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Summary Little is known about the internal circuitry of the primate lateral intraparietal area (LIP). During two versions of a delayed-saccade task, we found radically different network dynamics beneath similar population average firing patterns. When neurons are not influenced by stimuli outside their receptive fields (RFs), dynamics of the high-dimensional LIP network during slowly varying activity lie predominantly in one multi-neuronal dimension, as described previously. However, when activity is suppressed by stimuli outside the RF, slow LIP dynamics markedly deviate from a single dimension. The conflicting results can be reconciled if two LIP local networks, each underlying an RF location and dominated by a single multi-neuronal activity pattern, are suppressively coupled to each other. These results demonstrate the low dimensionality of slow LIP local dynamics, and suggest that LIP local networks encoding the attentional and movement priority of competing visual locations actively suppress one another. [ABSTRACT FROM AUTHOR]

Summary In primary visual cortex, a subset of neurons responds when a particular stimulus is encountered in a certain location in visual space. This activity can be modeled using a visual receptive field. In addition to visually driven activity, there are neurons in visual cortex that integrate visual and motor-related input to signal a mismatch between actual and predicted visual flow. Here we show that these mismatch neurons have receptive fields and signal a local mismatch between actual and predicted visual flow in restricted regions of visual space. These mismatch receptive fields are aligned to the retinotopic map of visual cortex and are similar in size to visual receptive fields. Thus, neurons with mismatch receptive fields signal local deviations of actual visual flow from visual flow predicted based on self-motion and could therefore underlie the detection of objects moving relative to the visual flow caused by self-motion. Video Abstract [ABSTRACT FROM AUTHOR]

Summary To deepen our understanding of object recognition, it is critical to understand the nature of transformations that occur in intermediate stages of processing in the ventral visual pathway, such as area V4. Neurons in V4 are selective to local features of global shape, such as extended contours. Previously, we found that V4 neurons selective for curved elements exhibit a high degree of spatial variation in their preference. If spatial variation in curvature selectivity was also marked by distinct temporal response patterns at different spatial locations, then it might be possible to untangle this information in subsequent processing based on temporal responses. Indeed, we find that V4 neurons whose receptive fields exhibit intricate selectivity also show variation in their temporal responses across locations. A computational model that decodes stimulus identity based on population responses benefits from using this temporal information, suggesting that it could provide a multiplexed code for spatio-temporal features. [ABSTRACT FROM AUTHOR]

Summary The primary visual cortex (V1) encodes a diverse set of visual features, including orientation, ocular dominance (OD), and spatial frequency (SF), whose joint organization must be precisely structured to optimize coverage within the retinotopic map. Prior experiments have only identified efficient coverage based on orthogonal maps. Here we used two-photon calcium imaging to reveal an alternative arrangement for OD and SF maps in macaque V1; their gradients run parallel but with unique spatial periods, whereby low-SF regions coincide with monocular regions. Next we mapped receptive fields and found surprisingly precise micro-retinotopy that yields a smaller point-image and requires more efficient inter-map geometry, thus underscoring the significance of map relationships. While smooth retinotopy is constraining, studies suggest that it improves both wiring economy and the V1 population code read downstream. Altogether, these data indicate that connectivity within V1 is finely tuned and precise at the level of individual neurons. [ABSTRACT FROM AUTHOR]

Summary Humans and monkeys have access to an accurate representation of visual space despite a constantly moving eye. One mechanism by which the brain accomplishes this is by remapping visual receptive fields around the time of a saccade. In this process a neuron can be excited by a probe stimulus in the current receptive field, and also simultaneously by a probe stimulus in the location that will be brought into the neuron’s receptive field by the saccade (the future receptive field), even before saccade begins. Here we show that perisaccadic neuronal excitability is not limited to the current and future receptive fields but encompasses the entire region of visual space across which the current receptive field will be swept by the saccade. A computational model shows that this receptive field expansion is consistent with the propagation of a wave of activity across the cerebral cortex as saccade planning and remapping proceed. [ABSTRACT FROM AUTHOR]

