Neural substrate for the engagement of the ventral visual stream in motor control in the macaque monkey.

The present study aimed to describe the cortical connectivity of a sector located in the ventral bank of the superior temporal sulcus in the macaque (intermediate area TEa and TEm [TEa/m]), which appears to represent the major source of output of the ventral visual stream outside the temporal lobe. The retrograde tracer wheat germ agglutinin was injected in the intermediate TEa/m in four macaque monkeys. The results showed that 58-78% of labeled cells were located within ventral visual stream areas other than the TE complex. Outside the ventral visual stream, there were connections with the memory-related medial temporal area 36 and the parahippocampal cortex, orbitofrontal areas involved in encoding subjective values of stimuli for action selection, and eye- or hand-movement related parietal (LIP, AIP, and SII), prefrontal (12r, 45A, and 45B) areas, and a hand-related dysgranular insula field. Altogether these data provide a solid substrate for the engagement of the ventral visual stream in large scale cortical networks for skeletomotor or oculomotor control. Accordingly, the role of the ventral visual stream could go beyond pure perceptual processes and could be also finalized to the neural mechanisms underlying the control of voluntary motor behavior.

Bilateral connections from the amygdala to extrastriate visual cortex in the marmoset monkey.

It is known that the primate amygdala forms projections to many areas of the ipsilateral cortex, but the extent to which it forms connections with the contralateral visual cortex remains less understood. Based on retrograde tracer injections in marmoset monkeys, we report that the amygdala forms widespread projections to the ipsilateral extrastriate cortex, including V1 and areas in both the dorsal (MT, V4T, V3a, 19M, and PG/PFG) and the ventral (VLP and TEO) streams. In addition, contralateral projections were found to target each of the extrastriate areas, but not V1. In both hemispheres, the tracer-labeled neurons were exclusively located in the basolateral nuclear complex. The number of labeled neurons in the contralateral amygdala was small relative to the ipsilateral connection (1.2% to 5.8%). The percentage of contralateral connections increased progressively with hierarchical level. An injection in the corpus callosum demonstrated that at least some of the amygdalo-cortical connections cross through this fiber tract, in addition to the previously documented path through the anterior commissure. Our results expand knowledge of the amygdalofugal projections to the extrastriate cortex, while also revealing pathways through which visual stimuli conveying affective content can directly influence early stages of neural processing in the contralateral visual field.

Chromatic processing and receptive-field structure in neurons of the anterior optic tract of the honeybee brain.

Color vision in honeybees is a well-documented perceptual phenomenon including multiple behavioral tests of trichromaticity and color opponency. Data on the combined color/space properties of high order visual neurons in the bee brain is however limited. Here we fill this gap by analyzing the activity of neurons in the anterior optic tract (AOT), a high order brain region suggested to be involved in chromatic processing. The spectral response properties of 72 units were measured using UV, blue and green light stimuli presented in 266 positions of the visual field. The majority of these units comprise combined chromatic-spatial processing properties. We found eight different neuron categories in terms of their spectral, spatial and temporal response properties. Color-opponent neurons, the most abundant neural category in the AOT, present large receptive fields and activity patterns that were typically opponent between UV and blue or green, particularly during the on-tonic response phase. Receptive field shapes and activity patterns of these color processing neurons are more similar between blue and green, than between UV and blue or green. We also identified intricate spatial antagonism and double spectral opponency in some receptive fields of color-opponent units. Stimulation protocols with different color combinations applied to 21 AOT units allowed us to uncover additional levels of spectral antagonism and hidden inhibitory inputs, even in some units that were initially classified as broad-band neurons based in their responses to single spectral lights. The results are discussed in the context of floral color discrimination and celestial spectral gradients.

Retinal Connectomics: A Review.

