The Role of Pulvinar in the Transmission of Information in the Visual Hierarchy

Visual receptive field (RF) attributes in visual cortex of primates have been explained mainly from cortical connections: visual RFs progress from simple to complex through cortico-cortical pathways from lower to higher levels in the visual hierarchy. This feedforward flow of information is paired with top-down processes through the feedback pathway. Although the hierarchical organization explains the spatial properties of RFs, is unclear how a non-linear transmission of activity through the visual hierarchy can yield smooth contrast response functions in all level of the hierarchy. Depending on the gain, non-linear transfer functions create either a bimodal response to contrast, or no contrast dependence of the response in the highest level of the hierarchy. One possible mechanism to regulate this transmission of visual contrast information from low to high level involves an external component that shortcuts the flow of information through the hierarchy. A candidate for this shortcut is the Pulvinar nucleus of the thalamus. To investigate representation of stimulus contrast a hierarchical model network of ten cortical areas is examined. In each level of the network, the activity from the previous layer is integrated and then non-linearly transmitted to the next level. The arrangement of interactions creates a gradient from simple to complex RFs of increasing size as one moves from lower to higher cortical levels. The visual input is modeled as a Gaussian random input, whose width codes for the contrast. This input is applied to the first area. The output activity ratio among different contrast values is analyzed for the last level to observe sensitivity to a contrast and contrast invariant tuning. For a purely cortical system, the output of the last area can be approximately contrast invariant, but the sensitivity to contrast is poor. To account for an alternative visual processing pathway, non-reciprocal connections from and to a parallel pulvinar like structure of nine areas is coupled to the system. Compared to the pure feedforward model, cortico-pulvino-cortical output presents much more sensitivity to contrast and has a similar level of contrast invariance of the tuning

Pulvinar thalamic nucleus allows for asynchronous spike propagation through the cortex

We create two multilayered feedforward networks composed of excitatoryand inhibitory integrate-and-fire neurons in the balanced state toinvestigate the role of cortico-pulvino-cortical connections. Thefirst network consists of ten feedforward levels where a Poisson spiketrain with varying firing rate is applied as an input in layerone. Although the balanced state partially avoids spikesynchronization during the transmission, the average firing-rate in the last layer either decays or saturates depending on the feedforwardpathway gain. The last layer activity is almost independent of the inputeven for a carefully chosen intermediate gain. Adding connectionsto the feedforward pathway by a nine areas Pulvinar structure improves the firing-rate propagation to become almost linear amonglayers. Incoming strong pulvinar spikes balance the low feedforwardgain to have a unit input-output relation in the last layer. Pulvinarneurons evoke a bimodal activity depending on the magnitude input: synchronized spike bursts between 20-80 Hz and an asynchronous activityfor very both low and high frequency inputs. In the first regime, spikes of last feedforward layer neurons areasynchronous with weak, low frequency, oscillations in the rate. Here,the uncorrelated incoming feedforward pathway washes out thesynchronized thalamic bursts. In the second regime, spikes in the wholenetwork are asynchronous. As the number of cortical layers increases,long-range pulvinar connections can link directly two or morecortical stages avoiding their either saturation or gradual activityfalling. The Pulvinar acts as a shortcut that supplies theinput-output firing-rate relationship of two separated cortical areaswithout changing the strength of connections in the feedforwardpathway

A laminar organization for selective cortico-cortical communication

The neocortex is central to mammalian cognitive ability, playing critical roles in sensory perception, motor skills and executive function. This thin, layered structure comprises distinct, functionally specialized areas that communicate with each other through the axons of pyramidal neurons. For the hundreds of such cortico-cortical pathways to underlie diverse functions, their cellular and synaptic architectures must differ so that they result in distinct computations at the target projection neurons. In what ways do these pathways differ? By originating and terminating in different laminae, and by selectively targeting specific populations of excitatory and inhibitory neurons, these “interareal” pathways can differentially control the timing and strength of synaptic inputs onto individual neurons, resulting in layer-specific computations. Due to the rapid development in transgenic techniques, the mouse has emerged as a powerful mammalian model for understanding the rules by which cortical circuits organize and function. Here we review our understanding of how cortical lamination constrains long-range communication in the mammalian brain, with an emphasis on the mouse visual cortical network. We discuss the laminar architecture underlying interareal communication, the role of neocortical layers in organizing the balance of excitatory and inhibitory actions, and highlight the structure and function of layer 1 in mouse visual cortex

