Orientation Preference Maps Research Articles

Local Origin of Field Potentials in Visual Cortex

The local field potential (LFP) is increasingly used to measure the combined activity of neurons within a region of tissue. Yet, available estimates of the size of this region are highly disparate, ranging from several hundred microns to a few millimeters. To measure the size of this region directly, we used a combination of multielectrode recordings and optical imaging. We determined the orientation selectivity of stimulus-evoked LFP signals in primary visual cortex and were able to predict it on the basis of the surrounding map of orientation preference. The results show that > 95% of the LFP signal originates within 250 microm of the recording electrode. This quantitative estimate indicates that LFPs are more local than often recognized and provides a guide to the interpretation of the increasing number of studies that rest on LFP recordings.

Uncovering the Mysterious Origins of Local Field Potentials

In this issue of Neuron, Katzner et al. use a combination of multielectrode recordings and optical imaging to determine the spatial extent of local field potential (LFP) activity in primary visual cortex. By estimating the orientation selectivity of stimulus-evoked LFP activity from the map of orientation preference obtained using optical imaging, they find that LFP selectivity is best fit using signals within 250 microm of the recording electrode.

Neuronal Selectivity and Local Map Structure in Visual Cortex

The organization of primary visual cortex (V1) into functional maps makes individual cells operate in a variety of contexts. For instance, some neurons lie in regions of fairly homogeneous orientation preference (iso-orientation domains), while others lie in regions with a variety of preferences (e.g., pinwheel centers). We asked whether this diversity in local map structure correlates with the degree of selectivity of spike responses. We used a combination of imaging and electrophysiology to reveal that neurons in regions of homogeneous orientation preference have much sharper tuning. Moreover, in both monkeys and cats, a common principle links the structure of the orientation map, on the spatial scale of dendritic integration, to the degree of selectivity of individual cells. We conclude that neural computation is not invariant across the cortical surface. This finding must factor into future theories of receptive field wiring and map development.

V1 Neurons: In Tune with the Neighbors

In this issue of Neuron, Nauhaus et al. use a combination of optical imaging and multiple electrode recording to demonstrate that the orientation tuning of single cells in primary visual cortex is reliably related to the local structure of the orientation preference map in both cats and monkeys.

Standing Waves and Traveling Waves Distinguish Two Circuits in Visual Cortex

The visual cortex represents stimuli through the activity of neuronal populations. We measured the evolution of this activity in space and time by imaging voltage-sensitive dyes in cat area V1. Contrast-reversing stimuli elicit responses that oscillate at twice the stimulus frequency, indicating that signals originate mostly in complex cells. These responses stand clear of the noise, whose amplitude decreases as 1/frequency, and yield high-resolution maps of orientation preference and retinotopy. We first show how these maps are combined to yield the responses to focal, oriented stimuli. We then study the evolution of the oscillating activity in space and time. In the orientation domain, it is a standing wave. In the spatial domain, it is a traveling wave propagating at 0.2-0.5 m/s. These different dynamics indicate a fundamental distinction in the circuits underlying selectivity for position and orientation, two key stimulus attributes.

