Similarity of visual selectivity among clonally related neurons in visual cortex

Neurons in rodent visual cortex are organized in a salt-and-pepper fashion for orientation selectivity, but it is still unknown how this functional architecture develops. A recent study reported that the progeny of single cortical progenitor cells are preferentially connected in the postnatal cortex. If these neurons acquire similar selectivity through their connections, a salt-and-pepper organization may be generated, because neurons derived from different progenitors are intermingled in rodents. Here we investigated whether clonally related cells have similar preferred orientation by using a transgenic mouse, which labels all the progeny of single cortical progenitor cells. We found that preferred orientations of clonally related cells are similar to each other, suggesting that cell lineage is involved in the development of response selectivity of neurons in the cortex. However, not all clonally related cells share response selectivity, suggesting that cell lineage is not the only determinant of response selectivity.     

Dynamics of orientation selectivity in the primary visual cortex and the importance of cortical inhibition

To test theories of orientation selectivity in primary visual cortex (V1), we have done experiments to measure the dynamics of orientation tuning of single neurons in the V1 cortex of macaque monkeys. Based on our dynamics results, we propose that a V1 cell's orientation selectivity is generated mainly by both tuned enhancement and global suppression. Enhancement near the preferred orientation is probably caused by feed-forward input from LGN (plus amplification by cortical-cortical interaction). Global suppression could be supplied by cortical inhibition. Additionally, in about 1/3 of V1 neurons (usually the most sharply tuned) there is tuned suppression, centered near the cell's preferred orientation but broader than tuned enhancement. These mechanisms also can explain important features of steady-state selectivity in the V1 neuron population. Furthermore, similar neuronal mechanisms may be used generally throughout the cerebral cortex.     

The Role of Thalamic Population Synchrony in the Emergence of Cortical Feature Selectivity

In a wide range of studies, the emergence of orientation selectivity in primary visual cortex has been attributed to a complex interaction between feed-forward thalamic input and inhibitory mechanisms at the level of cortex. Although it is well known that layer 4 cortical neurons are highly sensitive to the timing of thalamic inputs, the role of the stimulus-driven timing of thalamic inputs in cortical orientation selectivity is not well understood. Here we show that the synchronization of thalamic firing contributes directly to the orientation tuned responses of primary visual cortex in a way that optimizes the stimulus information per cortical spike. From the recorded responses of geniculate X-cells in the anesthetized cat, we synthesized thalamic sub-populations that would likely serve as the synaptic input to a common layer 4 cortical neuron based on anatomical constraints. We used this synchronized input as the driving input to an integrate-and-fire model of cortical responses and demonstrated that the tuning properties match closely to those measured in primary visual cortex. By modulating the overall level of synchronization at the preferred orientation, we show that efficiency of information transmission in the cortex is maximized for levels of synchronization which match those reported in thalamic recordings in response to naturalistic stimuli, a property which is relatively invariant to the orientation tuning width. These findings indicate evidence for a more prominent role of the feed-forward thalamic input in cortical feature selectivity based on thalamic synchronization.     

Cortical heterogeneity: Implications for visual processing and polysensory integration

Recent studies have revealed substantial variation in pyramidal cell structure in different cortical areas. Moreover, cell morphology has been shown to vary in a systematic fashion such that cells in visual association areas are larger and more spinous than those in the primary visual area. Various aspects of these structural differences appear to be important in influencing neuronal function. At the cellular level, differences in the branching patterns in the dendritic arbour may allow for varying degrees of non-linear compartmentalisation. Differences in total dendritic length and spine number may determine the number of inputs integrated by individual cells. Variations in spine density and geometry may affect cooperativity of inputs and shunting inhibition, and the tangential dimension of the dendritic arbours may determine sampling strategies within cortex. At the systems level, regional variation in pyramidal cell structure may determine thedegree of recurrent excitation through reentrant circuits influencing the discharge properties of individual neurones and the functional signature of the circuits they compose. The ability of pyramidal neurones in visual areas of the parietal and temporal lobes to integrate large numbers of excitatory inputs may also facilitate cortical binding. Here I summarise what I consider to be among the most salient, and testable, aspects of an inter-relationship between morphological and functional heterogeneity in visual cortex.     

Spontaneous symmetry-breaking energy functions and the emergence of orientation selective cortical cells

The mammalian visual cortex is comprised of hypercolumns of orientation selective cells. The developmental process by which cells are generated with receptive fields tuned to a variety of orientations has so far remained a mystery. We present a model for the production of orientation selective cells that requires no external stimuli and a minimum of input parameters. The process involves spontaneous symmetry-breaking in an energy function that governs the maturation of the cortical cells in a multi-layer network of Hebb-type feedforward neurons. An important feature is that the symmetry breaking occurs for each cell separately and is not due to global organizing effects. We present examples of receptive field profiles calculated with the symmetry-breaking procedure and note that the results seem robust and may be useful in the study of development in several types of cortical cells. The inclusion of long range lateral (intra-layer) correlations in the energy function could result in the development of cell groups with correlated preferred orientations that resemble the hypercolumns seen in the visual cortex.     

