Selective representations of texture and motion in mouse higher visual areas

Mice have a constellation of higher visual areas, but their functional specializations are unclear. Here, we used a data-driven approach to examine neuronal representations of complex visual stimuli across mouse higher visual areas, measured using large field-of-view two-photon calcium imaging. Using specialized stimuli, we found higher fidelity representations of texture in area LM, compared to area AL. Complementarily, we found higher fidelity representations of motion in area AL, compared to area LM. We also observed this segregation of information in response to naturalistic videos. Finally, we explored how popular models of visual cortical neurons could produce the segregated representations of texture and motion we observed. These selective representations could aid in behaviors such as visually guided navigation.

Functional connectomics spanning multiple areas of mouse visual cortex

The value of an integrated approach for understanding the neocortex by combining functional characterization of single neuron activity with the underlying circuit architecture has been understood since the dawn of modern neuroscience. However, in practice, anatomical connectivity and physiology have been studied mostly separately. Following in the footsteps of previous studies that have combined physiology and anatomy in the same tissue, here we present a unique functional connectomics dataset that contains calcium imaging of an estimated 75,000 neurons from primary visual cortex (VISp) and three higher visual areas (VISrl, VISal and VISlm), that were recorded while a mouse viewed natural movies and parametric stimuli. The functional data were co-registered with electron microscopy (EM) data of the same volume which were automatically segmented, reconstructing more than 200,000 cells (neuronal and non-neuronal) and 524 million synapses. Subsequent proofreading of some neurons in this volume yielded reconstructions that include complete dendritic trees as well the local and inter-areal axonal projections. The largest proofread excitatory axon reached a length of 19 mm and formed 1,893 synapses, while the largest inhibitory axon formed 10,081 synapses. Here we release this dataset as an open access resource to the scientific community including a set of analysis tools that allows easy data access, both programmatically and through a web user interface.

The essential role of recurrent processing for figure-ground perception in mice

The segregation of figures from the background is an important step in visual perception. In primary visual cortex, figures evoke stronger activity than backgrounds during a delayed phase of the neuronal responses, but it is unknown how this figure-ground modulation (FGM) arises and whether it is necessary for perception. Here, we show, using optogenetic silencing in mice, that the delayed V1 response phase is necessary for figure-ground segregation. Neurons in higher visual areas also exhibit FGM and optogenetic silencing of higher areas reduced FGM in V1. In V1, figures elicited higher activity of vasoactive intestinal peptide–expressing (VIP) interneurons than the background, whereas figures suppressed somatostatin-positive interneurons, resulting in an increased activation of pyramidal cells. Optogenetic silencing of VIP neurons reduced FGM in V1, indicating that disinhibitory circuits contribute to FGM. Our results provide insight into how lower and higher areas of the visual cortex interact to shape visual perception.

Effects of muscarinic and nicotinic receptors on contextual modulation in macaque area V1

Context affects the salience and visibility of image elements in visual scenes. Collinear flankers can enhance or decrease the perceptual and neuronal sensitivity to flanked stimuli. These effects are mediated through lateral interactions between neurons in the primary visual cortex (area V1), in conjunction with feedback from higher visual areas. The strength of lateral interactions is affected by cholinergic neuromodulation. Blockade of muscarinic receptors should increase the strength of lateral intracortical interactions, while nicotinic blockade should reduce thalamocortical feed-forward drive. Here we test this proposal through local iontophoretic application of the muscarinic receptor antagonist scopolamine and the nicotinic receptor antagonist mecamylamine, while recording single cells in parafoveal representations in awake fixating macaque V1. Collinear flankers generally reduced neuronal contrast sensitivity. Muscarinic and nicotinic receptor blockade equally reduced neuronal contrast sensitivity. Contrary to our hypothesis, flanker interactions were not systematically affected by either receptor blockade.