The retina is an ideal model for understanding the fundamental rules for how neural networks are constructed. The compact neural networks of the retina perform all of the initial processing of visual information before transmission to higher visual centers in the brain. The field of retinal connectomics uses high-resolution electron microscopy datasets to map the intricate organization of these networks and further our understanding of how these computations are performed by revealing the fundamental topologies and allowable networks behind retinal computations. In this article, we review some of the notable advances that retinal connectomics has provided in our understanding of the specific cells and the organization of their connectivities within the retina, as well as how these are shaped in development and break down in disease. Using these anatomical maps to inform modeling has been, and will continue to be, instrumental in understanding how the retina processes visual signals.

Cortical and subcortical intraoperative-monitoring of the visual pathway under general anesthesia in epilepsy surgery.

OBJECTIVE: The purpose of this study was to evaluate the applicability of visual evoked potentials (VEP) for intraoperative visual pathway monitoring in epilepsy surgery of the posterior hemispheric quadrant (PHQ) and to correlate it with post-operative visual field status. METHODS: VEP monitoring was performed in 16 patients (12 females, 7 children). Flash-induced VEP were recorded with strip electrodes from the banks of the calcarine cortex. Latency and amplitude of the first component of VEP (V1-lat, V1-amp) were monitored. Evaluation of the visual field was performed pre- and post-operatively in all patients. RESULTS: All procedures were successfully completed without adverse events. In 10 patients the strip covered both the inferior and superior calcarine banks, while only one bank was sampled in 6 cases (inferior in 4, superior in 2). Considering one of the two calcarine banks, at the end of the resection VEP had disappeared in 4 patients, whereas a decrease >33.3% in 4 and <20% of V1-amp was recorded in 5 and in 4 cases respectively. The percentage of V1-amp reduction was significantly higher for the patients who experienced a post-operative visual field reduction (p < 0.001). Post-operative visual field deficits were found in patients presenting a reduction >33.3% of V1-amp. CONCLUSIONS: VEP monitoring is possible and safe in epilepsy surgery under general anesthesia. SIGNIFICANCE: Intraoperative recording of VEP from the banks of the calcarine cortex allows monitoring the integrity of post-geniculate visual pathways during PHQ resections for epilepsy and it is pivotal to prevent disabling visual field defects, including hemianopia and inferior quadrantanopia.

The big mixup: Neural representation during natural modes of primate visual behavior.

The primate brain has evolved specialized visual capacities to navigate complex physical and social environments. Researchers studying cortical circuits underlying these capacities have traditionally favored the use of simplified tasks and brief stimulus presentations in order to isolate cognitive variables with tight experimental control. As a result, operational theories about visual brain function have come to emphasize feature detection, hierarchical stimulus encoding, top-down task modulation, and functional segregation in distinct cortical areas. Recently, however, experimental paradigms combining natural behavior with electrophysiological recordings have begun to offer a distinctly different portrait of how the brain takes in and analyzes its visual surroundings. The present article reviews recent work in this area, highlighting some of the more surprising findings in domains of social vision and spatial navigation along with shifts in thinking that have begun to emanate from this approach.

Cooperative thalamocortical circuit mechanism for sensory prediction errors.

The brain functions as a prediction machine, utilizing an internal model of the world to anticipate sensations and the outcomes of our actions. Discrepancies between expected and actual events, referred to as prediction errors, are leveraged to update the internal model and guide our attention towards unexpected events1-10. Despite the importance of prediction-error signals for various neural computations across the brain, surprisingly little is known about the neural circuit mechanisms responsible for their implementation. Here we describe a thalamocortical disinhibitory circuit that is required for generating sensory prediction-error signals in mouse primary visual cortex (V1). We show that violating animals' predictions by an unexpected visual stimulus preferentially boosts responses of the layer 2/3 V1 neurons that are most selective for that stimulus. Prediction errors specifically amplify the unexpected visual input, rather than representing non-specific surprise or difference signals about how the visual input deviates from the animal's predictions. This selective amplification is implemented by a cooperative mechanism requiring thalamic input from the pulvinar and cortical vasoactive-intestinal-peptide-expressing (VIP) inhibitory interneurons. In response to prediction errors, VIP neurons inhibit a specific subpopulation of somatostatin-expressing inhibitory interneurons that gate excitatory pulvinar input to V1, resulting in specific pulvinar-driven response amplification of the most stimulus-selective neurons in V1. Therefore, the brain prioritizes unpredicted sensory information by selectively increasing the salience of unpredicted sensory features through the synergistic interaction of thalamic input and neocortical disinhibitory circuits.