Recording and manipulating the in vivo correlational structure of neuronal activity during visual cortical development.

Many aspects of visual cortical functional architecture, such as orientation and ocular dominance columns, are present before animals have had any visual experience, indicating that the initial formation of cortical circuitry takes place without the influence of environmental cues. For this reason, it has been proposed that spontaneous activity within the developing visual pathway carries instructive information to guide the early establishment of cortical circuits. Recently developed recording and stimulation techniques are revealing new information about the in vivo organization of this spontaneous activity and its contribution to cortical development. Multielectrode recordings in the developing lateral geniculate nucleus (LGN) of ferrets demonstrate that retinal spontaneous activity is not simply relayed to the visual cortex, but is reshaped and transformed by a variety of mechanisms including cortical feedback and endogenous oscillatory activity. The resulting patterns are consistent with many of the predictions of correlation-based models of cortical development. In addition, the introduction of artificially correlated activity into the visual pathway disrupts some but not all aspects of orientation tuning development. Thus, while these results support an instructive role of spontaneous activity in shaping cortical development, there still appears to be a number of aspects of this process that cannot be accounted for by activity alone.     

Diversity and cell type specificity of local excitatory connections to neurons in layer 3B of monkey primary visual cortex

In the primary visual cortex of macaque monkeys, laminar and columnar axonal specificity are correlated with functional differences between locations. We describe evidence that embedded within this anatomical framework is finer specificity of functional connections. Photostimulation-based mapping of functional input to 31 layer 3B neurons revealed that input sources to individual cells were highly diverse. Although some input differences were correlated with neuronal anatomy, no 2 neurons received excitatory input from the same cortical layers. Thus, input diversity reveals far more cell types than does anatomical diversity. This implies relatively little functional redundancy; despite trends related to laminar or columnar position, pools of neurons contributing uniquely to visual processing are likely relatively small. These results also imply that similarities in the anatomy of circuits in different cortical areas or species may not indicate similar functional connectivity.     

Stability of cortical responses and the statistics of natural scenes.

The primary visual cortex (V1) of higher mammals contains maps of stimulus features; how these maps influence vision remains unknown. We have examined the functional significance of an asymmetry in the orientation map in cat V1, i.e., the fact that a larger area of V1 is preferentially activated by vertical and horizontal contours than by contours at oblique orientations. Despite the fact that neurons tuned to cardinal and oblique orientations have indistinguishable tuning characteristics, cardinal neurons remain more stable in their response properties after selective perturbation induced by adaptation. Similarly, human observers report different adaptation-induced changes in orientation tuning between cardinal and oblique axes. We suggest that the larger cortical area devoted to cardinal orientations imposes stability on the processing of cardinal contours during visual perception, by retaining invariant cortical responses along cardinal axes.     

Orientation tuning--a crooked path to the straight and narrow

Neurons in visual cortex are selective for the orientation of a visual stimulus, while the receptive fields of their thalamic input are circular. Cortical orientation selectivity arises from the organization of both thalamic input and local cortical circuits. In this issue of Neuron, Schummers and colleagues provide evidence that the local circuit mechanisms contributing to orientation selectivity differ depending on the local organization of the orientation map.     

Computational Modeling of Orientation Tuning Dynamics in Monkey Primary Visual Cortex

In the primate visual pathway, orientation tuning of neurons is first observed in the primary visual cortex. The LGN cells that comprise the thalamic input to V1 are not orientation tuned, but some V1 neurons are quite selective. Two main classes of theoretical models have been offered to explain orientation selectivity: feedforward models, in which inputs from spatially aligned LGN cells are summed together by one cortical neuron; and feedback models, in which an initial weak orientation bias due to convergent LGN input is sharpened and amplified by intracortical feedback. Recent data on the dynamics of orientation tuning, obtained by a cross-correlation technique, may help to distinguish between these classes of models. To test this possibility, we simulated the measurement of orientation tuning dynamics on various receptive field models, including a simple Hubel-Wiesel type feedforward model: a linear spatiotemporal filter followed by an integrate-and-fire spike generator. The computational study reveals that simple feedforward models may account for some aspects of the experimental data but fail to explain many salient features of orientation tuning dynamics in V1 cells. A simple feedback model of interacting cells is also considered. This model is successful in explaining the appearance of Mexican-hat orientation profiles, but other features of the data continue to be unexplained.     