Summary Our tactile perception of external objects depends on skin-object interactions. The mechanics of contact dictates the existence of fundamental spatiotemporal input features—contact initiation and cessation, slip, and rolling contact—that originate from the fact that solid objects do not interpenetrate. However, it is unknown whether these features are represented within the brain. We used a novel haptic interface to deliver such inputs to the glabrous skin of finger/digit pads and recorded from neurons of the cuneate nucleus (the brain’s first level of tactile processing) in the cat. Surprisingly, despite having similar receptive fields and response properties, each cuneate neuron responded to a unique combination of these inputs. Hence, distinct haptic input features are encoded already at subcortical processing stages. This organization maps skin-object interactions into rich representations provided to higher cortical levels and may call for a re-evaluation of our current understanding of the brain’s somatosensory systems. [ABSTRACT FROM AUTHOR]

Summary: It is widely assumed that mosaics of retinal ganglion cells establish the optimal representation of visual space. However, relay cells in the visual thalamus often receive convergent input from several retinal afferents and, in cat, outnumber ganglion cells. To explore how the thalamus transforms the retinal image, we built a model of the retinothalamic circuit using experimental data and simple wiring rules. The model shows how the thalamus might form a resampled map of visual space with the potential to facilitate detection of stimulus position in the presence of sensor noise. Bayesian decoding conducted with the model provides support for this scenario. Despite its benefits, however, resampling introduces image blur, thus impairing edge perception. Whole-cell recordings obtained in vivo suggest that this problem is mitigated by arrangements of excitation and inhibition within the receptive field that effectively boost contrast borders, much like strategies used in digital image processing. [Copyright &y& Elsevier]

Summary: Functional maps in the cerebral cortex reorganize in response to changes in experience, but the synaptic underpinnings remain uncertain. Here, we demonstrate that layer (L) 2/3 pyramidal cell synapses in mouse barrel cortex can be potentiated upon pairing of whisker-evoked postsynaptic potentials (PSPs) with action potentials (APs). This spike-timing-dependent long-term potentiation (STD-LTP) was only effective for PSPs evoked by deflections of a whisker in the neuron’s receptive field center, and not its surround. Trimming of all except two whiskers rapidly opened the possibility to drive STD-LTP by the spared surround whisker. This facilitated STD-LTP was associated with a strong decrease in the surrounding whisker-evoked inhibitory conductance and partially occluded picrotoxin-mediated LTP facilitation. Taken together, our data demonstrate that sensory deprivation-mediated disinhibition facilitates STD-LTP from the sensory surround, which may promote correlation- and experience-dependent expansion of receptive fields. [Copyright &y& Elsevier]

“Receptive Fields, Binocular Interaction and Functional Architecture in the Cat''s Visual Cortex” by reported several important discoveries: orientation columns, the distinct structures of simple and complex receptive fields, and binocular integration. But perhaps the paper''s greatest influence came from the concept of functional architecture (the complex relationship between in vivo physiology and the spatial arrangement of neurons) and several models of functionally specific connectivity. They thus identified two distinct concepts, topographic specificity and functional specificity, which together with cell-type specificity constitute the major determinants of nonrandom cortical connectivity. Orientation columns are iconic examples of topographic specificity, whereby axons within a column connect with cells of a single orientation preference. Hubel and Wiesel also saw the need for functional specificity at a finer scale in their model of thalamic inputs to simple cells, verified in the 1990s. The difficult but potentially more important question of functional specificity between cortical neurons is only now becoming tractable with new experimental techniques. [Copyright &y& Elsevier]

Orientation selectivity in the primary visual cortex (V1) is a receptive field property that is at once simple enough to make it amenable to experimental and theoretical approaches and yet complex enough to represent a significant transformation in the representation of the visual image. As a result, V1 has become an area of choice for studying cortical computation and its underlying mechanisms. Here we consider the receptive field properties of the simple cells in cat V1—the cells that receive direct input from thalamic relay cells—and explore how these properties, many of which are highly nonlinear, arise. We have found that many receptive field properties of V1 simple cells fall directly out of Hubel and Wiesel''s feedforward model when the model incorporates realistic neuronal and synaptic mechanisms, including threshold, synaptic depression, response variability, and the membrane time constant. [Copyright &y& Elsevier]

