Cortical Map Formation


Invariant computations in local cortical networks with balanced excitation and inhibition

J. Mariño and J. Schummers and D. C. Lyon and L. Schwabe and O. Beck and P. Wiesing and K. Obermayer and M. Sur

Nat Neurosci  8  194-201  (2005)

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.


The operating regime of local computations in primary visual cortex

M. Stimberg and K. Wimmer and R. Martin and L. Schwabe and J. Mariño and J. Schummers and D. C. Lyon and M. Sur and K. Obermayer

Cereb Cortex  19  2166-80  (2009)

In V1, local circuitry depends on the position in the orientation map: close to pinwheel centers, recurrent inputs show variable orientation preferences; within iso-orientation domains, inputs are relatively uniformly tuned. Physiological properties such as cell's membrane potentials, spike outputs, and temporal characteristics change systematically with map location. We investigate in a firing rate and a Hodgkin-Huxley network model what constraints these tuning characteristics of V1 neurons impose on the cortical operating regime. Systematically varying the strength of both recurrent excitation and inhibition, we test a wide range of model classes and find the likely models to account for the experimental observations. We show that recent intracellular and extracellular recordings from cat V1 provide the strongest evidence for a regime where excitatory and inhibitory recurrent inputs are balanced and dominate the feed-forward input. Our results are robust against changes in model assumptions such as spatial extent and strength of lateral inhibition. Intriguingly, the most likely recurrent regime is in a region of parameter space where small changes have large effects on the network dynamics, and it is close to a regime of "runaway excitation," where the network shows strong self-sustained activity. This could make the cortical response particularly sensitive to modulation.


Critical period plasticity in local cortical circuits

T. K. Hensch

Nat Rev Neurosci  6  877-88  (2005)

Neuronal circuits in the brain are shaped by experience during 'critical periods' in early postnatal life. In the primary visual cortex, this activity-dependent development is triggered by the functional maturation of local inhibitory connections and driven by a specific, late-developing subset of interneurons. Ultimately, the structural consolidation of competing sensory inputs is mediated by a proteolytic reorganization of the extracellular matrix that occurs only during the critical period. The reactivation of this process, and subsequent recovery of function in conditions such as amblyopia, can now be studied with realistic circuit models that might generalize across systems.


Role of subplate neurons in functional maturation of visual cortical columns

P. O. Kanold and P. Kara and R. C. Reid and C. J. Shatz

Science  301  521-5  (2003)

The subplate forms a transient circuit required for development of connections between the thalamus and the cerebral cortex. When subplate neurons are ablated, ocular dominance columns do not form in the visual cortex despite the robust presence of thalamic axons in layer 4. We show that subplate ablation also prevents formation of orientation columns. Visual responses are weak and poorly tuned to orientation. Furthermore, thalamocortical synaptic transmission fails to strengthen, whereas intracortical synapses are unaffected. Thus, subplate circuits are essential not only for the anatomical segregation of thalamic inputs but also for key steps in synaptic remodeling and maturation needed to establish the functional architecture of visual cortex.


Columnar architecture sculpted by GABA circuits in developing cat visual cortex

T. K. Hensch and M. P. Stryker

Science  303  1678-81  (2004)

The mammalian visual cortex is organized into columns. Here, we examine cortical influences upon developing visual afferents in the cat by altering intrinsic gamma-aminobutyric acid (GABA)-mediated inhibition with benzodiazepines. Local enhancement by agonist (diazepam) infusion did not perturb visual responsiveness, but did widen column spacing. An inverse agonist (DMCM) produced the opposite effect. Thus, intracortical inhibitory circuits shape the geometry of incoming thalamic arbors, suggesting that cortical columnar architecture depends on neuronal activity.


Activity-dependent PSA expression regulates inhibitory maturation and onset of critical period plasticity

G. Di Cristo and B. Chattopadhyaya and S. J. Kuhlman and Y. Fu and M.-C. Bélanger and C. Z. Wu and U. Rutishauser and L. Maffei and Z. J. Huang

Nat Neurosci  10  1569-77  (2007)

Functional maturation of GABAergic innervation in the developing visual cortex is regulated by neural activity and sensory inputs and in turn influences the critical period of ocular dominance plasticity. Here we show that polysialic acid (PSA), presented by the neural cell adhesion molecule, has a role in the maturation of GABAergic innervation and ocular dominance plasticity. Concentrations of PSA significantly decline shortly after eye opening in the adolescent mouse visual cortex; this decline is hindered by visual deprivation. The developmental and activity-dependent regulation of PSA expression is inversely correlated with the maturation of GABAergic innervation. Premature removal of PSA in visual cortex results in precocious maturation of perisomatic innervation by basket interneurons, enhanced inhibitory synaptic transmission, and earlier onset of ocular dominance plasticity. The developmental and activity-dependent decline of PSA expression therefore regulates the timing of the maturation of GABAergic inhibition and the onset of ocular dominance plasticity.