猫前内侧上雪氏区视神经元对运动随机线条的反应

对于运动信息在脑内的加工,一种观点认为分两阶段进行,低级视皮层只对运动图形内部成分的取向进行调谐,高级视皮层整合低级视皮层的输入,对图形整体的运动方向敏感。用网格（plaid）作为刺激的实验表明,在较低级皮层区,细胞多表现为成分方向选择性（Component-motion Selectivity),即对刺激中的取向因素敏感：而较高视皮层的细胞多表现为整体方向选择性（Pattern-motion Selecitivity),对运动整体的方向敏感,从而支持运动信息加工的“两阶段”理论。实验中,用一系列运动随机线条刺激（random line patterns)。研究猫前内侧上雪氏区（Anteriormedial lateral suprasylvian area,AMLS)神经元的方向调谐特性。结果表明多数细胞为整体方向选择性,且随线长增加此类细胞比例下降,而成分方向选择性细胞的比例有所增加,呈现由整体方向选择性向中间类型（Unclassified),由中间类型向成分方向选择性变化的趋势,提示整体或成分方向选择性可能并非细胞的固有特性,而是可以随刺激取向因素的变化而改变的。     

How does the cerebral cortex work? Learning, attention, and grouping by the laminar circuits of visual cortex

The organization of neocortex into layers is one of its most salient anatomical features. These layers include circuits that form functional columns in cortical maps. A major unsolved problem concerns how bottom-up, top-down, and horizontal interactions are organized within cortical layers to generate adaptive behaviors. This article models how these interactions help visual cortex to realize: (i) the binding process whereby cortex groups distributed data into coherent object representations; (ii) the attentional process whereby cortex selectively processes important events; and (iii) the developmental and learning processes whereby cortex shapes its circuits to match environmental constraints. New computational ideas about feedback systems suggest how neocortex develops and learns in a stable way, and why top-down attention requires converging bottom-up inputs to fully activate cortical cells, whereas perceptual groupings do not.     

Neural Coding of Finger and Wrist Movements

Previous work (Schieber and Hibbard, 1993) has shown that single motor cortical neurons do not discharge specifically for a particular flexion-extension finger movement but instead are active with movements of different fingers. In addition, neuronal populations active with movements of different fingers overlap extensively in their spatial locations in the motor cortex. These data suggested that control of any finger movement utilizes a distributed population of neurons. In this study we applied the neuronal population vector analysis (Georgopoulos et al., 1983) to these same data to determine (1) whether single cells are tuned in an abstract, three-dimensional (3D) instructed finger and wrist movement space with hand-like geometry and (2) whether the neuronal population encodes specific finger movements. We found that the activity of 132/176 (75%) motor cortical neurons related to finger movements was indeed tuned in this space. Moreover, the population vector computed in this space predicted well the instructed finger movement. Thus, although single neurons may be related to several disparate finger movements, and neurons related to different finger movements are intermingled throughout the hand area of the motor cortex, the neuronal population activity does specify particular finger movements.     

Emergence of orientation-selective inhibition in the primary visual cortex: a Bayes–Markov computational model

The recent consensus is that virtually all aspects of response selectivity exhibited by the primary visual cortex are either created or sharpened by cortical inhibitory interneurons. Experimental studies have shown that there are cortical inhibitory cells that are driven by geniculate cells and that, like their cortical excitatory counterparts, are orientation selective, though less sharply tuned. The main goal of this article is to demonstrate how orientation-selective inhibition might be created by the circuitry of the primary visual cortex (striate cortex, V1) from its nonoriented geniculate inputs. To fulfill this goal, first, a Bayes–Markov computational model is developed for the V1 area dedicated to foveal vision. The developed model consists of three parts: (i) a two-layered hierarchical Markov random field that is assumed to generate the activity patterns of the geniculate and cortical inhibitory cells, (ii) a Bayesian computational goal that is formulated based on the maximum a posteriori (MAP) estimation principle, and (iii) an iterative, deterministic, parallel algorithm that leads the cortical circuitry to achieve its assigned computational goal. The developed model is not fully LGN driven and it is not implementable by the neural machinery of V1. The model, then, is transformed into a fully LGN-driven and physiologically plausible form. Computer simulation is used to demonstrate the performance of the developed models.     

Rewiring cortex: the role of patterned activity in development and plasticity of neocortical circuits.

