Statistics and geometry of orientation selectivity in primary visual cortex

Orientation maps are a prominent feature of the primary visual cortex of higher mammals. In macaques and cats, for example, preferred orientations of neurons are organized in a specific pattern, where cells with similar selectivity are clustered in iso-orientation domains. However, the map is not always continuous, and there are pinwheel-like singularities around which all orientations are arranged in an orderly fashion. Although subject of intense investigation for half a century now, it is still not entirely clear how these maps emerge and what function they might serve. Here, we suggest a new model of orientation selectivity that combines the geometry and statistics of clustered thalamocortical afferents to explain the emergence of orientation maps. We show that the model can generate spatial patterns of orientation selectivity closely resembling the maps found in cats or monkeys. Without any additional assumptions, we further show that the pattern of ocular dominance columns is inherently connected to the spatial pattern of orientation.     

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

The development of orientation selectivity in the primary visual cortex is described by first-order kinetics between three functional compartments chained in a catenary mode. A first model is presented, in which two unidirectional kinetics with constant exchange coefficients, symmetrical in their effects, function in an alternating mode depending on the presence or absence of visual experience. The failure of this model to simulate the modifications induced by a delayed visual experience, when the exchange coefficients are identified to fit normal and dark rearing, supports the hypothesis that the maturation process consequent to interaction with visual environment is dependent on the date at which it is allowed to take place. A second model is then proposed, in which exchange coefficients are piecewise linear functions of time. In order to correctly predict the functional effects of restricted visual experience following prior dark rearing, it is assumed that visuomotor experience during the critical period permits the expression of a non-linear modifiability gradient which may have been masked up to this point by the absence of vision or eye movements.     

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.     

Direction selectivity of excitation and inhibition in simple cells of the cat primary visual cortex

Direction selectivity in simple cells of primary visual cortex, defined from their spike responses, cannot be predicted using linear models. It has been suggested that the shunting inhibition evoked by visual stimulation is responsible for the nonlinear component of direction selectivity. Cortical inhibition would suppress a neuron's firing when stimuli move in the nonpreferred direction, but would allow responses to stimuli in the preferred direction. Models of direction selectivity based solely on input from the lateral geniculate nucleus, however, propose that the nonlinear response is caused by spike threshold. By extracting excitatory and inhibitory components of synaptic inputs from intracellular records obtained in vivo, we demonstrate that excitation and inhibition are tuned for the same direction, but differ in relative timing. Further, membrane potential responses combine in a linear fashion. Spike threshold, however, quantitatively accounts for the nonlinear component of direction selectivity, amplifying the direction selectivity of spike output relative to that of synaptic inputs.     

Fast coding of orientation in primary visual cortex

Understanding how populations of neurons encode sensory information is a major goal of systems neuroscience. Attempts to answer this question have focused on responses measured over several hundred milliseconds, a duration much longer than that frequently used by animals to make decisions about the environment. How reliably sensory information is encoded on briefer time scales, and how best to extract this information, is unknown. Although it has been proposed that neuronal response latency provides a major cue for fast decisions in the visual system, this hypothesis has not been tested systematically and in a quantitative manner. Here we use a simple 'race to threshold' readout mechanism to quantify the information content of spike time latency of primary visual (V1) cortical cells to stimulus orientation. We find that many V1 cells show pronounced tuning of their spike latency to stimulus orientation and that almost as much information can be extracted from spike latencies as from firing rates measured over much longer durations. To extract this information, stimulus onset must be estimated accurately. We show that the responses of cells with weak tuning of spike latency can provide a reliable onset detector. We find that spike latency information can be pooled from a large neuronal population, provided that the decision threshold is scaled linearly with the population size, yielding a processing time of the order of a few tens of milliseconds. Our results provide a novel mechanism for extracting information from neuronal populations over the very brief time scales in which behavioral judgments must sometimes be made.     

Sensitivity profile for orientation selectivity in the visual cortex of goggle-reared mice

It has been widely accepted that ocular dominance in the responses of visual cortical neurons can change depending on visual experience in a postnatal period. However, experience-dependent plasticity for orientation selectivity, which is another important response property of visual cortical neurons, is not yet fully understood. To address this issue, using intrinsic signal imaging and two-photon calcium imaging we attempted to observe the alteration of orientation selectivity in the visual cortex of juvenile and adult mice reared with head-mounted goggles, through which animals can experience only the vertical orientation. After one week of goggle rearing, the density of neurons optimally responding to the exposed orientation increased, while that responding to unexposed orientations decreased. These changes can be interpreted as a reallocation of preferred orientations among visually responsive neurons. Our obtained sensitivity profile for orientation selectivity showed a marked peak at 5 weeks and sustained elevation at 12 weeks and later. These features indicate the existence of a critical period between 4 and 7 weeks and residual orientation plasticity in adult mice. The presence of a dip in the sensitivity profile at 10 weeks suggests that different mechanisms are involved in orientation plasticity in childhood and adulthood.     