Reconciling models of surround modulation and V1 feature map development

The cerebral cortex of mammals is organized as a set of topographic maps, forming sensory and motor areas such as those in the visual, auditory, and somatosensory systems. Understanding how these maps develop and whether they have any functional significance is critical for understanding cortical processing. The prototypical example of topographic feature maps is the map of orientation preference in primary visual cortex (V1). Models of V1 orientation map development have been very successful in reproducing the features of biological maps. The majority of these models are based on a principle of Mexican-hat connectivity i.e. short-range excitatory and long-range inhibitory connections between neurons (e.g. [1]). However, experimental data is in striking disagreement with this principle. There is a consensus that long-range connections between V1 neurons are excitatory [2]. Moreover, models with long-range excitatory connections are able to account for a wide range of experimental data from adult V1, such as surround modulation (e.g. [3]). Models of orientation map development are thus based on a connectivity which is precisely opposite to that suggested by a mounting body of experimental and computational evidence. It is not yet clear if the circuits used in surround modulation models are consistent with the development of orientation maps. It is also important to consider how the topographic organization of orientation preference may affect surround modulation. Since cortical circuitry is intimately tied to topographic organization, it is likely that surround modulation properties differ depending on the position of a cell within the orientation map. In order to address the above issues, we have developed the first model that is consistent with current models of surround modulation, yet also reproduces the features of successful developmental models of topographic map formation. The model consists of sheets of firing-rate-based units that represent the retina, LGN, excitatory, and inhibitory neurons in V1. An activity-driven Hebbian learning mechanism results in the adjustment of afferent (retina to V1) and long-range lateral connection weights (within V1), leading to the development of orientation selectivity organized smoothly in a realistic orientation map.

The Effect of Angioscotomas on Map Structure in Primary Visual Cortex

When blood vessels occlude the photoreceptor layer in the retina, they cast shadows onto the photoreceptors, creating angioscotomas (regions of the visual field to which that eye is blind). Remarkably, Adams and Horton (2002) have recently shown that it is sometimes possible to observe representations of these angioscotomas anatomically in the primary visual cortices of squirrel monkeys. However, there is substantial variability in the degree and form of these representations. The source of this variability is difficult to determine experimentally, because experimental studies are unavoidably limited by small sample size. In addition, experimental studies cannot compare the map structure that would develop with and without an angioscotoma. Here, we investigate these phenomena computationally using feature-mapping models of visual cortical development, which are not subject to the same limitations. These models suggest that the primary source of variability in angioscotoma representation is the precise timing of the onset of visual experience relative to the time course of ocular dominance column segregation. Furthermore, the models predict that angioscotomas could compete for control of local column layout with other influences such as cortical shape but that they have a small effect on the structure of orientation preference maps.

How do functional maps in primary visual cortex vary with eccentricity?

It is important to understand whether functional maps of primary visual cortex (V1) are organized differently at the representation of different eccentricities. By using optical imaging of intrinsic signals, we compared the maps of orientation and spatial frequency (SF) preference between central (0-3 degrees ) and paracentral (4-8 degrees ) V1 in the prosimian bush baby (Otolemur garnetti). No differences related to eccentricity were found for orientation selectivity or magnitude between central and paracentral V1. We found, however, that cardinal orientations were overrepresented in central but not in paracentral V1 and that isoorientation domain size tended to be smaller in the central representation. We demonstrated that spatial frequency was represented continuously across V1, and that the map of SF preference exhibited eccentricity-dependent variations, with more territory devoted to higher SFs in central than in paracentral V1. Although there were no spatial relationships between orientation domains and cytochrome oxidase (CO) blobs or interblobs, CO blobs tended to prefer lower SFs than interblobs. Taken together with previous research, our data indicate that functional domains in V1 show eccentricity-related differences in organization and also support the idea that different maps (with or without specific geometrical relationships) are organized for adequate coverage of each feature in visual space.

The influence of cortical feature maps on the encoding of the orientation of a short line

The inhomogeneous distribution of the receptive fields of cortical neurons influences the cortical representation of the orientation of short lines seen in visual images. We construct a model of the response of populations of neurons in the human primary visual cortex by combining realistic response properties of individual neurons and cortical maps of orientation and location preferences. The encoding error, which characterizes the difference between the parameters of a visual stimulus and their cortical representation, is calculated using Fisher information as the square root of the variance of a statistically efficient estimator. The error of encoding orientation varies considerably with the location and orientation of the short line stimulus as modulated by the underlying orientation preference map. The average encoding error depends only weakly on the structure of the orientation preference map and is much smaller than the human error of estimating orientation measured psychophysically. From this comparison we conclude that the actual mechanism of orientation perception does not make efficient use of all the information available in the neuronal responses and that it is the decoding of visual information from neuronal responses that limits psychophysical performance.