Visually driven activity is not required for the establishment of ocular dominance columns, orientation columns, and long-range horizontal connections in visual cortex, although spontaneous activity appears to be necessary. The role of activity may be instructive or simply permissive; evidence for an instructive role requires inquiry into the role of the pattern of activity in shaping cortical circuits. The few experiments that have probed the role of patterned activity include the effects of artificial strabismus, artificial stimulation of the optic nerve, and rewiring visual projections from the retina to the auditory thalamus and cortex. These experiments demonstrate that patterned activity is vital for the maintenance of thalamocortical, local intracortical, and long-range horizontal connections in cortex.     

Orientation preference patterns in mammalian visual cortex: a wire length minimization approach

In the visual cortex of many mammals, orientation preference changes smoothly along the cortical surface, with the exception of singularities such as pinwheels and fractures. The reason for the existence of these singularities has remained elusive, suggesting that they are developmental artifacts. We show that singularities reduce the length of intracortical neuronal connections for some connection rules. Therefore, pinwheels and fractures could be evolutionary adaptations keeping cortical volume to a minimum. Wire length minimization approach suggests that interspecies differences in orientation preference maps reflect differences in intracortical neuronal circuits, thus leading to experimentally testable predictions. We discuss application of our model to direction preference maps.     

Broad inhibition sharpens orientation selectivity by expanding input dynamic range in mouse simple cells

Orientation selectivity (OS) is an emergent property in the primary visual cortex (V1). How OS arises from synaptic circuits remains unsolved. Here, in vivo whole-cell recordings in the mouse V1 revealed that simple cells received broadly tuned excitation and even more broadly tuned inhibition. Excitation and inhibition shared a similar orientation preference and temporally overlapped substantially. Neuron modeling and dynamic-clamp recording further revealed that excitatory inputs alone would result in membrane potential responses with significantly attenuated selectivity, due to a saturating input-output function of the membrane filtering. Inhibition ameliorated the attenuation of excitatory selectivity by expanding the input dynamic range and caused additional sharpening of output responses beyond unselectively suppressing responses at all orientations. This "blur-sharpening" effect allows selectivity conveyed by excitatory inputs to be better expressed, which may be a general mechanism underlying the generation of feature-selective responses in the face of strong excitatory inputs that are weakly biased.     

Neural processing of gustatory information in insular circuits

The insular cortex is the primary cortical site devoted to taste processing. A large body of evidence is available for how insular neurons respond to gustatory stimulation in both anesthetized and behaving animals. Most of the reports describe broadly tuned neurons that are involved in processing the chemosensory, physiological and psychological aspects of gustatory experience. However little is known about how these neural responses map onto insular circuits. Particularly mysterious is the functional role of the three subdivisions of the insular cortex: the granular, the dysgranular and the agranular insular cortices. In this article we review data on the organization of the local and long-distance circuits in the three subdivisions. The functional significance of these results is discussed in light of the latest electrophysiological data. A view of the insular cortex as a functionally integrated system devoted to processing gustatory, multimodal, cognitive and affective information is proposed.     

Top-Down Inputs Enhance Orientation Selectivity in Neurons of the Primary Visual Cortex during Perceptual Learning

Perceptual learning has been used to probe the mechanisms of cortical plasticity in the adult brain. Feedback projections are ubiquitous in the cortex, but little is known about their role in cortical plasticity. Here we explore the hypothesis that learning visual orientation discrimination involves learning-dependent plasticity of top-down feedback inputs from higher cortical areas, serving a different function from plasticity due to changes in recurrent connections within a cortical area. In a Hodgkin-Huxley-based spiking neural network model of visual cortex, we show that modulation of feedback inputs to V1 from higher cortical areas results in shunting inhibition in V1 neurons, which changes the response properties of V1 neurons. The orientation selectivity of V1 neurons is enhanced without changing orientation preference, preserving the topographic organizations in V1. These results provide new insights to the mechanisms of plasticity in the adult brain, reconciling apparently inconsistent experiments and providing a new hypothesis for a functional role of the feedback connections.     

Development of orientation selectivity in the primary visual cortex of normally and dark reared kittens

Kinetics of the development of orientation tuning are inferred from quantitative analysis of extracellular recordings in the primary visual cortex of normally and dark reared kittens. 712 visual cells were classified in three functional groups: a) non-specific cells, and b) immature cells which are not as orientation selective as c) specific cells. Power regression and covariance analysis indicate that the "critical period" begins before 19 days and that the kinetics of the immature pool are the same in both rearing conditions. A catenary process of development of orientation selectivity is proposed, the immature compartment being a transit pool between non-specific and specific cells. Two sequential stages occur: 1) the realisation of an intrinsic programme of maturation, by which cortical specificity appears at eye opening and increases independently of visual experience 2) a phase of "epigenesis" beginning at 19 days, during which functional modification depends on visual experience.