Equalization of ocular dominance columns induced by an activity-dependent learning rule and the maturation of inhibition

T. Toyoizumi and K. D. Miller

J Neurosci  29  6514-25  (2009)

Early in development, the cat primary visual cortex (V1) is dominated by inputs driven by the contralateral eye. The pattern then reorganizes into ocular dominance columns that are roughly equally distributed between inputs serving the two eyes. This reorganization does not occur if the eyes are kept closed. The mechanism of this equalization is unknown. It has been argued that it is unlikely to involve Hebbian activity-dependent learning rules, on the assumption that these would favor an initially dominant eye. The reorganization occurs at the onset of the critical period (CP) for monocular deprivation (MD), the period when MD can cause a shift of cortical innervation in favor of the nondeprived eye. In mice, the CP is opened by the maturation of cortical inhibition, which does not occur if the eyes are kept closed. Here we show how these observations can be united: under Hebbian rules of activity-dependent synaptic modification, strengthening of intracortical inhibition can lead to equalization of the two eyes' inputs. Furthermore, when the effects of homeostatic synaptic plasticity or certain other mechanisms are incorporated, activity-dependent learning can also explain how MD causes a shift toward the open eye during the CP despite the drive by inhibition toward equalization of the two eyes' inputs. Thus, assuming similar mechanisms underlie the onset of the CP in cats as in mice, this and activity-dependent learning rules can explain the interocular equalization observed in cat V1 and its failure to occur without visual experience.


Dissociating ocular dominance column development and ocular dominance plasticity: a neurotrophic model

T. Elliott and N. R. Shadbolt

Biol Cybern  86  281-92  (2002)

Recent experimental data indicate that both neurotrophic factors (NTFs) and intracortical inhibitory circuitry are implicated in the development and plasticity of ocular dominance columns. We extend a neurotrophic model of developmental synaptic plasticity, which previously failed to account correctly for the differences between monocular deprivation and binocular deprivation, and show that the inclusion of lateral cortical inhibition is indeed necessary in understanding the effects of visual deprivation in the model. In particular, we argue that monocular deprivation causes a differential shift in the balance between inhibition and excitation in cortical columns, down-regulating NTFs in deprived-eye columns and up-regulating NTFs in undeprived-eye columns; during binocular deprivation, however, no such shift occurs. We thus postulate that the response to visual deprivation is at the level of the cortical circuit, while the mechanisms of afferent segregation are at the molecular or cellular level. Such a dissociation is supported by recent experimental work challenging the assumption that columnar organisation develops in an activity-dependent, competitive fashion. Our extended model also questions recent attempts to distinguish between heterosynaptic and homosynaptic models of synaptic plasticity.


Reducing intracortical inhibition in the adult visual cortex promotes ocular dominance plasticity

A. Harauzov and M. Spolidoro and G. DiCristo and R. De Pasquale and L. Cancedda and T. Pizzorusso and A. Viegi and N. Berardi and L. Maffei

J Neurosci  30  361-71  (2010)

Experience-dependent plasticity in the cortex is often higher during short critical periods in postnatal development. The mechanisms limiting adult cortical plasticity are still unclear. Maturation of intracortical GABAergic inhibition is suggested to be crucial for the closure of the critical period for ocular dominance (OD) plasticity in the visual cortex. We find that reduction of GABAergic transmission in the adult rat visual cortex partially reactivates OD plasticity in response to monocular deprivation (MD). This is accompanied by an enhancement of activity-dependent potentiation of synaptic efficacy but not of activity-dependent depression. We also found a decrease in the expression of chondroitin sulfate proteoglycans in the visual cortex of MD animals with reduced inhibition, after the reactivation of OD plasticity. Thus, intracortical inhibition is a crucial limiting factor for the induction of experience-dependent plasticity in the adult visual cortex.