Summary: Both human speech and animal vocal signals contain frequency-modulated (FM) sounds. Although central auditory neurons that selectively respond to the direction of frequency modulation are known, the synaptic mechanisms underlying the generation of direction selectivity (DS) remain elusive. Here we show the emergence of DS neurons in the inferior colliculus by mapping the three major subcortical auditory nuclei. Cell-attached recordings reveal a highly reliable and precise firing of DS neurons to FM sweeps in a preferred direction. By using in vivo whole-cell current-clamp and voltage-clamp recordings, we found that the synaptic inputs to DS neurons are not direction selective, but temporally reversed excitatory and inhibitory synaptic inputs are evoked in response to opposing directions of FM sweeps. The construction of such temporal asymmetry, resulting DS, and its topography can be attributed to the spectral disparity of the excitatory and the inhibitory synaptic tonal receptive fields. [ABSTRACT FROM AUTHOR]

Summary: Dendrites of the same neuron usually avoid each other. Some neurons also repel similar neurons through dendrite-dendrite interaction to tile the receptive field. Nonoverlapping coverage based on such contact-dependent repulsion requires dendrites to compete for limited space. Here we show that Drosophila class IV dendritic arborization (da) neurons, which tile the larval body wall, grow their dendrites mainly in a 2D space on the extracellular matrix (ECM) secreted by the epidermis. Removing neuronal integrins or blocking epidermal laminin production causes dendrites to grow into the epidermis, suggesting that integrin-laminin interaction attaches dendrites to the ECM. We further show that some of the previously identified tiling mutants fail to confine dendrites in a 2D plane. Expansion of these mutant dendrites in three dimensions results in overlap of dendritic fields. Moreover, overexpression of integrins in these mutant neurons effectively reduces dendritic crossing and restores tiling, revealing an additional mechanism for tiling. [ABSTRACT FROM AUTHOR]

The primary visual cortex has a map of multiple visual parameters whose topographic relations remain poorly understood. A new study ( Nauhaus et al., 2016 ) reveals a nearly geometric map-topography that coexists within a remarkably precise representation of visual space. [ABSTRACT FROM AUTHOR]

The claustrum, a subcortical nucleus forming extensive connections with the neocortex, has been implicated in sensory selection. Sensory-evoked claustrum activity is thought to modulate the neocortex's context-dependent response to sensory input. Recording from claustrum neurons while mice performed a tactile-visual sensory-selection task, we found that neurons in the anterior claustrum, including putative optotagged claustrocortical neurons projecting to the primary somatosensory cortex (S1), were rarely modulated by sensory input. Rather, they exhibited different types of direction-tuned motor responses. Furthermore, we found that claustrum neurons encoded upcoming movement during intertrial intervals and that pairs of claustrum neurons exhibiting synchronous firing were enriched for pairs preferring contralateral lick directions, suggesting that the activity of specific ensembles of similarly tuned claustrum neurons may modulate cortical activity. Chemogenetic inhibition of claustrocortical neurons decreased lick responses to inappropriate sensory stimuli. Altogether, our data indicate that the claustrum is integrated into higher-order premotor circuits recently implicated in decision-making. [Display omitted] • Anterior claustrum neurons exhibit motor responses • Claustrum neurons, including S1-projecting neurons, encode lick direction • Neuron pairs with synchronous firing during intertrial intervals are similarly tuned • Chemogenetic inhibition of claustrocortical neurons decreases false alarms Chevée, Finkel et al. show that the activity of neurons in the anterior claustrum recorded during a cross-modal sensory selection task reflects movement rather than sensory input. Premotor activity in individual claustrum neurons was biased for ipsilateral or contralateral movements and encoded upcoming lick direction during intertrial intervals. [ABSTRACT FROM AUTHOR]

