Ga Keliris

Decorrelated Neuronal Firing in Cortical Microcircuits

Columns, Connections, and Correlations What is the nature of interactions between neurons in neural circuits? The prevalent hypothesis suggests that dense local connectivity causes nearby cortical neurons to receive substantial amounts of common input, which in turn leads to strong correlations between them. Now two studies challenge this view, which impacts our fundamental understanding of coding in the cortex. Ecker et al. (p. 584) investigated the statistics of correlated firing in pairs of neurons from area V1 of awake macaque monkeys. In contrast to previous studies, correlations turned out to be very low, irrespective of the stimulus being shown to the animals, the distances of the recording sites, and the similarity of the neurons receptive fields or response properties. In an accompanying modeling and recording paper, Renart et al. (p. 587) demonstrate how it is possible to have zero noise correlation, even among cells with common input. Despite dense connectivity and shared input, the firing rates of nearby neurons are largely uncorrelated. Correlated trial-to-trial variability in the activity of cortical neurons is thought to reflect the functional connectivity of the circuit. Many cortical areas are organized into functional columns, in which neurons are believed to be densely connected and to share common input. Numerous studies report a high degree of correlated variability between nearby cells. We developed chronically implanted multitetrode arrays offering unprecedented recording quality to reexamine this question in the primary visual cortex of awake macaques. We found that even nearby neurons with similar orientation tuning show virtually no correlated variability. Our findings suggest a refinement of current models of cortical microcircuit architecture and function: Either adjacent neurons share only a few percent of their inputs or, alternatively, their activity is actively decorrelated.

Functional MRI of the vocalization-processing network in the macaque brain

Using functional magnetic resonance imaging in awake behaving monkeys we investigated how species-specific vocalizations are represented in auditory and auditory-related regions of the macaque brain. We found clusters of active voxels along the ascending auditory pathway that responded to various types of complex sounds: inferior colliculus (IC), medial geniculate nucleus (MGN), auditory core, belt, and parabelt cortex, and other parts of the superior temporal gyrus (STG) and sulcus (STS). Regions sensitive to monkey calls were most prevalent in the anterior STG, but some clusters were also found in frontal and parietal cortex on the basis of comparisons between responses to calls and environmental sounds. Surprisingly, we found that spectrotemporal control sounds derived from the monkey calls (“scrambled calls”) also activated the parietal and frontal regions. Taken together, our results demonstrate that species-specific vocalizations in rhesus monkeys activate preferentially the auditory ventral stream, and in particular areas of the antero-lateral belt and parabelt.

Neurons in macaque area V4 acquire directional tuning after adaptation to motion stimuli

Neurons in area V4 of the macaque are generally not selective for direction of motion, as judged from their response to directional stimuli presented after a baseline condition devoid of movement. We used motion adaptation to investigate whether stimulation history influences direction-of-motion selectivity. We found that classically nondirectional V4 neurons develop direction-of-motion selectivity after adaptation, an observation that underscores the dynamic nature of functional cortical architecture.

Introduction to research topic – binocular rivalry: a gateway to studying consciousness

In 1593, Neapolitan polymath Giambattista della Porta publicly lamented that he was unable to improve his impressive productivity (he had published in areas as diverse as cryptography, hydraulics, pharmacology, optics, and classic fiction). Della Porta was trying to read two books simultaneously by placing both volumes side-by-side, and using each eye independently. To his great surprise, his setup allowed him to only read one book at a time. This discovery arguably marks the first written account of binocular rivalry (Wade, 2000) – a perceptual phenomenon that more than 400 years later still both serves to intrigue as well as to illuminate the limits of scientific knowledge. At first glance, binocular rivalry is an oddball. In every day vision, our eyes receive largely matching views of the world. The brain combines the two images into a cohesive scene, and concurrently, perception is stable. However, when showing two very different images (such as two different books) to each eye, the brain resolves the conflict by adopting a “diplomatic” strategy. Rather than mixing the views of the two eyes into an insensible visual percept, observers perceive a dynamically changing series of perceptual snapshots, with one eye’s view dominating for a few seconds before being replaced by its rival from the other eye. With prolonged viewing of a rivalrous stimulus, one inevitably experiences a sequence of subjective perceptual reversals, separated by random time intervals, and this process continues for as long as the sensory conflict is present.