Inhibitory sharpening of receptive fields contributes to whisker map plasticity in rat somatosensory cortex

E. Foeller and T. Celikel and D. E. Feldman

J Neurophysiol  94  4387-400  (2005)

The role of inhibition in sensory cortical map plasticity is not well understood. Here we tested whether inhibition contributes to expression of receptive field plasticity in developing rat somatosensory (S1) cortex. In normal rats, microiontophoresis of gabazine (SR 95531), a competitive gamma-aminobutyric acid (GABA)-A receptor antagonist, preferentially disinhibited surround whisker responses relative to principal whisker responses, indicating that GABA(A) inhibition normally acts to sharpen whisker tuning. Plasticity was induced by transiently depriving adolescent rats of all but one whisker; this causes layer 2/3 (L2/3) receptive fields to shift away from the deprived principal whisker and toward the spared surround whisker. In units with shifted receptive fields, gabazine preferentially disinhibited responses to the deprived principal whisker, unlike in controls, suggesting that GABA(A) inhibition was acting to preferentially suppress these responses relative to spared whisker responses. This effect was not observed for L2/3 units that did not express receptive field plasticity or in layer 4, where receptive field plasticity did not occur. Thus GABA(A) inhibition promoted expression of sensory map plasticity by helping to sharpen receptive fields around the spared input.


Models of orientation and ocular dominance columns in the visual cortex: a critical comparison

E. Erwin and K. Obermayer and K. Schulten

Neural Comput  7  425-68  (1995)

Orientation and ocular dominance maps in the primary visual cortex of mammals are among the most thoroughly investigated of the patterns in the cerebral cortex. A considerable amount of work has been dedicated to unraveling both their detailed structure and the neural mechanisms that underlie their formation and development. Many schemes have been proposed, some of which are in competition. Some models focus on development of receptive fields while others focus on the structure of cortical maps, i.e., the arrangement of receptive field properties across the cortex. Each model used different means to determine its success at reproducing experimental map patterns, often relying principally on visual comparison. Experimental data are becoming available that allow a more careful evaluation of models. In this contribution more than 10 of the most prominent models of cortical map formation and structure are critically evaluated and compared with the most recent experimental findings from macaque striate cortex. Comparisons are based on properties of the predicted or measured cortical map patterns. We introduce several new measures for comparing experimental and model map data that reveal important differences between models. We expect that the use of these measures will improve current models by helping determine parameters to match model maps to experimental data now becoming available from a variety of species. Our study reveals that (1) despite apparent differences, many models are based on similar principles and consequently make similar predictions, (2) several models produce orientation map patterns that are not consistent with the experimental data from macaques, regardless of the plausibility of the models' suggested physiological implementations, and (3) no models have yet fully accounted for both the local and the global relationships between orientation and ocular dominance map patterns.


A micro-architecture for binocular disparity and ocular dominance in visual cortex

P. Kara and J. D. Boyd

Nature  458  627-31  (2009)

In invertebrate predators such as the praying mantis and vertebrate predators such as wild cats the ability to detect small differences in inter-ocular retinal disparities is a critical means for accurately determining the depth of moving objects such as prey. In mammals, the first neurons along the visual pathway that encode binocular disparities are found in the visual cortex. However, a precise functional architecture for binocular disparity has never been demonstrated in any species, and coarse maps for disparity have been found in only one primate species. Moreover, the dominant approach for assaying the developmental plasticity of binocular cortical neurons used monocular tests of ocular dominance to infer binocular function. The few studies that examined the relationship between ocular dominance and binocular disparity of individual cells used single-unit recordings and have provided conflicting results regarding whether ocular dominance can predict the selectivity or sensitivity to binocular disparity. We used two-photon calcium imaging to sample the response to monocular and binocular visual stimuli from nearly every adjacent neuron in a small region of the cat visual cortex, area 18. Here we show that local circuits for ocular dominance always have smooth and graded transitions from one apparently monocular functional domain to an adjacent binocular region. Most unexpectedly, we discovered a new map in the cat visual cortex that had a precise functional micro-architecture for binocular disparity selectivity. At the level of single cells, ocular dominance was unrelated to binocular disparity selectivity or sensitivity. When the local maps for ocular dominance and binocular disparity both had measurable gradients at a given cortical site, the two gradient directions were orthogonal to each other. Together, these results indicate that, from the perspective of the spiking activity of individual neurons, ocular dominance cannot predict binocular disparity tuning. However, the precise local arrangement of ocular dominance and binocular disparity maps provide new clues regarding how monocular and binocular depth cues may be combined and decoded.