Processing of sensory information in neural circuits is modulated by an animal's behavioral state, but the underlying cellular mechanisms are not well understood. Focusing on the mouse visual cortex, here we analyze the role of GABAergic interneurons that are located in layer 1 and express Ndnf (L1 NDNF INs) in the state-dependent control over sensory processing. We find that the ongoing and sensory-evoked activity of L1 NDNF INs is strongly enhanced when an animal is aroused and that L1 NDNF INs gain-modulate local excitatory neurons selectively during high-arousal states by inhibiting their apical dendrites while disinhibiting their somata via Parvalbumin -expressing interneurons. Because active NDNF INs are evenly spread in L1 and can affect excitatory neurons across all cortical layers, this indicates that the state-dependent activation of L1 NDNF INs and the subsequent shift of inhibition in excitatory neurons toward their apical dendrites gain-modulate sensory processing in whole cortical columns. [Display omitted] • Arousal strongly enhances the activity and sensory-evoked responses of L1 NDNF INs • L1 NDNF INs gain-modulate local EXC neurons selectively during high-arousal states • L1 NDNF INs inhibit the apical dendrites of EXC neurons and disinhibit their somata • Active NDNF INs are evenly spread across L1 and can affect EXC neurons in all layers Cohen-Kashi Malina et al. show that visual cortex L1 NDNF INs are strongly driven by arousal. Active NDNF INs are evenly spread in L1 and gain-modulate local excitatory neurons in all cortical layers during high-arousal states by directly inhibiting their apical dendrites while disinhibiting their somata via Parvalbumin -expressing interneurons. [ABSTRACT FROM AUTHOR]

When navigating the environment, animals need to prioritize responses to the most relevant stimuli. Although a theoretical framework for selective visual attention exists, its circuit implementation has remained obscure. Here we investigated how larval zebrafish select between simultaneously presented visual stimuli. We found that a mix of winner-take-all (WTA) and averaging strategies best simulates behavioral responses. We identified two circuits whose activity patterns predict the relative saliencies of competing visual objects. Stimuli presented to only one eye are selected by WTA computation in the inner retina. Binocularly presented stimuli, on the other hand, are processed by reciprocal, bilateral connections between the nucleus isthmi (NI) and the tectum. This interhemispheric computation leads to WTA or averaging responses. Optogenetic stimulation and laser ablation of NI neurons disrupt stimulus selection and behavioral action selection. Thus, depending on the relative locations of competing stimuli, a combination of retinotectal and isthmotectal circuits enables selective visual attention. • Zebrafish respond to competing stimuli using winner-take-all and averaging strategies • Retinotectal and isthmotectal circuits enable context-dependent stimulus selection • Perturbing nucleus isthmi function disrupts behavioral action selection • Isthmotectal circuit layout is consistent with local enhancement and global suppression Fernandes et al. investigate how zebrafish larvae respond selectively to one of two stimuli competing for the animal's attention. Two strategies for stimulus selection are used: winner-take-all or averaging. The corresponding neuronal computations are implemented in an intricate system of feedback loops between tectum and nucleus isthmi. [ABSTRACT FROM AUTHOR]

Single-cell RNA-sequencing and in vivo functional imaging provide expansive but disconnected views of neuronal diversity. Here, we developed a strategy for linking these modes of classification to explore molecular and cellular mechanisms responsible for detecting and encoding touch. By broadly mapping function to neuronal class, we uncovered a clear transcriptomic logic responsible for the sensitivity and selectivity of mammalian mechanosensory neurons. Notably, cell types with divergent gene-expression profiles often shared very similar properties, but we also discovered transcriptomically related neurons with specialized and divergent functions. Applying our approach to knockout mice revealed that Piezo2 differentially tunes all types of mechanosensory neurons with marked cell-class dependence. Together, our data demonstrate how mechanical stimuli recruit characteristic ensembles of transcriptomically defined neurons, providing rules to help explain the discriminatory power of touch. We anticipate a similar approach could expose fundamental principles governing representation of information throughout the nervous system. • Naturalistic mechanical stimuli activate large overlapping ensembles of neurons • In situ hybridization after functional imaging maps responses to cell class • Tuning properties of the classes reveal a transcriptomic basis for specialization • Mechanotransduction via Piezo2 contributes to almost all aspects of touch von Buchholtz et al. evaluate the representation of naturalistic mechanosensory stimuli by combining functional imaging with multigene in situ hybridization to determine gene expression profiles of large ensembles of trigeminal neurons. Their results expose a transcriptomic logic for touch discrimination and cell-class-specific roles for the Piezo2 ion channel. [ABSTRACT FROM AUTHOR]