Sound-driven synaptic inhibition in primary visual cortex

Multimodal objects and events activate many sensory cortical areas simultaneously. This is possibly reflected in reciprocal modulations of neuronal activity, even at the level of primary cortical areas. However, the synaptic character of these interareal interactions, and their impact on synaptic and behavioral sensory responses are unclear. Here, we found that activation of auditory cortex by a noise burst drove local GABAergic inhibition on supragranular pyramids of the mouse primary visual cortex, via cortico-cortical connections. This inhibition was generated by sound-driven excitation of a limited number of cells in infragranular visual cortical neurons. Consequently, visually driven synaptic and spike responses were reduced upon bimodal stimulation. Also, acoustic stimulation suppressed conditioned behavioral responses to a dim flash, an effect that was prevented by acute blockade of GABAergic transmission in visual cortex. Thus, auditory cortex activation by salient stimuli degrades potentially distracting sensory processing in visual cortex by recruiting local, translaminar, inhibitory circuits.     

Inhibition, spike threshold, and stimulus selectivity in primary visual cortex

Ever since Hubel and Wiesel described orientation selectivity in the visual cortex, the question of how precise selectivity emerges has been marked by considerable debate. There are essentially two views of how selectivity arises. Feed-forward models rely entirely on the organization of thalamocortical inputs. Feedback models rely on lateral inhibition to refine selectivity relative to a weak bias provided by thalamocortical inputs. The debate is driven by two divergent lines of evidence. On the one hand, many response properties appear to require lateral inhibition, including precise orientation and direction selectivity and crossorientation suppression. On the other hand, intracellular recordings have failed to find consistent evidence for lateral inhibition. Here we demonstrate a resolution to this paradox. Feed-forward models incorporating the intrinsic nonlinear properties of cortical neurons and feed-forward circuits (i.e., spike threshold, contrast saturation, and spike-rate rectification) can account for properties that have previously appeared to require lateral inhibition.     

A reaction-diffusion model to capture disparity selectivity in primary visual cortex

Decades of experimental studies are available on disparity selective cells in visual cortex of macaque and cat. Recently, local disparity map for iso-orientation sites for near-vertical edge preference is reported in area 18 of cat visual cortex. No experiment is yet reported on complete disparity map in V1. Disparity map for layer IV in V1 can provide insight into how disparity selective complex cell receptive field is organized from simple cell subunits. Though substantial amounts of experimental data on disparity selective cells is available, no model on receptive field development of such cells or disparity map development exists in literature. We model disparity selectivity in layer IV of cat V1 using a reaction-diffusion two-eye paradigm. In this model, the wiring between LGN and cortical layer IV is determined by resource an LGN cell has for supporting connections to cortical cells and competition for target space in layer IV. While competing for target space, the same type of LGN cells, irrespective of whether it belongs to left-eye-specific or right-eye-specific LGN layer, cooperate with each other while trying to push off the other type. Our model captures realistic 2D disparity selective simple cell receptive fields, their response properties and disparity map along with orientation and ocular dominance maps. There is lack of correlation between ocular dominance and disparity selectivity at the cell population level. At the map level, disparity selectivity topography is not random but weakly clustered for similar preferred disparities. This is similar to the experimental result reported for macaque. The details of weakly clustered disparity selectivity map in V1 indicate two types of complex cell receptive field organization.     

Directional tunings independent of orientation in the primary visual cortex of the cat

A family of moving ‘random-line’ patterns was developed and used to study the directional tuning of 91 single units in cat primary visual cortex (V1). The results suggest that, in addition to the well-known orientation-dependent mechanism, there is also some kind of orientationindependent mechanism underlying the direction selectivity. The directional tuning of the neurons varies in accordance with the increase of orientation or non-orientation element in the stimulus.     

Directional tunings independent of orientation in the primary visual cortex of the cat

A family of moving 'random-line' patterns was developed and used to study the directional tuning of 91 single units in cat primary visual cortex (V1). The results suggest that, in addition to the well-known orientation-dependent mechanism, there is also some kind of orientation-independent mechanism underlying the direction selectivity. The directional tuning of the neurons varies in accordance with the increase of orientation or non-orientation element in the stimulus.     

