visual coding in the human pulvinar

J. Fischer and D. Whitney

Nat Commun  3  1051  (2012)

The pulvinar nucleus of the thalamus is suspected to have an important role in visual attention, based on its widespread connectivity with the visual cortex and the fronto-parietal attention network. However, at present, there remain many hypotheses on the pulvinar's specific function, with sparse or conflicting evidence for each. Here we characterize how the human pulvinar encodes attended and ignored objects when they appear simultaneously and compete for attentional resources. Using multivoxel pattern analyses on data from two functional magnetic resonance imaging (fMRI) experiments, we show that attention gates both position and orientation information in the pulvinar: attended objects are encoded with high precision, while there is no measurable encoding of ignored objects. These data support a role of the pulvinar in distractor filtering--suppressing information from competing stimuli to isolate behaviourally relevant objects.


Responses of pulvinar neurons reflect a subject's confidence in visual categorization

Y. Komura and A. Nikkuni and N. Hirashima and T. Uetake and A. Miyamoto

Nat Neurosci  16  749-55  (2013)

When we recognize a sensory event, we experience a confident feeling that we certainly know the perceived world 'here and now'. However, it is unknown how and where the brain generates such 'perceptual confidence'. Here we found neural correlates of confidence in the primate pulvinar, a visual thalamic nucleus that has been expanding markedly through evolution. During a categorization task, the majority of pulvinar responses did not correlate with any 'perceptual content'. During an opt-out task, pulvinar responses decreased when monkeys chose 'escape' options, suggesting less confidence in their perceptual categorization. Functional silencing of the pulvinar increased monkeys' escape choices in the opt-out task without affecting categorization performance; this effect was specific to the contralateral visual target. These data were supported by a theoretical model of confidence, indicating that pulvinar activities encode a subject's certainty of visual categorization and contribute to perceptual confidence.