Yuri B. Saalmann

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

The Conductor in the Thalamus The pulvinar is the largest thalamic nucleus in the brain but its functions remain unclear. The pulvinar is ideally positioned to synchronize activity across the visual cortex. Saalmann et al. (p. 753) combined diffusion tensor imaging with multi-electrode recordings from three different brain areas in monkeys to probe thalamo-cortical interactions during visual attention. The pulvinar was found to play a vital role in attention by routing behaviorally relevant information across the visual cortex. A region of the thalamus synchronizes neuronal firing in two cortical areas and thus allocates attention. 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.

Neural Mechanisms of Visual Attention: How Top-Down Feedback Highlights Relevant Locations

Attention helps us process potentially important objects by selectively increasing the activity of sensory neurons that represent the relevant locations and features of our environment. This selection process requires top-down feedback about what is important in our environment. We investigated how parietal cortical output influences neural activity in early sensory areas. Neural recordings were made simultaneously from the posterior parietal cortex and an earlier area in the visual pathway, the medial temporal area, of macaques performing a visual matching task. When the monkey selectively attended to a location, the timing of activities in the two regions became synchronized, with the parietal cortex leading the medial temporal area. Parietal neurons may thus selectively increase activity in earlier sensory areas to enable focused spatial attention.

Cognitive and Perceptual Functions of the Visual Thalamus

The thalamus is classically viewed as passively relaying information to the cortex. However, there is growing evidence that the thalamus actively regulates information transmission to the cortex and between cortical areas using a variety of mechanisms, including the modulation of response magnitude, firing mode, and synchrony of neurons according to behavioral demands. We discuss how the visual thalamus contributes to attention, awareness, and visually guided actions, to present a general role for the thalamus in perception and cognition.

Intralaminar and medial thalamic influence on cortical synchrony, information transmission and cognition

The intralaminar and medial thalamic nuclei are part of the higher-order thalamus, which receives little sensory input, and instead forms extensive cortico-thalamo-cortical pathways. The large mediodorsal thalamic nucleus predominantly connects with the prefrontal cortex, the adjacent intralaminar nuclei connect with fronto-parietal cortex, and the midline thalamic nuclei connect with medial prefrontal cortex and medial temporal lobe. Taking into account this connectivity pattern, it is not surprising that the intralaminar and medial thalamus has been implicated in a variety of cognitive functions, including memory processing, attention and orienting, as well as reward-based behavior. This review addresses how the intralaminar and medial thalamus may regulate information transmission in cortical circuits. A key neural mechanism may involve intralaminar and medial thalamic neurons modulating the degree of synchrony between different groups of cortical neurons according to behavioral demands. Such a thalamic-mediated synchronization mechanism may give rise to large-scale integration of information across multiple cortical circuits, consequently influencing the level of arousal and consciousness. Overall, the growing evidence supports a general role for the higher-order thalamus in the control of cortical information transmission and cognitive processing.

Gain control in the visual thalamus during perception and cognition

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.

Functional and structural architecture of the human dorsal frontoparietal attention network

Significance Everyday actions require us to represent attentional priorities in different reference frames. For example, to pick up a cup of coffee, we need to know where the cup is relative to our body, and where the handle is relative to the cup (i.e., body-centered and object-centered reference frames). Multiple brain areas in frontal and parietal cortex help process attentional priorities. Although these areas are commonly conceptualized as an attentional network, it is not clear what neural pathways connect these areas, nor the pathways’ functions. We demonstrate that two pathways link these areas in frontal and parietal cortex. The pathways help represent attentional priorities in different reference frames, enabling us to flexibly interact with objects in our environment. The dorsal frontoparietal attention network has been subdivided into at least eight areas in humans. However, the circuitry linking these areas and the functions of different circuit paths remain unclear. Using a combination of neuroimaging techniques to map spatial representations in frontoparietal areas, their functional interactions, and structural connections, we demonstrate different pathways across human dorsal frontoparietal cortex for the control of spatial attention. Our results are consistent with these pathways computing object-centered and/or viewer-centered representations of attentional priorities depending on task requirements. Our findings provide an organizing principle for the frontoparietal attention network, where distinct pathways between frontal and parietal regions contribute to multiple spatial representations, enabling flexible selection of behaviorally relevant information.