Towards a Unified View on Pathways and Functions of Neural Recurrent Processing

There are three neural feedback pathways to the primary visual cortex (V1): corticocortical, pulvinocortical, and cholinergic. What are the respective functions of these three projections? Possible functions range from contextual modulation of stimulus processing and feedback of high-level information to predictive processing (PP). How are these functions subserved by different pathways and can they be integrated into an overarching theoretical framework? We propose that corticocortical and pulvinocortical connections are involved in all three functions, whereas the role of cholinergic projections is limited by their slow response to stimuli. PP provides a broad explanatory framework under which stimulus-context modulation and high-level processing are subsumed, involving multiple feedback pathways that provide mechanisms for inferring and interpreting what sensory inputs are about

Impact of the pulvinar on the ventral pathway of the cat visual cortex

Signals from the retina are relayed to the lateral geniculate nucleus from which they are sent to the primary visual cortex. At the cortical level, the information is transferred across several visual areas in which the complexity of the processing increases progressively. Anatomical and functional evidence demonstrate the existence of two main pathways in visual cortex processing distinct features of the visual information: the dorsal and ventral streams. Cortical areas composing the dorsal stream are implicated mostly in motion processing while those comprising the ventral stream are involved in the processing of form and colour. This classic view of the cortical functional organization is challenged by the existence of reciprocal connections of visual cortical areas with the thalamic nucleus named pulvinar. These connections allow the creation of a trans-thalamic pathway that parallels the cortico-cortical communications across the visual hierarchy. The main goal of the present thesis is twofold: first, to obtain a better comprehension of the processing of light increments and decrements in an area of the cat ventral stream (area 21a); second, to characterize the nature of the thalamo-cortical inputs from the cat lateral posterior nucleus (LP) to area 21a. In study #1, we investigated the spatiotemporal response profile of neurons from area 21a to light increments (brights) and decrements (darks) using a reverse correlation analysis of a sparse noise stimulus. Our findings showed that 21a neurons exhibited stronger responses to darks with receptive fields exhibiting larger dark subfields. However, no differences were found between the temporal dynamics of brights and darks. In comparison with the primary visual cortex, the dark preference in area 21a was found to be strongly enhanced, supporting the notion that the asymmetries between brights and darks are transmitted and amplified along the ventral stream. In study #2, we investigated the impact of the reversible pharmacological inactivation of the LP nucleus on the contrast response function (CRF) of neurons from area 21a and the primary visual cortex (area 17). The thalamic inactivation yielded distinct effects on both cortical areas. While in area 17 the LP inactivation caused a slight decrease in the response gain, in area 21a a strong increase was observed. Thus, our findings suggest that the LP exerts a modulatory influence on the cortical processing along the ventral stream with stronger impact on higher order extrastriate areas. Taken together, our findings allowed a better comprehension of the functional properties of the cat ventral stream and contributed to the current knowledge on the role of the pulvinar on the cortico-thalamo-cortical processing of visual information.Les signaux provenant de la rétine sont relayés dans le corps géniculé latéral où ils sont envoyés au cortex visuel primaire. L’information passe ensuite à travers plusieurs aires visuelles où la complexité du traitement augmente progressivement. Des données tant anatomiques que fonctionnelles ont démontré l’existence de deux voies principales qui traitent différentes propriétés de l’information visuelle : les voies dorsale et ventrale. Les aires corticales composant la voie dorsale sont impliquées principalement dans le traitement du mouvement tandis que les aires de la voie ventrale sont impliquées dans le traitement de la forme et de la couleur. Cette vision classique de l’organisation fonctionnelle du cortex est toutefois remise en question par l’existence de connections réciproques entre les aires corticales visuelles et le pulvinar, un noyau thalamique. En effet, ces connections permettent la création d’une voie trans-thalamique parallèle aux connections cortico-corticales à travers la hiérarchie visuelle. Le but principal de la présente thèse consiste en deux volets : le premier est d’obtenir une meilleure compréhension du traitement des incréments et décréments de la lumière dans une aire de la voie ventrale du chat (aire 21a); le second est de caractériser la nature des inputs thalamo-corticaux du noyau latéral postérieur (LP) à l’aire 21a chez le chat. Dans l’étude #1, nous avons investigué le profil spatiotemporel des réponses des neurones de l’aire 21a aux incréments (blancs) et décréments (noirs) de lumière en utilisant l’analyse de corrélation inverse d’un stimulus de bruit épars. Les neurones de l’aire 21a ont répondu plus fortement aux stimuli noirs, en montrant des champs récepteurs avec des sous-champs noirs plus larges. Cependant, aucune différence n’a été trouvée en ce qui concerne les dynamiques temporelles des réponses aux blancs et aux noirs. En comparaison avec le cortex visuel primaire, la préférence aux stimuli noirs dans l’aire 21a s’est avérée fortement augmentée. Ces données indiquent que les asymétries entre les réponses aux blancs et aux noirs sont transmises et amplifiées à travers la voie ventrale. Dans l’étude #2, nous avons investigué l’impact de l’inactivation pharmacologique réversible du noyau LP sur la fonction de réponse au contraste (CRF) des neurones de l’aire 21a et du cortex visuel primaire (aire 17). L’inactivation a eu différents effets dans les deux aires corticales. Alors que, dans l’aire 17, l’inactivation du LP a causé une légère réduction du gain de la réponse, une forte augmentation a été observée dans l’aire 21a. Ainsi, nos résultats suggèrent que le LP exerce une influence modulatrice dans le traitement cortical à travers la voie ventrale avec un impact plus important dans des aires extrastriées de plus haut niveau. Nos résultats ont permis d’avoir une meilleure compréhension des propriétés fonctionnelles de la voie ventrale du chat et de contribuer à enrichir les connaissances actuelles sur le rôle du pulvinar dans le traitement cortico-thalamo-cortical de l’information visuelle