Spontaneous symmetry breaking in self–organizing neural fields

We extend the theory of self-organizing neural fields in order to analyze the joint emergence of topography and feature selectivity in primary visual cortex through spontaneous symmetry breaking. We first show how a binocular one-dimensional topographic map can undergo a pattern forming instability that breaks the underlying symmetry between left and right eyes. This leads to the spatial segregation of eye specific activity bumps consistent with the emergence of ocular dominance columns. We then show how a 2-dimensional isotropic topographic map can undergo a pattern forming instability that breaks the underlying rotation symmetry. This leads to the formation of elongated activity bumps consistent with the emergence of orientation preference columns. A particularly interesting property of the latter symmetry breaking mechanism is that the linear equations describing the growth of the orientation columns exhibits a rotational shift-twist symmetry, in which there is a coupling between orientation and topography. Such coupling has been found in experimentally generated orientation preference maps.

Cortical Maps of Separable Tuning Properties Predict Population Responses to Complex Visual Stimuli

In the earliest cortical stages of visual processing, a scene is represented in different functional domains selective for specific features. Maps of orientation and spatial frequency preference have been described in the primary visual cortex using simple sinusoidal grating stimuli. However, recent imaging experiments suggest that the maps of these two spatial parameters are not sufficient to describe patterns of activity in different orientation domains generated in response to complex, moving stimuli. A model of cortical organization is presented in which cortical temporal frequency tuning is superimposed on the maps of orientation and spatial frequency tuning. The maps of these three tuning properties are sufficient to describe the activity in orientation domains that have been measured in response to drifting complex images. The model also makes specific predictions about how moving images are represented in different spatial frequency domains. These results suggest that the tangential organization of primary visual cortex can be described by a set of maps of separable neuronal receptive field features including maps of orientation, spatial frequency, and temporal frequency tuning properties.

Invariant computations in local cortical networks with balanced excitation and inhibition

Cortical computations critically involve local neuronal circuits. The computations are often invariant across a cortical area yet are carried out by networks that can vary widely within an area according to its functional architecture. Here we demonstrate a mechanism by which orientation selectivity is computed invariantly in cat primary visual cortex across an orientation preference map that provides a wide diversity of local circuits. Visually evoked excitatory and inhibitory synaptic conductances are balanced exquisitely in cortical neurons and thus keep the spike response sharply tuned at all map locations. This functional balance derives from spatially isotropic local connectivity of both excitatory and inhibitory cells. Modeling results demonstrate that such covariation is a signature of recurrent rather than purely feed-forward processing and that the observed isotropic local circuit is sufficient to generate invariant spike tuning.

Contrast invariance of functional maps in cat primary visual cortex.

Neurons in cat primary visual cortex (V1) are clustered according to their preference for stimulus position, orientation, spatial frequency, and eye of presentation, thereby giving rise to functional maps. It is not known, however, whether a similar arrangement is present for stimulus contrast. Neurons in cat V1 vary considerably in their contrast responses, and might be clustered in a systematic fashion in this respect. Additionally, stimulus contrast might affect other functional maps. For example, there has been debate over whether the contrast threshold of neurons in cytochrome oxidase blobs is lower than elsewhere. Here we have imaged intrinsic signals to measure orientation maps in cat V1 at a range of contrast levels. We determined, on a pixel-by-pixel basis, contrast-response functions and orientation tuning curves. The fit parameters describing contrast responses were more or less uniform: We found no regions where neurons have lower contrast threshold than elsewhere. If such regions do exist, their functional maps must be substantially weaker than maps of orientation preference. Moreover, we found that contrast has no impact on maps of orientation preference: The orientation selectivity of each pixel is invariant with stimulus contrast. The contrast invariance that we demonstrate at the level of maps is well known at the level of single neurons. It suggests that neurons contributing to a pixel response generally have similar orientation preferences or similar contrast responses. The latter explanation is likely to hold in pinwheel centers, where preferred orientation of nearby neurons can differ markedly. In summary, our data suggest that contrast is represented uniformly over the surface of cat V1, and changes in contrast do not affect maps of orientation preference.