Comparing the feature selectivity of the gamma-band of the local field potential and the underlying spiking activity in primate visual cortex

The local field potential (LFP), comprised of low-frequency extra-cellular voltage fluctuations, has been used extensively to study the mechanisms of brain function. In particular, oscillations in the gamma-band (30–90 Hz) are ubiquitous in the cortex of many species during various cognitive processes. Surprisingly little is known about the underlying biophysical processes generating this signal. Here, we examine the relationship of the local field potential to the activity of localized populations of neurons by simultaneously recording spiking activity and LFP from the primary visual cortex (V1) of awake, behaving macaques. The spatial organization of orientation tuning and ocular dominance in this area provides an excellent opportunity to study this question, because orientation tuning is organized at a scale around one order of magnitude finer than the size of ocular dominance columns. While we find a surprisingly weak correlation between the preferred orientation of multi-unit activity and gamma-band LFP recorded on the same tetrode, there is a strong correlation between the ocular preferences of both signals. Given the spatial arrangement of orientation tuning and ocular dominance, this leads us to conclude that the gamma-band of the LFP seems to sample an area considerably larger than orientation columns. Rather, its spatial resolution lies at the scale of ocular dominance columns.

Feature selectivity of the gamma-band of the local field potential in primate primary visual cortex.

Extracellular voltage fluctuations (local field potentials, LFPs) reflecting neural mass action are ubiquitous across species and brain regions. Numerous studies have characterized the properties of LFP signals in the cortex to study sensory and motor computations as well as cognitive processes like attention, perception and memory. In addition, its extracranial counterpart – the electroencephalogram – is widely used in clinical applications. However, the link between LFP signals and the underlying activity of local populations of neurons remains largely elusive. Here, we review recent work elucidating the relationship between spiking activity of local neural populations and LFP signals. We focus on oscillations in the gamma-band (30–90 Hz) of the LFP in the primary visual cortex (V1) of the macaque that dominate during visual stimulation. Given that in area V1 much is known about the properties of single neurons and the cortical architecture, it provides an excellent opportunity to study the mechanisms underlying the generation of the LFP.

The Role of the Primary Visual Cortex in Perceptual Suppression of Salient Visual Stimuli

The role of primary visual cortex (area V1) in subjective perception has intrigued students of vision for decades. Specifically, the extent to which the activity of different types of cells (monocular versus binocular) and electrophysiological signals (i.e., local field potentials versus spiking activity) reflect perception is still debated. To address these questions we recorded from area V1 of the macaque using tetrodes during the paradigm of binocular flash suppression, where incongruent images presented dichoptically compete for perceptual dominance. We found that the activity of a minority (20%) of neurons reflect the perceived visual stimulus and these cells exhibited perceptual modulations substantially weaker compared with their sensory modulation induced by congruent stimuli. Importantly, perceptual modulations were found equally often for monocular and binocular cells, demonstrating that perceptual competition in V1 involves mechanisms across both types of neurons. The power of the local field potential (LFP) also showed moderate perceptual modulations with similar percentages of sites showing significant effects across frequency bands (18–22%). The possibility remains that perception may be strongly reflected in more elaborate aspects of activity in V1 circuits (e.g., specific neuronal subtypes) or perceptual states might have a modulatory role on more intricate aspects of V1 firing patterns (e.g., synchronization), not necessarily altering the firing rates of single cells or the LFP power dramatically.

Robust controlled functional MRI in alert monkeys at high magnetic field: Effects of jaw and body movements

The use of functional magnetic resonance imaging (fMRI) in alert non-human primates is of great potential for research in systems neuroscience. It can be combined with invasive techniques and afford better understanding of non-invasively acquired brain imaging signals in humans. However, the difficulties in optimal application of alert monkey fMRI are multi-faceted, especially at high magnetic fields where the effects of motion and of changes in B0 are greatly amplified. To overcome these difficulties, strict behavioral controls and elaborate animal-training are needed. Here, we introduce a number of hardware developments, quantify the effect of movements on fMRI data, and present procedures for animal training and scanning for well-controlled and artifact-reduced alert monkey fMRI at high magnetic field. In particular, we describe systems for monitoring jaw and body movements, and for accurately tracking eye movements. A link between body and jaw movement and MRI image artifacts is established, showing that relying on the immobilization of an animals head is not sufficient for high-quality imaging. Quantitative analysis showed that body and jaw movement events caused large instabilities in fMRI time series. On average, body movement events caused larger instabilities than jaw movement events. Residual baseline brain image position and signal amplitude shifts were observed after the jaw and body movement events ended. Based on these findings, we introduce a novel behavioral paradigm that relies on training the monkeys to stay still during long trials. A corresponding analysis method discards all data that were not obtained during the movement-free periods. The baseline position and amplitude shifts are overcome by motion correction and trial-by-trial signal normalization. The advantages of the presented method over conventional scanning and analysis are demonstrated with data obtained at 7 T. It is anticipated that the techniques presented here will prove useful for alert monkey fMRI at any magnetic field.