Retinal Input Is Required for the Maintenance of Neuronal Laminae in the Ventrolateral Geniculate Nucleus.

Retinal ganglion cell (RGC) axons provide direct input into several brain regions, including the dorsal lateral geniculate nucleus (dLGN), which is important for image-forming vision, and the ventrolateral geniculate nucleus (vLGN), which is associated with nonimage-forming vision. Through both activity- and morphogen-dependent mechanisms, retinal inputs play important roles in the development of dLGN, including the refinement of retinal projections, morphological development of thalamocortical relay cells (TRCs), timing of corticogeniculate innervation, and recruitment and distribution of inhibitory interneurons. In contrast, little is known about the role of retinal inputs in the development of vLGN. Grossly, vLGN is divided into two domains, the retinorecipient external vLGN (vLGNe) and nonretinorecipient internal vLGN (vLGNi). Studies previously found that vLGNe consists of transcriptionally distinct GABAergic subtypes distributed into at least four adjacent laminae. At present, it remains unclear whether retinal inputs influence the development of these cell-type-specific neuronal laminae in vLGNe. Here, we elucidated the developmental timeline for these laminae in the mouse vLGNe, and results indicate that these laminae are specified at or before birth. We observed that mutant mice without retinal inputs have a normal laminar distribution of GABAergic cells at birth; however, after the first week of postnatal development, these mutants exhibited a dramatic disruption in the laminar organization of inhibitory neurons and clear boundaries between vLGNe and vLGNi. Overall, our results show that while the formation of cell-type-specific layers in mouse vLGNe does not depend on RGC inputs, retinal signals are critical for their maintenance.

Signatures of hierarchical temporal processing in the mouse visual system.

A core challenge for the brain is to process information across various timescales. This could be achieved by a hierarchical organization of temporal processing through intrinsic mechanisms (e.g., recurrent coupling or adaptation), but recent evidence from spike recordings of the rodent visual system seems to conflict with this hypothesis. Here, we used an optimized information-theoretic and classical autocorrelation analysis to show that information- and correlation timescales of spiking activity increase along the anatomical hierarchy of the mouse visual system under visual stimulation, while information-theoretic predictability decreases. Moreover, intrinsic timescales for spontaneous activity displayed a similar hierarchy, whereas the hierarchy of predictability was stimulus-dependent. We could reproduce these observations in a basic recurrent network model with correlated sensory input. Our findings suggest that the rodent visual system employs intrinsic mechanisms to achieve longer integration for higher cortical areas, while simultaneously reducing predictability for an efficient neural code.

Primate brain: A unique connection between dorsal and ventral visual cortex.

In humans and other primates, vision is subserved by at least two parallel processing streams that are interconnected through a pathway known as the vertical occipital fasciculus. New research reveals that this white matter pathway may be a unique feature of the primate brain.

A circuit motif for color in the human foveal retina.