Visual experience promotes the isotropic representation of orientation preference.

Within the visual cortex of several mammalian species, more circuitry is devoted to the representation of vertical and horizontal orientations than oblique orientations. The sensitivity of this representation of orientation preference to visual experience during cortical maturation and the overabundance of cardinal contours in the environment suggest that vision promotes the development of this cortical anisotropy. We tested this idea by measuring the distribution of cortical orientation preference and the degree of orientation selectivity in developing normal and dark-reared ferrets using intrinsic signal optical imaging. The area of the angle map of orientation preference representing cardinal and oblique orientations was determined; in addition, orientation selectivity indices were computed separately for cardinal and oblique difference images. In normal juvenile animals, we confirm a small, but statistically significant overrepresentation of near horizontal orientations in the cortical angle map. However, the degree of anisotropy did not increase in the weeks that followed eye opening when orientation selectivity matured; rather, it decreased. In dark-reared ferrets, an even greater cortical anisotropy emerged, but angle maps in these animals developed an apparently anomalous overrepresentation of near vertical orientations. Thus, the overrepresentation of cardinal orientations in the visual cortex does not require experience with an anisotropic visual environment; indeed, cortical anisotropy can develop in the complete absence of vision. These observations suggest that the role of visual experience in cortical maturation is to promote the isotropic representation of orientation preference.

Large-scale modeling of the primary visual cortex: influence of cortical architecture upon neuronal response

A large-scale computational model of a local patch of input layer 4 Cα of the primary visual cortex (V1) of the macaque monkey, together with a coarse-grained reduction of the model, are used to understand potential effects of cortical architecture upon neuronal performance. Both the large-scale point neuron model and its asymptotic reduction are described. The work focuses upon orientation preference and selectivity, and upon the spatial distribution of neuronal responses across the cortical layer. Emphasis is given to the role of cortical architecture (the geometry of synaptic connectivity, of the ordered and disordered structure of input feature maps, and of their interplay) as mechanisms underlying cortical responses within the model. Specifically: (i) Distinct characteristics of model neuronal responses (firing rates and orientation selectivity) as they depend upon the neuron’s location within the cortical layer relative to the pinwheel centers of the map of orientation preference; (ii) A time independent (DC) elevation in cortico-cortical conductances within the model, in contrast to a “push–pull” antagonism between excitation and inhibition; (iii) The use of asymptotic analysis to unveil mechanisms which underly these performances of the model; (iv) A discussion of emerging experimental data. The work illustrates that large-scale scientific computation––coupled together with analytical reduction, mathematical analysis, and experimental data, can provide significant understanding and intuition about the possible mechanisms of cortical response. It also illustrates that the idealization which is a necessary part of theoretical modeling can outline in sharp relief the consequences of differing alternative interpretations and mechanisms––with final arbiter being a body of experimental evidence whose measurements address the consequences of these analyses.

Orientation mosaic in barn owl’s visual Wulst revealed by optical imaging: comparison with cat and monkey striate and extra-striate areas

Using the technique of intrinsic signal optical imaging, orientation preference maps were obtained from the Wulst of the barn owl in the area that represents central vision, and from the visual cortices (V1 and V2) of cat and marmoset monkey. Iso-orientation domains in barn owl’s visual Wulst were patch-like structures with an inter-patch distance of ∼0.9 mm, arranged in a pinwheel-like manner around singularity points. The size of the iso-orientation domains in barn owl was larger than those found in area V1, but comparable to those found in area V2, of cat and monkey. Superficial layers of the owl visual Wulst may be equivalent to extra-striate visual areas of primates and carnivores, as already suggested by electrophysiologists discussing the much increased radial dimensions of the Wulst compared with neocortex in mammals.