Dynamics of absolute and relative disparity processing in human visual cortex

Cortical processing of binocular disparity is believed to begin in V1 where cells are sensitive to absolute disparity, followed by the extraction of relative disparity in higher visual areas. While much is known about the cortical distribution and spatial tuning of disparity-selective neurons, the relationship between their spatial and temporal properties is less well understood. Here, we use steady-state Visual Evoked Potentials and dynamic random dot stereograms to characterize the temporal dynamics of spatial mechanisms in human visual cortex that are primarily sensitive to either absolute or relative disparity. Stereograms alternated between disparate and non-disparate states at 2 Hz. By varying the spatial frequency content of the disparate fields from a planar surface to corrugated ones, we biased responses towards absolute vs. relative disparities. Reliable Components Analysis was used to derive two dominant sources from the 128 channel EEG records. The first component (RC1) was maximal over the occipital pole while the second component (RC2) was maximal over right lateral occipital electrodes. In RC1, first harmonic responses were sustained, tuned for corrugation frequency, and sensitive to the presence of disparity references, consistent with prior psychophysical sensitivity measurements. By contrast, the second harmonic, associated with transient processing, was not spatially tuned and was indifferent to references, consistent with it being generated by an absolute disparity mechanism. In RC2, the sustained response component showed similar tuning and sensitivity to references. However, sensitivity for absolute disparity dropped off, and transient signals were mainly driven by the lowest corrugation frequencies.

Increased region of surround stimulation enhances contextual feedback and feedforward processing in human V1

The majority of synaptic inputs to the primary visual cortex (V1) are non-feedforward, instead originating from local and anatomical feedback connections. Animal electrophysiology experiments show that feedback signals originating from higher visual areas with larger receptive fields modulate the surround receptive fields of V1 neurons. Theories of cortical processing propose various roles for feedback and feedforward processing, but systematically investigating their independent contributions to cortical processing is challenging because feedback and feedforward processes coexist even in single neurons. Capitalising on the larger receptive fields of higher visual areas compared to primary visual cortex (V1), we used an occlusion paradigm that isolates top-down influences from feedforward processing. We utilised functional magnetic resonance imaging (fMRI) and multi-voxel pattern analysis methods in humans viewing natural scene images. We parametrically measured how the availability of contextual information determines the presence of detectable feedback information in non-stimulated V1, and how feedback information interacts with feedforward processing. We show that increasing the visibility of the contextual surround increases scene-specific feedback information, and that this contextual feedback enhances feedforward information. Our findings are in line with theories that cortical feedback signals transmit internal models of predicted inputs.

Spatial modulation of visual responses arises in cortex with active navigation

During navigation, the visual responses of neurons in mouse primary visual cortex (V1) are modulated by the animal’s spatial position. Here we show that this spatial modulation is similarly present across multiple higher visual areas but negligible in the main thalamic pathway into V1. Similar to hippocampus, spatial modulation in visual cortex strengthens with experience and with active behavior. Active navigation in a familiar environment, therefore, enhances the spatial modulation of visual signals starting in the cortex.

Fine-scale computations for adaptive processing in the human brain

Adapting to the environment statistics by reducing brain responses to repetitive sensory information is key for efficient information processing. Yet, the fine-scale computations that support this adaptive processing in the human brain remain largely unknown. Here, we capitalise on the sub-millimetre resolution of ultra-high field imaging to examine functional magnetic resonance imaging signals across cortical depth and discern competing hypotheses about the brain mechanisms (feedforward vs. feedback) that mediate adaptive processing. We demonstrate layer-specific suppressive processing within visual cortex, as indicated by stronger BOLD decrease in superficial and middle than deeper layers for gratings that were repeatedly presented at the same orientation. Further, we show altered functional connectivity for adaptation: enhanced feedforward connectivity from V1 to higher visual areas, short-range feedback connectivity between V1 and V2, and long-range feedback occipito-parietal connectivity. Our findings provide evidence for a circuit of local recurrent and feedback interactions that mediate rapid brain plasticity for adaptive information processing.

Binocular integration of retinal motion information underlies optic flow processing by the cortex

Locomotion creates various patterns of optic flow on the retina, which provide the observer with information about their movement relative to the environment. However, it is unclear how these optic flow patterns are encoded by the cortex. Here we use two-photon calcium imaging in awake mice to systematically map monocular and binocular responses to horizontal motion in four areas of the visual cortex. We find that neurons selective to translational or rotational optic flow are abundant in higher visual areas, whereas neurons suppressed by binocular motion are more common in the primary visual cortex. Disruption of retinal direction selectivity in Frmd7 mutant mice reduces the number of translation-selective neurons in the primary visual cortex, and translation- and rotation-selective neurons as well as binocular direction-selective neurons in the rostrolateral and anterior visual cortex, blurring the functional distinction between primary and higher visual areas. Thus, optic flow representations in specific areas of the visual cortex rely on binocular integration of motion information from the retina.