The neural pathways that start human color vision begin in the complex synaptic network of the foveal retina where signals originating in long (L), middle (M), and short (S) wavelength-sensitive cone photoreceptor types are compared through antagonistic interactions, referred to as opponency. In nonhuman primates, two cone opponent pathways are well established: an L vs. M cone circuit linked to the midget ganglion cell type, often called the red-green pathway, and an S vs. L + M cone circuit linked to the small bistratified ganglion cell type, often called the blue-yellow pathway. These pathways have been taken to correspond in human vision to cardinal directions in a trichromatic color space, providing the parallel inputs to higher-level color processing. Yet linking cone opponency in the nonhuman primate retina to color mechanisms in human vision has proven particularly difficult. Here, we apply connectomic reconstruction to the human foveal retina to trace parallel excitatory synaptic outputs from the S-ON (or "blue-cone") bipolar cell to the small bistratified cell and two additional ganglion cell types: a large bistratified ganglion cell and a subpopulation of ON-midget ganglion cells, whose synaptic connections suggest a significant and unique role in color vision. These two ganglion cell types are postsynaptic to both S-ON and L vs. M opponent midget bipolar cells and thus define excitatory pathways in the foveal retina that merge the cardinal red-green and blue-yellow circuits, with the potential for trichromatic cone opponency at the first stage of human vision.

Heterogeneous orientation tuning in the primary visual cortex of mice diverges from Gabor-like receptive fields in primates.

A key feature of neurons in the primary visual cortex (V1) of primates is their orientation selectivity. Recent studies using deep neural network models showed that the most exciting input (MEI) for mouse V1 neurons exhibit complex spatial structures that predict non-uniform orientation selectivity across the receptive field (RF), in contrast to the classical Gabor filter model. Using local patches of drifting gratings, we identified heterogeneous orientation tuning in mouse V1 that varied up to 90° across sub-regions of the RF. This heterogeneity correlated with deviations from optimal Gabor filters and was consistent across cortical layers and recording modalities (calcium vs. spikes). In contrast, model-synthesized MEIs for macaque V1 neurons were predominantly Gabor like, consistent with previous studies. These findings suggest that complex spatial feature selectivity emerges earlier in the visual pathway in mice than in primates. This may provide a faster, though less general, method of extracting task-relevant information.

Decoding dynamic visual scenes across the brain hierarchy.

Understanding the computational mechanisms that underlie the encoding and decoding of environmental stimuli is a crucial investigation in neuroscience. Central to this pursuit is the exploration of how the brain represents visual information across its hierarchical architecture. A prominent challenge resides in discerning the neural underpinnings of the processing of dynamic natural visual scenes. Although considerable research efforts have been made to characterize individual components of the visual pathway, a systematic understanding of the distinctive neural coding associated with visual stimuli, as they traverse this hierarchical landscape, remains elusive. In this study, we leverage the comprehensive Allen Visual Coding-Neuropixels dataset and utilize the capabilities of deep learning neural network models to study neural coding in response to dynamic natural visual scenes across an expansive array of brain regions. Our study reveals that our decoding model adeptly deciphers visual scenes from neural spiking patterns exhibited within each distinct brain area. A compelling observation arises from the comparative analysis of decoding performances, which manifests as a notable encoding proficiency within the visual cortex and subcortical nuclei, in contrast to a relatively reduced encoding activity within hippocampal neurons. Strikingly, our results unveil a robust correlation between our decoding metrics and well-established anatomical and functional hierarchy indexes. These findings corroborate existing knowledge in visual coding related to artificial visual stimuli and illuminate the functional role of these deeper brain regions using dynamic stimuli. Consequently, our results suggest a novel perspective on the utility of decoding neural network models as a metric for quantifying the encoding quality of dynamic natural visual scenes represented by neural responses, thereby advancing our comprehension of visual coding within the complex hierarchy of the brain.

Sub-bundle based analysis reveals the role of human optic radiation in visual working memory.