High acuity stereopsis emerges during an early postnatal critical period when binocular neurons in the primary visual cortex sharpen their receptive field tuning properties. We find that this sharpening is achieved by dismantling the binocular circuit present at critical period onset and building it anew. Longitudinal imaging of receptive field tuning (e.g., orientation selectivity) of thousands of neurons reveals that most binocular neurons present in layer 2/3 at critical period onset are poorly tuned and are rendered monocular. In parallel, new binocular neurons are established by conversion of well-tuned monocular neurons as they gain matched input from the other eye. These improvements in binocular tuning in layer 2/3 are not inherited from layer 4 but are driven by the experience-dependent sharpening of ipsilateral eye responses. Thus, vision builds a new and more sharply tuned binocular circuit in layer 2/3 by cellular exchange and not by refining the original circuit. • Improvements in ipsilateral eye tuning change binocularity during the critical period • Poorly tuned binocular neurons are rendered monocular • Conversion of sharply tuned monocular neurons establishes new binocular neurons • Vision drives this sharpening and binocular conversion in layer 2/3 and not 4 Tan et al. demonstrate that visually evoked responses of binocular neurons improve across the critical period. This is caused by changing the cellular composition of the binocular pool. Poorly tuned binocular neurons become monocular, while sharply tuned monocular neurons gain matched responses to the other eye and become binocular. [ABSTRACT FROM AUTHOR]

Single-cell transcriptomics of neocortical neurons have revealed more than 100 clusters corresponding to putative cell types. For inhibitory and subcortical projection neurons (SCPNs), there is a strong concordance between clusters and anatomical descriptions of cell types. In contrast, cortico-cortical projection neurons (CCPNs) separate into surprisingly few transcriptomic clusters, despite their diverse anatomical projection types. We used projection-dependent single-cell transcriptomic analyses and monosynaptic rabies tracing to compare mouse primary visual cortex CCPNs projecting to different higher visual areas. We find that layer 2/3 CCPNs with different anatomical projections differ systematically in their gene expressions, despite forming only a single genetic cluster. Furthermore, these neurons receive feedback selectively from the same areas to which they project. These findings demonstrate that gene-expression analysis in isolation is insufficient to identify neuron types and have important implications for understanding the functional role of cortical feedback circuits. • V1 CCPNs display differential gene expression depending on their projections • V1 CCPNs receive feedback inputs from the same areas to which they project • Gene-expression analysis in isolation is insufficient to identify neuron types Kim et al. show that neuronal cell groups from within a single transcriptomic cluster can be further separated based on their anatomical projections and connectivity patterns. Connectivity is an important feature for cell-type identification. Gene expression alone cannot be used to fully annotate cortical cell types. [ABSTRACT FROM AUTHOR]

In the mammalian visual system, information from the retina streams into parallel bottom-up pathways. It remains unclear how these pathways interact to contribute to contextual modulation of visual cortical processing. By optogenetic inactivation and activation of mouse lateral posterior nucleus (LP) of thalamus, a homolog of pulvinar, or its projection to primary visual cortex (V1), we found that LP contributes to surround suppression of layer (L) 2/3 responses in V1 by driving L1 inhibitory neurons. This results in subtractive suppression of visual responses and an overall enhancement of orientation, direction, spatial, and size selectivity. Neurons in V1-projecting LP regions receive bottom-up input from the superior colliculus (SC) and respond preferably to non-patterned visual noise. The noise-dependent LP activity allows V1 to "cancel" noise effects and maintain its orientation selectivity under varying noise background. Thus, the retina-SC-LP-V1 pathway forms a differential circuit with the canonical retino-geniculate pathway to achieve context-dependent sharpening of visual representations. • LP enhances feature selectivity in V1 by providing subtractive surround suppression • This suppression is mediated by LP innervation of layer 1 inhibitory neurons in V1 • The bottom-up retina-SC-LP-V1 pathway constructs a differential visual circuit • LP helps V1 maintain its orientation selectivity under varying noise background Fang et al. show that the lateral posterior nucleus of thalamus, the rodent homolog of pulvinar, enhances feature selectivity in primary visual cortex via subtractive surround suppression mediated by inhibition from cortical layer 1 driven by the bottom-up retina-SC-LP-V1 pathway. [ABSTRACT FROM AUTHOR]