Segregation of short-wavelength-sensitive (S) cone signals in the macaque dorsal lateral geniculate nucleus

An important problem in the study of the mammalian visual system is whether functionally different retinal ganglion cell types are anatomically segregated further up along the central visual pathway. It was previously demonstrated that, in a New World diurnal monkey (marmoset), the neurones carrying signals from the short‐wavelength‐sensitive (S) cones [blue–yellow (B/Y)‐opponent cells] are predominantly located in the koniocellular layers of the dorsal lateral geniculate nucleus (LGN), whereas the red–green (R/G)‐opponent cells carrying signals from the medium‐ and long‐wavelength‐sensitive cones are segregated in the parvocellular layers. Here, we used extracellular single‐unit recordings followed by histological reconstruction to investigate the distribution of color‐selective cells in the LGN of the macaque, an Old World diurnal monkey. Cells were classified using cone‐isolating stimuli to identify their cone inputs. Our results indicate that the majority of cells carrying signals from S‐cones are located either in the koniocellular layers or in the ‘koniocellular bridges’ that fully or partially span the parvocellular layers. By contrast, the R/G‐opponent cells are located in the parvocellular layers. We conclude that anatomical segregation of B/Y‐ and R/G‐opponent afferent signals for color vision is common to the LGNs of New World and Old World diurnal monkeys.

Spontaneous Neural Dynamics and Multi-scale Network Organization.

Spontaneous neural activity has historically been viewed as task-irrelevant noise that should be controlled for via experimental design, and removed through data analysis. However, electrophysiology and functional MRI studies of spontaneous activity patterns, which have greatly increased in number over the past decade, have revealed a close correspondence between these intrinsic patterns and the structural network architecture of functional brain circuits. In particular, by analyzing the large-scale covariation of spontaneous hemodynamics, researchers are able to reliably identify functional networks in the human brain. Subsequent work has sought to identify the corresponding neural signatures via electrophysiological measurements, as this would elucidate the neural origin of spontaneous hemodynamics and would reveal the temporal dynamics of these processes across slower and faster timescales. Here we survey common approaches to quantifying spontaneous neural activity, reviewing their empirical success, and their correspondence with the findings of neuroimaging. We emphasize invasive electrophysiological measurements, which are amenable to amplitude- and phase-based analyses, and which can report variations in connectivity with high spatiotemporal precision. After summarizing key findings from the human brain, we survey work in animal models that display similar multi-scale properties. We highlight that, across many spatiotemporal scales, the covariance structure of spontaneous neural activity reflects structural properties of neural networks and dynamically tracks their functional repertoire.

A minimally invasive and reversible system for chronic recordings from multiple brain sites in macaque monkeys.

We have developed a reversible system for performing simultaneous recordings from multiple brain areas of trained macaque monkeys. It consists of a near-circular halo fitted around the head of the monkey with 5-10 thin plastic or stainless steel posts that either jut against or are screwed into the skull, respectively. Both methods of implantation of the posts are easily reversible, enabling protracted recordings over many years and training the monkeys in more complex tasks. The former is more useful for shorter periods of recordings (2-4 months) separated by long intervals and the latter for longer periods of recordings at a time (6-12 months). With both systems, essentially the entire scalp is intact, allowing multi-site recordings from a number of dorsal cortical areas, as well as other areas, simultaneously. These recordings are performed through tiny craniotomies of usually less than 2mm diameter, which are fitted with small plastic cones that serve as guide tubes for the microelectrodes. The surgery involved in these procedures is relatively minor compared to classical methods and the implants are also usually free of infections, thus requiring little maintenance of recording chambers.

A Subcortical Pathway for Rapid, Goal-Driven, Attentional Filtering.

Prefrontal cortex can exercise goal-driven attentional control over sensory information via cortical pathways. However, recent work demonstrates that prefrontal cortex can also influence thalamic relay nuclei via the thalamic reticular nucleus. This suggests the prefrontal-thalamic pathway mediates rapid and goal-driven attentional filtering at the earliest stages of sensory processing.