White matter (WM) functional activity has been reliably detected through functional magnetic resonance imaging (fMRI). Previous studies have primarily examined WM bundles as unified entities, thereby obscuring the functional heterogeneity inherent within these bundles. Here, for the first time, we investigate the function of sub-bundles of a prototypical visual WM tract-the optic radiation (OR). We use the 7T retinotopy dataset from the Human Connectome Project (HCP) to reconstruct OR and further subdivide the OR into sub-bundles based on the fiber's termination in the primary visual cortex (V1). The population receptive field (pRF) model is then applied to evaluate the retinotopic properties of these sub-bundles, and the consistency of the pRF properties of sub-bundles with those of V1 subfields is evaluated. Furthermore, we utilize the HCP working memory dataset to evaluate the activations of the foveal and peripheral OR sub-bundles, along with LGN and V1 subfields, during 0-back and 2-back tasks. We then evaluate differences in 2bk-0bk contrast between foveal and peripheral sub-bundles (or subfields), and further examine potential relationships between 2bk-0bk contrast and 2-back task d-prime. The results show that the pRF properties of OR sub-bundles exhibit standard retinotopic properties and are typically similar to the properties of V1 subfields. Notably, activations during the 2-back task consistently surpass those under the 0-back task across foveal and peripheral OR sub-bundles, as well as LGN and V1 subfields. The foveal V1 displays significantly higher 2bk-0bk contrast than peripheral V1. The 2-back task d-prime shows strong correlations with 2bk-0bk contrast for foveal and peripheral OR fibers. These findings demonstrate that the blood oxygen level-dependent (BOLD) signals of OR sub-bundles encode high-fidelity visual information, underscoring the feasibility of assessing WM functional activity at the sub-bundle level. Additionally, the study highlights the role of OR in the top-down processes of visual working memory beyond the bottom-up processes for visual information transmission. Conclusively, this study innovatively proposes a novel paradigm for analyzing WM fiber tracts at the individual sub-bundle level and expands understanding of OR function.

Top-down modulation of the retinal code via histaminergic neurons of the hypothalamus.

The mammalian retina is considered an autonomous circuit, yet work dating back to Ramon y Cajal indicates that it receives inputs from the brain. How such inputs affect retinal processing has remained unknown. We confirmed brain-to-retina projections of histaminergic neurons from the mouse hypothalamus. Histamine application ex vivo altered the activity of various retinal ganglion cells (RGCs), including direction-selective RGCs that gained responses to high motion velocities. These results were reproduced in vivo with optic tract recordings where histaminergic retinopetal axons were activated chemogenetically. Such changes could improve vision of fast-moving objects (e.g., while running), which fits with the known increased activity of histaminergic neurons during arousal. An antihistamine drug reduced optomotor responses to high-speed moving stimuli in freely moving mice. In humans, the same antihistamine nonuniformly modulated visual sensitivity across the visual field, indicating an evolutionary conserved function of the histaminergic system. Our findings expose a previously unappreciated role for brain-to-retina projections in modulating retinal function.

Retinotopy drives the variation in scene responses across visual field map divisions of the occipital place area.

The occipital place area (OPA) is a scene-selective region on the lateral surface of human occipitotemporal cortex that spatially overlaps multiple visual field maps, as well as portions of cortex that are not currently defined as retinotopic. Here we combined population receptive field modeling and responses to scenes in a representational similarity analysis (RSA) framework to test the prediction that the OPA's visual field map divisions contribute uniquely to the overall pattern of scene selectivity within the OPA. Consistent with this prediction, the patterns of response to a set of complex scenes were heterogeneous between maps. To explain this heterogeneity, we tested the explanatory power of seven candidate models using RSA. These models spanned different scene dimensions (Content, Expanse, Distance), low- and high-level visual features, and navigational affordances. None of the tested models could account for the variation in scene response observed between the OPA's visual field maps. However, the heterogeneity in scene response was correlated with the differences in retinotopic profiles across maps. These data highlight the need to carefully examine the relationship between regions defined as category-selective and the underlying retinotopy, and they suggest that, in the case of the OPA, it may not be appropriate to conceptualize it as a single scene-selective region.

Microglia are dispensable for experience-dependent refinement of mouse visual circuitry.

To test the hypothesized crucial role of microglia in the developmental refinement of neural circuitry, we depleted microglia from mice of both sexes with PLX5622 and examined the experience-dependent maturation of visual circuitry and function. We assessed retinal function, receptive field tuning of visual cortex neurons, acuity and experience-dependent plasticity. None of these measurements detectibly differed in the absence of microglia, challenging the role of microglia in sculpting neural circuits.