Functional neuroanatomy of visual pathways involving the pulvinar

Les neurones du cortex visuel primaire (V1) peuvent emprunter deux voies de communications afin d’atteindre les aires extrastriées : une voie cortico-corticale, et une voie cortico-thalamo-corticale à travers des noyaux thalamiques de haut niveau (HO) comme le pulvinar. Les fonctions respectives de ces deux voies restent toujours méconnues. Un pas vers une meilleure compréhension de celles-ci seraient d’investiguer la nature des signaux qu’elles transmettent. Dans ce contexte, deux grands types de projections cortico-thalamiques (CT) ont été identifiés dans le système visuel : les neurones de type I (modulator) et type II (driver) caractérisés respectivement par des axones minces dotés de petits boutons terminaux et par des axones plus épais et de plus grands boutons respectivement. Une proposition récente a aussi émis l'hypothèse que ces deux types pourraient également être distingués par leur expression de transporteur de glutamate vésiculaire. Cette hypothèse suggère que les projections de type II et de type I peuvent exprimer sélectivement VGLUT2 et VGLUT1, respectivement (Balaram, 2013; Rovo et al, 2012). Chez le chat, les projections de V1 vers le pulvinar se composent principalement de terminaux de type II, tandis que celles de l’aire PMLS présentent une combinaison de terminaux de type I et II suggérant ainsi que, la proportion de terminaux de type I augmente avec le niveau hiérarchique cortical des zones visuelles. Afin de tester cette hypothèse, nous avons cartographié la distribution des terminaux CT du cortex AEV (article 1) ainsi que de l’aire 21a (article 2). Nous avons aussi étudié l’expression de VGLUT 1 et 2 dans le système visuel du chat afin de tester si leurs expressions corrèlent avec les sites de projections de neurones de type I et II (article 3). Nos résultats indiquent que la grande majorité des terminaux marqués dans le pulvinar provenant de l’AEV et de l’aire 21a sont de type I (Article 1 et 2) alors que ceux de V1 sont majoritairement de type II. Une comparaison de la proportion des projections de type I à travers les aires V1, PMLS, 21a et AEV révèlent une corrélation positive de sorte que celle-ci augmente avec le degré hiérarchique des aires visuelles. Nos résultats indiquent que VGLUT 1 et 2 présentent une distribution complémentaire et que leur localisation dans des sites connus pour recevoir une projection de type ‘modulateur’ et ‘déclencheur’ proéminente suggère que leurs expressions peuvent montrer un biais pour celles-ci dans la voie géniculo-strié. Les résultats de cette thèse ont permis de mieux connaitre la nature des projections CT des aires visuelles extrastriées. Ces résultats sont d’autant plus importants qu’ils établissent un lien entre la nature de ces projections et le degré hiérarchique des aires visuelles, suggérant ainsi l’existence une organisation anatomofonctionnelle des voies CT passant par le pulvinar. Enfin, les résultats de cette thèse ont aussi permis une meilleure compréhension des vésicules VGLUT 1 et 2 dans le système visuel du chat et leurs affinités respectives pour les sites de projections de neurones de type I et II.Visual signals from the primary visual cortex (V1), can take two main communication routes in order to reach higher visual areas: a corticocortical pathway and a cortico-thalamo-cortical (or transthalamic) pathway through high-order thalamic nuclei such as the pulvinar. While these pathways are receiving an increasing interest from the scientific community, their respective functions still remain largely unknown. An important step towards a better understanding of these pathways would be to investigate the nature of the signals they transmit. In this context, two main types of corticothalamic (CT) projections have been identified in the visual system: type I projections (modulators) and type II (drivers) characterized respectively by thin axons with small terminal and by thicker axons and larger terminals. A recent proposal has also hypothesized that these two types