Summary Many animals guide their movements using optic flow, the displacement of stationary objects across the retina caused by self-motion. How do animals selectively synthesize a global motion pattern from its local motion components? To what extent does this feature selectivity rely on circuit mechanisms versus dendritic processing? Here we used in vivo calcium imaging to identify pre- and postsynaptic mechanisms for processing local motion signals in global motion detection circuits in Drosophila. Lobula plate tangential cells (LPTCs) detect global motion by pooling input from local motion detectors, T4/T5 neurons. We show that T4/T5 neurons suppress responses to adjacent local motion signals whereas LPTC dendrites selectively amplify spatiotemporal sequences of local motion signals consistent with preferred global patterns. We propose that sequential nonlinear suppression and amplification operations allow optic flow circuitry to simultaneously prevent saturating responses to local signals while creating selectivity for global motion patterns critical to behavior. Highlights • Global motion circuits in Drosophila exhibit nonlinear summation of local signals • Neurons that detect local motion suppress spatially adjacent signals • Dendrites that pool local motion inputs align with a preferred direction of motion • Oriented dendrites amplify responses to specific spatiotemporal input sequences Barnhart et al. show that sequential nonlinear summation of local motion cues shapes feature selectivity in the Drosophila visual system. In global motion circuits, adjacent local signals are suppressed presynaptically, whereas specific spatiotemporal sequences of local signals are amplified postsynaptically. [ABSTRACT FROM AUTHOR]

Summary Visual perception is affected by spatial context. In visual cortex, neuronal responses to stimuli inside the receptive field (RF) are suppressed by stimuli in the RF surround. To understand the circuits and cortical layers processing spatial context, we simultaneously recorded across all layers of macaque primary visual cortex while presenting stimuli at increasing distances from the recorded cells' RF. We find that near versus far-surround stimuli activate distinct layers, thus revealing unique laminar contributions to the processing of local and global spatial context. Stimuli in the near-surround evoke the earliest subthreshold responses in superficial and upper-deep layers, and earliest suppression of spiking responses in superficial layers. Conversely, far-surround stimuli evoke the earliest subthreshold responses in feedback-recipient layer 1 and lower-deep layers, and earliest suppression of spiking responses almost simultaneously in all layers, except 4C, where suppression emerges last. Our results suggest distinct circuits for local and global signal integration. Graphical Abstract Highlights • Local and global visuo-spatial context engage V1 laminae in selective ways • Processing of local information is faster and begins in superficial and deep layers • Processing of global information is slower and begins in layers 1 and 6 • Local information engages multiple circuits, and global information engages feedback Visual perception is affected by spatial context. Here Bijanzadeh et al. examine the role of V1 layers in the processing of contextual information. They find layer-specific differences in the processing of local and global visuo-spatial context suggestive of distinct underlying neural circuits. [ABSTRACT FROM AUTHOR]

Summary Substantial evidence at the subcellular level indicates that the spatial arrangement of synaptic inputs onto dendrites could play a significant role in cortical computations, but how synapses of functionally defined cortical networks are arranged within the dendrites of individual neurons remains unclear. Here we assessed one-dimensional spatial receptive fields of individual dendritic spines within individual layer 2/3 neuron dendrites. Spatial receptive field properties of dendritic spines were strikingly diverse, with no evidence of large-scale topographic organization. At a fine scale, organization was evident: neighboring spines separated by less than 10 μm shared similar spatial receptive field properties and exhibited a distance-dependent correlation in sensory-driven and spontaneous activity patterns. Fine-scale dendritic organization was supported by the fact that functional groups of spines defined by dimensionality reduction of receptive field properties exhibited non-random dendritic clustering. Our results demonstrate that functional synaptic clustering is a robust feature existing at a local spatial scale. Video Abstract [ABSTRACT FROM AUTHOR]