Prediction of orientation selectivity from receptive field architecture in simple cells of cat visual cortex

From the intracellularly recorded responses to small, rapidly flashed spots, we have quantitatively mapped the receptive fields of simple cells in the cat visual cortex. We then applied these maps to a feedforward model of orientation selectivity. Both the preferred orientation and the width of orientation tuning of the responses to oriented stimuli were well predicted by the model. Where tested, the tuning curve was well predicted at different spatial frequencies. The model was also successful in predicting certain features of the spatial frequency selectivity of the cells. It did not successfully predict the amplitude of the responses to drifting gratings. Our results show that the spatial organization of the receptive field can account for a large fraction of the orientation selectivity of simple cells.     

Activation of orientation selectivity mechanisms in neurons of the cat visual cortex by a moving visual "noise" field

A relationship was established between the response of neurons of the cat visual cortex and the direction of movement in the visual "noise" field and of a slit of light. It was shown that a shift in the preferred direction of movement in the "noise" field in relation to that of the slit was found in orientationally selective neurons only. It was concluded that the "noise" field, which is a stimulus lacking an orientation component, does activate mechanisms of neuronal orientation selectively.V. Kapsukas State University, Vilnius. Translated from Neirofiziologiya, Vol. 17, No. 5, pp. 596–601, September–October, 1985.     

A neuronal network model of primary visual cortex explains spatial frequency selectivity

We address how spatial frequency selectivity arises in Macaque primary visual cortex (V1) by simulating V1 with a large-scale network model consisting of O(10⁴) excitatory and inhibitory integrate-and-fire neurons with realistic synaptic conductances. The new model introduces variability of the widths of subregions in V1 neuron receptive fields. As a consequence different model V1 neurons prefer different spatial frequencies. The model cortex has distributions of spatial frequency selectivity and of preference that resemble experimental findings from the real V1. Two main sources of spatial frequency selectivity in the model are the spatial arrangement of feedforward excitation, and cortical nonlinear suppression, a result of cortical inhibition. Action Editor: Jonathan D. Victor     

Dynamics of tuning to orientation of cross-like figures in neurons from the cat visual cortex

Dynamics of tuning to orientation of flashing light bar and to orientation of cross-like figure was studied by a temporal slices method in 87 neurons of the cat primary visual cortex. Tuning was plotted by spikes number in the entire response and in its successive fragments with a step of 20 ms. It was found that successive dynamic shift of preferred orientation of a bar was typical for 87% units, white such shift of preferred orientation of a cross was met in 75% of cases. Comparison of tuning dynamics for bar and cross allowed to separate units into three groups: the first one (58.6% of cases) with larger dynamic shift of a bar preferred orientation then of a cross (74.9 +/- 5.8 degrees [symbol: see text] 29.8 +/- 4.1 degrees, correspondingly, p < 0.00001), the second group (21.5%) with opposite effect (24.2 +/- 5.2 degrees and 69.2 +/- 10.0 degrees, p < 0.0002) and the third group (19.8%) without significant shift of preferred orientation of bar and cross and without difference in their dynamics. Possible mechanisms of the preferred orientation dynamics and its difference for bar and cross are discussed.     

Geometry of orientation columns in the visual cortex

The optimal direction of lines in the visual field to which neurons in the visual cortex respond changes in a regular way when the recording electrode progresses tangentially through the cortex (Hubel and Wiesel, 1962). It is possible to reconstruct the field of orientations from long, sometimes multiple parallel penetrations (Hubel and Wiesel, 1974; Albus, 1975) by assuming that the orientations are arranged radially around centers. A method is developed which makes it possible to define uniquely the position of the centers in the vicinity of the electrode track. They turn out to be spaced at distances of about 0.5 mm and may be tentatively identified with the positions of the giant cells of Meynert.     

Comparative study on direction selectivity and functional organization of the primary visual cortical cells in monkeys and cats

Although the directionally selective cells in many visual cortical areas are organized in columnar manner, the functional organization of direction selectivity of area VI in the monkey still remains unclear. We quantitatively studied the proportion of directionally selective cells, direction selectivity and the functional organization of the striate cortical cells in the monkey and compared those with the cat. The results show that the direction selectivity and directional organization of striate cortical cells in the monkey are significantly weaker than those in the cat, suggesting that the species difference between the two kinds of animal is related to their different anatomic pathways.