Laminar fMRI: applications for cognitive neuroscience

The cortex is a massively recurrent network, characterized by feedforward and feedback connections between brain areas as well as lateral connections within an area. Feedforward, horizontal and feedback responses largely activate separate layers of a cortical unit, meaning they can be dissociated by lamina-resolved neurophysiological techniques. Such techniques are invasive and are therefore rarely used in humans. However, recent developments in high spatial resolution fMRI allow for non-invasive, in vivo measurements of brain responses specific to separate cortical layers. This provides an important opportunity to dissociate between feedforward and feedback brain responses, and investigate communication between brain areas at a more fine- grained level than previously possible in the human species. In this review, we highlight recent studies that successfully used laminar fMRI to isolate layer-specific feedback responses in human sensory cortex. In addition, we review several areas of cognitive neuroscience that stand to benefit from this new technological development, highlighting contemporary hypotheses that yield testable predictions for laminar fMRI. We hope to encourage researchers with the opportunity to embrace this development in fMRI research, as we expect that many future advancements in our current understanding of human brain function will be gained from measuring lamina-specific brain responses

A feedback model of visual attention

Feedback connections are a prominent feature of cortical anatomy and are likely to have significant functional role in neural information processing. We present a neural network model of cortical feedback that successfully simulates neurophysiological data associated with attention. In this domain our model can be considered a more detailed, and biologically plausible, implementation of the biased competition model of attention. However, our model is more general as it can also explain a variety of other top-down processes in vision, such as figure/ground segmentation and contextual cueing. This model thus suggests that a common mechanism, involving cortical feedback pathways, is responsible for a range of phenomena and provides a unified account of currently disparate areas of research

Contributions of cortical feedback to sensory processing in primary visual cortex

Closing the structure-function divide is more challenging in the brain than in any other organ (Lichtman and Denk, 2011). For example, in early visual cortex, feedback projections to V1 can be quantified (e.g., Budd, 1998) but the understanding of feedback function is comparatively rudimentary (Muckli and Petro, 2013). Focusing on the function of feedback, we discuss how textbook descriptions mask the complexity of V1 responses, and how feedback and local activity reflects not only sensory processing but internal brain states

Cortical Spike Synchrony as a Measure of Input Familiarity

J.G.O. was supported by the Ministerio de Economia y Competividad and FEDER (Spain, project FIS2015-66503-C3-1-P) and the ICREA Academia programme. E.U. acknowledges support from the Scottish Universities Life Sciences Alliance (SULSA) and HPC-Europa2.Peer reviewedPostprin

The reentry hypothesis: The putative interaction of the frontal eye field, ventrolateral prefrontal cortex, and areas V4, IT for attention and eye movement

Attention is known to play a key role in perception, including action selection, object recognition and memory. Despite findings revealing competitive interactions among cell populations, attention remains difficult to explain. The central purpose of this paper is to link up a large number of findings in a single computational approach. Our simulation results suggest that attention can be well explained on a network level involving many areas of the brain. We argue that attention is an emergent phenomenon that arises from reentry and competitive interactions. We hypothesize that guided visual search requires the usage of an object-specific template in prefrontal cortex to sensitize V4 and IT cells whose preferred stimuli match the target template. This induces a feature-specific bias and provides guidance for eye movements. Prior to an eye movement, a spatially organized reentry from occulomotor centers, specifically the movement cells of the frontal eye field, occurs and modulates the gain of V4 and IT cells. The processes involved are elucidated by quantitatively comparing the time course of simulated neural activity with experimental data. Using visual search tasks as an example, we provide clear and empirically testable predictions for the participation of IT, V4 and the frontal eye field in attention. Finally, we explain a possible physiological mechanism that can lead to non-flat search slopes as the result of a slow, parallel discrimination process

State Dependence of Stimulus-Induced Variability Tuning in Macaque MT

Behavioral states marked by varying levels of arousal and attention modulate some properties of cortical responses (e.g. average firing rates or pairwise correlations), yet it is not fully understood what drives these response changes and how they might affect downstream stimulus decoding. Here we show that changes in state modulate the tuning of response variance-to-mean ratios (Fano factors) in a fashion that is neither predicted by a Poisson spiking model nor changes in the mean firing rate, with a substantial effect on stimulus discriminability. We recorded motion-sensitive neurons in middle temporal cortex (MT) in two states: alert fixation and light, opioid anesthesia. Anesthesia tended to lower average spike counts, without decreasing trial-to-trial variability compared to the alert state. Under anesthesia, within-trial fluctuations in excitability were correlated over longer time scales compared to the alert state, creating supra-Poisson Fano factors. In contrast, alert-state MT neurons have higher mean firing rates and largely sub-Poisson variability that is stimulus-dependent and cannot be explained by firing rate differences alone. The absence of such stimulus-induced variability tuning in the anesthetized state suggests different sources of variability between states. A simple model explains state-dependent shifts in the distribution of observed Fano factors via a suppression in the variance of gain fluctuations in the alert state. A population model with stimulus-induced variability tuning and behaviorally constrained information-limiting correlations explores the potential enhancement in stimulus discriminability by the cortical population in the alert state.Comment: 36 pages, 18 figure