Hue and orientation pinwheels in macaque area V4.

Area V4 is an intermediate-level area of the macaque visual cortical hierarchy that serves key functions in visual processing by integrating inputs from lower areas such as V1 and V2 and providing feedforward inputs to many higher cortical areas. Previous V4 imaging studies have focused on differential responses to color, orientation, disparity, and motion stimuli, but many details of the spatial organization of significant hue and orientation tuning have not been fully described. We used support vector machine (SVM) decoding of intrinsic cortical single-condition responses to generate high-resolution maps of hue and orientation tuning and to describe the organization of hue and orientation pinwheels in V4. Like V1 and V2, V4 contains maps of orientation that are organized as pinwheels. V4 also contains maps of hue that are organized as pinwheels, whose circular organization more closely represents the perception of hue than is observed in antecedent cortical areas. Unlike V1, where orientation is continuously mapped across the surface, V4 hue and orientation pinwheels are organized in limited numbers of pinwheel sequences. The organization of these sequences and the distance between pinwheels may provide insight into the functional organization of V4. Regions significantly tuned for hue occupy roughly four times that of the orientation, are largely separated from each other, and overlap by roughly 5%. This spatial organization is largely consistent with segregated inputs arising from V2 thin and interstripes. This modular organization of V4 suggests that further integration of color and shape might occur in higher areas in inferotemporal cortical.NEW & NOTEWORTHY The representation of hue and orientation in macaque monkey area V4 was determined by intrinsic cortical imaging of responses to isoluminant hues and achromatic grating stimuli. Vector summation of support vector machine (SVM) decoded single-condition responses was used to generate hue and orientation maps that, like V1 orientation maps, were both characterized by distinct pinwheel patterns. These data suggest that pinwheels are an important structure to represent different stimulus features across multiple visual cortical areas.

Orientation selectivity mapping in the visual cortex.

The orientation map is one of the most well-studied functional maps of the visual cortex. However, results from the literature are of different qualities. Clear boundaries among different orientation domains and blurred uncertain distinctions were shown in different studies. These unclear imaging results will lead to an inaccuracy in depicting cortical structures, and the lack of consideration in experimental design will also lead to biased depictions of the cortical features. How we accurately define orientation domains will impact the entire field of research. In this study, we test how spatial frequency (SF), stimulus size, location, chromatic, and data processing methods affect the orientation functional maps (including a large area of dorsal V4, and parts of dorsal V1) acquired by intrinsic signal optical imaging. Our results indicate that, for large imaging fields, large grating stimuli with mixed SF components should be considered to acquire the orientation map. A diffusion model image enhancement based on the difference map could further improve the map quality. In addition, the similar outcomes of achromatic and chromatic gratings indicate two alternative types of afferents from LGN, pooling in V1 to generate cue-invariant orientation selectivity.

Diversity of visual inputs to Kenyon cells of the Drosophila mushroom body.

The arthropod mushroom body is well-studied as an expansion layer representing olfactory stimuli and linking them to contingent events. However, 8% of mushroom body Kenyon cells in Drosophila melanogaster receive predominantly visual input, and their function remains unclear. Here, we identify inputs to visual Kenyon cells using the FlyWire adult whole-brain connectome. Input repertoires are similar across hemispheres and connectomes with certain inputs highly overrepresented. Many visual neurons presynaptic to Kenyon cells have large receptive fields, while interneuron inputs receive spatially restricted signals that may be tuned to specific visual features. Individual visual Kenyon cells randomly sample sparse inputs from combinations of visual channels, including multiple optic lobe neuropils. These connectivity patterns suggest that visual coding in the mushroom body, like olfactory coding, is sparse, distributed, and combinatorial. However, the specific input repertoire to the smaller population of visual Kenyon cells suggests a constrained encoding of visual stimuli.