can also be distinguished by their expression of vesicular glutamate transporter (VGLUT) in their respective synaptic terminals such that type II (driver) and type I (modulator) projections can selectively express VGLUT 2 and VGLUT 1, respectively (Balaram, 2013; Rovo et al, 2012). In cats, projections from V1 to the LP-pulvinar are mainly composed of type II terminals, while those from the Posteromedial lateral suprasylvian (PMLS) cortex present a combination of type I and II terminals. This observation suggests that, in higher-order (HO) thalamic nuclei, the proportion of type I terminals increases with the hierarchical level of the visual areas. To test this hypothesis, we charted the distribution of CT terminals originating from the Anterior EctoSylvian visual cortex (AEV) (article 1) and from area 21a (article 2). We also studied the expression of VGLUT 1 and 2 in the cat's visual system in order to test whether their expressions correlate with the projection sites of type I and II axon terminals (article 3). Our results from article 1 and 2 indicate that the vast majority of terminals sampled in the pulvinar from the AEV and area 21a are of type I while projections from V1 projections to the pulvinar were mostly composed of type II terminals. A comparison of the proportion of type I projections across areas V1, PMLS, 21a and the AEV revealed a positive correlation such that its proportion increased with the hierarchical rank of visual areas. Our results also indicate that VGLUT 1 and 2 have a complementary distribution pattern which matches prominent projection of type I and II respectively in ascending visual projections but does not in extra-geniculate pathways involving the pulvinar (Article 3). Taken together, results from this thesis have allowed a better understanding of the nature of cortico-thalamic projections originating from extra-striate visual areas (21a and AEV). These results are all the more important in that they establish a link between the nature of these projections and the hierarchical degree of their cortical area of origin, thus suggesting that there is a functional organization of CT pathways passing through the pulvinar. Finally, results of this thesis also enabled a better understanding of the expression of VGLUT 1 and 2 in the visual system and their possible respective biases for type I and type II projections

Seeing the invisible: The scope and limits of unconscious processing in binocular rivalry

When an image is presented to one eye and a very different image is presented to the corresponding location of the other eye, they compete for conscious representation, such that only one image is visible at a time while the other is suppressed. Called binocular rivalry, this phenomenon and its deviants have been extensively exploited to study the mechanism and neural correlates of consciousness. In this paper, we propose a framework, the unconscious binding hypothesis, to distinguish unconscious processing from conscious processing. According to this framework, the unconscious mind not only encodes individual features but also temporally binds distributed features to give rise to cortical representation, but unlike conscious binding, such unconscious binding is fragile. Under this framework, we review evidence from psychophysical and neuroimaging studies, which suggests that: (1) for invisible low level features, prolonged exposure to visual pattern and simple translational motion can alter the appearance of subsequent visible features (i.e. adaptation); for invisible high level features, although complex spiral motion cannot produce adaptation, nor can objects/words enhance subsequent processing of related stimuli (i.e. priming), images of tools can nevertheless activate the dorsal pathway; and (2) although invisible central cues cannot orient attention, invisible erotic pictures in the periphery can nevertheless guide attention, likely through emotional arousal; reciprocally, the processing of invisible information can be modulated by attention at perceptual and neural levels