Occlusion-related lateral connections stabilize kinetic depth stimuli through perceptual coupling

Local sensory information is often ambiguous forcing the brain to integrate spatiotemporally separated information for stable conscious perception. Lateral connections between clusters of similarly tuned neurons in the visual cortex are a potential neural substrate for the coupling of spatially separated visual information. Ecological optics suggests that perceptual coupling of visual information is particularly beneficial in occlusion situations. Here we present a novel neural network model and a series of human psychophysical experiments that can together explain the perceptual coupling of kinetic depth stimuli with activity-driven lateral information sharing in the far depth plane. Our most striking finding is the perceptual coupling of an ambiguous kinetic depth cylinder with a coaxially presented and disparity defined cylinder backside, while a similar frontside fails to evoke coupling. Altogether, our findings are consistent with the idea that clusters of similarly tuned far depth neurons share spatially separated motion information in order to resolve local perceptual ambiguities. The classification of far depth in the facilitation mechanism results from a combination of absolute and relative depth that suggests a functional role of these lateral connections in the perception of partially occluded objects

Visual adaptation to convexity in macaque area V4

Aftereffects are perceptual illusions caused by visual adaptation to one or more stimulus attribute, such as orientation, motion, or shape. Neurophysiological studies seeking to understand the basis of visual adaptation have observed firing rate reduction and changes in tuning of stimulus-selective neurons following periods of prolonged visual stimulation. In the domain of shape, recent psychophysical work has shown that adaptation to a convex pattern induces a subsequently seen rectangle to appear slightly concave. In the present study, we investigate the possible contribution of V4 neurons of rhesus monkeys, which are thought to be involved in the coding of convexity, to shape-specific adaptation. Visually responsive neurons were monitored during the brief presentation of simple shapes varying in their convexity level. Each test presentation was preceded by either a blank period or several seconds of adaptation to a convex or concave stimulus, presented in two different sizes. Adaptation consistently shifted the tuning of neurons away from the convex or concave adapter, including shifting response to the neutral rectangle in the direction of the opposite convexity. This repulsive shift resembled the known perceptual distortion associated with adaptation to such stimuli. In addition, adaptation caused a nonspecific response decrease, as well as a specific decrease for repeated stimuli. The latter effects were observed whether or not the adapting and test stimuli matched closely in their size. Taken together, these results provide evidence for shape-specific adaptation of neurons in area V4, which may contribute to the perception of the convexity aftereffect

Contextual modulation of primary visual cortex by auditory signals

Early visual cortex receives non-feedforward input from lateral and top-down connections (Muckli & Petro 2013 Curr. Opin. Neurobiol. 23, 195–201. (doi:10.1016/j.conb.2013.01.020)), including long-range projections from auditory areas. Early visual cortex can code for high-level auditory information, with neural patterns representing natural sound stimulation (Vetter et al. 2014 Curr. Biol. 24, 1256–1262. (doi:10.1016/j.cub.2014.04.020)). We discuss a number of questions arising from these findings. What is the adaptive function of bimodal representations in visual cortex? What type of information projects from auditory to visual cortex? What are the anatomical constraints of auditory information in V1, for example, periphery versus fovea, superficial versus deep cortical layers? Is there a putative neural mechanism we can infer from human neuroimaging data and recent theoretical accounts of cortex? We also present data showing we can read out high-level auditory information from the activation patterns of early visual cortex even when visual cortex receives simple visual stimulation, suggesting independent channels for visual and auditory signals in V1. We speculate which cellular mechanisms allow V1 to be contextually modulated by auditory input to facilitate perception, cognition and behaviour. Beyond cortical feedback that facilitates perception, we argue that there is also feedback serving counterfactual processing during imagery, dreaming and mind wandering, which is not relevant for immediate perception but for behaviour and cognition over a longer time frame. This article is part of the themed issue ‘Auditory and visual scene analysis’