The visual cortex as a crystal

A theory of pattern formation in primary visual cortex (V1) is presented that takes into account its crystalline-like structure. The cortex is partitioned into fundamental domains or hypercolumns of a lattice describing the distribution of singularities or pinwheels in the orientation preference map. Each hypercolumn is modelled as a network of orientation and spatial frequency selective cells organised around a pair of pinwheels, which are associated with high and low spatial frequency domains, respectively. The network topology of the hypercolumn is taken to be a sphere with the pinwheels located at the poles of the sphere. Interactions between hypercolumns are mediated by anisotropic long-range lateral connections that link cells with similar feature preferences. Using weakly nonlinear analysis, we investigate the spontaneous formation of cortical activity patterns through the simultaneous breaking of an internal O (3) symmetry and a discrete lattice symmetry. The resulting patterns are characterised by states in which each hypercolumn exhibits a tuned response to both orientation and spatial frequency and the distribution of optimal responses across hypercolumns is doubly periodic or quasi-periodic with respect to the underlying lattice.

Formation of an Orientation Preference Map - Gradual Inhibition Method

Formation of an Orientation Preference Map - Gradual Inhibition Method

Plasticity of orientation preference maps in the visual cortex of adult cats.

In contrast to the high degree of experience-dependent plasticity usually exhibited by cortical representational maps, a number of experiments performed in visual cortex suggest that the basic layout of orientation preference maps is only barely susceptible to activity-dependent modifications. In fact, most of what we know about activity-dependent plasticity in adults comes from experiments in somatosensory, auditory, or motor cortex. Applying a stimulation protocol that has been proven highly effective in other cortical areas, we demonstrate here that enforced synchronous cortical activity induces major changes of orientation preference maps (OPMs) in adult cats. Combining optical imaging of intrinsic signals and electrophysiological single-cell recordings, we show that a few hours of intracortical microstimulation (ICMS) lead to an enlargement of the cortical representational zone at the ICMS site and an extensive restructuring of the entire OPM layout up to several millimeters away, paralleled by dramatic changes of pinwheel numbers and locations. At the single-cell level, we found that the preferred orientation was shifted toward the orientation of the ICMS site over a region of up to 4 mm. Our results show that manipulating the synchronicity of cortical activity locally without invoking training, attention, or reinforcement, OPMs undergo large-scale reorganization reminiscent of plastic changes observed for nonvisual cortical maps. However, changes were much more widespread and enduring. Such large-scale restructuring of the visual cortical networks indicates a substantial capability for activity-dependent plasticity of adult visual cortex and may provide the basis for cognitive learning processes.

Orientation specificity of contrast adaptation in visual cortical pinwheel centres and iso-orientation domains.

Exposure to a high-contrast visual stimulus causes adaptation, a psychophysical phenomenon that is quite selective for stimulus orientation. Its mechanism is largely cortical but the underlying circuitry is still not unambiguously resolved. It has been suggested that adaptation could be the result of integration of inputs from cells within a large local pool, effectively scaling their outputs with respect to local contrast. In this case, orientation selectivity of neuronal adaptation should depend on the location of neurons within the cortical map of orientation preference. We tested this hypothesis by quantifying adaptation to optimally oriented and to orthogonal-to-optimum gratings among neurons recorded either from iso-orientation domains or orientation pinwheel centres, as identified by optical imaging of cat visual cortex. We did not find a significant difference in adaptation characteristics for these two populations of cells, implying that these characteristics do not depend on the local functional architecture. Surprisingly, however, we additionally observed that under isoflurane (but not halothane) anaesthesia, most neurons exhibited adaptation by cross-oriented gratings, regardless of their location within the orientation map. It seems likely that, under isoflurane, inputs became visible that were masked by the commonly used, deeper halothane anaesthesia. For individual cells, the presence of these inputs was independent of their location within the cortical orientation map.