A new method for estimating population receptive field topography in visual cortex

We introduce a new method for measuring visual population receptive fields (pRF) with functional magnetic resonance imaging (fMRI). The pRF structure is modeled as a set of weights that can be estimated by solving a linear model that predicts the Blood Oxygen Level-Dependent (BOLD) signal using the stimulus protocol and the canonical hemodynamic response function. This method does not make a priori assumptions about the specific pRF shape and is therefore a useful tool for uncovering the underlying pRF structure at different spatial locations in an unbiased way. We show that our method is more accurate than a previously described method (Dumoulin and Wandell, 2008) which directly fits a 2-dimensional isotropic Gaussian pRF model to predict the fMRI time-series. We demonstrate that direct-fit models do not fully capture the actual pRF shape, and can be prone to pRF center mislocalization when the pRF is located near the border of the stimulus space. A quantitative comparison demonstrates that our method outperforms the direct-fit methods in the pRF center modeling by achieving higher explained variance of the BOLD signal. This was true for direct-fit isotropic Gaussian, anisotropic Gaussian, and difference of isotropic Gaussians model. Importantly, our model is also capable of exploring a variety of pRF properties such as surround suppression, receptive field center elongation, orientation, location and size. Additionally, the proposed method is particularly attractive for monitoring pRF properties in the visual areas of subjects with lesions of the visual pathways, where it is difficult to anticipate what shape the reorganized pRF might take. Finally, the method proposed here is more efficient in computation time than direct-fit methods, which need to search for a set of parameters in an extremely large searching space. Instead, this method uses the pRF topography to constrain the space that needs to be searched for the subsequent modeling.

Population receptive field analysis of the primary visual cortex complements perimetry in patients with homonymous visual field defects

Significance Partial damage of the primary visual cortex (V1), or damage to the white matter inputs to V1 (optic radiation), cause blindness in specific regions of the visual field. We use functional MRI to measure responses in individual patients with a localized, chronic V1 injury that resulted in blindness in a quarter of the visual field. The fMRI responses of patients and controls are generally similar, but in some patients differences from controls can be measured. Importantly, responses in spared early visual cortex are not always congruent with visual perception. Understanding how the properties of early visual areas respond to injury will lead to better strategies for visual rehabilitation. Injury to the primary visual cortex (V1) typically leads to loss of conscious vision in the corresponding, homonymous region of the contralateral visual hemifield (scotoma). Several studies suggest that V1 is highly plastic after injury to the visual pathways, whereas others have called this conclusion into question. We used functional magnetic resonance imaging (fMRI) to measure area V1 population receptive field (pRF) properties in five patients with partial or complete quadrantic visual field loss as a result of partial V1+ or optic radiation lesions. Comparisons were made with healthy controls deprived of visual stimulation in one quadrant [“artificial scotoma” (AS)]. We observed no large-scale changes in spared-V1 topography as the V1/V2 border remained stable, and pRF eccentricity versus cortical-distance plots were similar to those of controls. Interestingly, three observations suggest limited reorganization: (i) the distribution of pRF centers in spared-V1 was shifted slightly toward the scotoma border in 2 of 5 patients compared with AS controls; (ii) pRF size in spared-V1 was slightly increased in patients near the scotoma border; and (iii) pRF size in the contralesional hemisphere was slightly increased compared with AS controls. Importantly, pRF measurements yield information about the functional properties of spared-V1 cortex not provided by standard perimetry mapping. In three patients, spared-V1 pRF maps overlapped significantly with dense regions of the perimetric scotoma, suggesting that pRF analysis may help identify visual field locations amenable to rehabilitation. Conversely, in the remaining two patients, spared-V1 pRF maps failed to cover sighted locations in the perimetric map, indicating the existence of V1-bypassing pathways able to mediate useful vision.