Whither the hypercolumn?

D. Y. Ts'o and M. Zarella and G. Burkitt

J Physiol  587  2791-805  (2009)

Among the crowning achievements of Hubel and Wiesel's highly influential studies on primary visual cortex is the description of the cortical hypercolumn, a set of cortical columns with functional properties spanning a particular parameter space. This fundamental concept laid the groundwork for the notion of a modular sensory cortex, canonical cortical circuits and an understanding of visual field coverage beyond simple retinotopy. Surprisingly, the search for and description of analogous hypercolumnar organizations in other cortical areas to date has been limited. In the present work, we have applied the hypercolumn concept to the functional organization of the second visual area, V2. We found it important to separate out the original definition of the hypercolumn from other associated observations and concepts, not all of which are applicable to V2. We present results indicating that, as in V1, the V2 hypercolumns for orientation and binocular interaction (disparity) run roughly orthogonal to each other. We quantified the 'nearest neighbour' periodicities for the hypercolumns for ocular dominance, orientation, colour and disparity, and found a marked similarity in the periodicities of all of these hypercolumns, both across hypercolumn type and across visual areas V1 and V2. The results support an underlying common mechanism that constrains the anatomical extent of hypercolumn systems, and highlight the original definition of the cortical hypercolumn.


Consistent mapping of orientation preference across irregular functional domains in ferret visual cortex

L. E. White and W. H. Bosking and D. Fitzpatrick

Vis Neurosci  18  65-76  (2001)

The mammalian visual cortex harbors a number of functional maps that represent distinct attributes of stimuli in the visual environment. How different functional maps are accommodated within the same cortical space, especially in species that show marked irregularities in one or more functional maps, remains poorly understood. We used optical imaging of intrinsic signals and electrophysiological techniques to investigate the organization of the maps of orientation preference, ocular dominance, and visual space in ferret. This species shows striking nonuniformity in the arrangement of ocular dominance domains and disruption of the mapping of visual space along the V1/V2 border. We asked whether these irregularities would be reflected in the organization of the map of orientation preference. The results show that orientation preference is mapped consistently within both V1 and V2, and across the interareal boundary, with no reflection of the irregularities in the other maps. These observations demonstrate the accommodation of multiple functional maps within the same cortical space without systematic geometrical relationships that necessarily constrain the organization of each representation. Furthermore, they imply that the structure of the map of orientation preference reflects the architecture and activity patterns of cortical circuits that are independent of other columnar systems established in layer 4.


The coordinated mapping of visual space and response features in visual cortex

H. Yu and B. J. Farley and D. Z. Jin and M. Sur

Neuron  47  267-80  (2005)

Whether general principles can explain the layouts of cortical maps remains unresolved. In primary visual cortex of ferret, the relationships between the maps of visual space and response features are predicted by a "dimension-reduction" model. The representation of visual space is anisotropic, with the elevation and azimuth axes having different magnification. This anisotropy is reflected in the orientation, ocular dominance, and spatial frequency domains, which are elongated such that their directions of rapid change, or high-gradient axes, are orthogonal to the high-gradient axis of the visual map. The feature maps are also strongly interdependent-their high-gradient regions avoid one another and intersect orthogonally where essential, so that overlap is minimized. Our results demonstrate a clear influence of the visual map on each feature map. In turn, the local representation of visual space is smooth, as predicted when many features are mapped within a cortical area.


Are cortical motor maps based on body parts or coordinated actions? Implications for embodied semantics

L. Fernandino and M. Iacoboni

Brain Lang      (2009)

The embodied cognition approach to the study of the mind proposes that higher order mental processes such as concept formation and language are essentially based on perceptual and motor processes. Contrary to the classical approach in cognitive science, in which concepts are viewed as amodal, arbitrary symbols, embodied semantics argues that concepts must be "grounded" in sensorimotor experiences in order to have meaning. In line with this view, neuroimaging studies have shown a roughly somatotopic pattern of activation along cortical motor areas (broadly construed) for the observation of actions involving different body parts, as well as for action-related language comprehension. These findings have been interpreted in terms of a mirror-neuron system, which automatically matches observed and executed actions. However, the somatotopic pattern of activation found in these studies is very coarse, with significant overlap between body parts, and sometimes with multiple representations for the same body part. Furthermore, the localization of the respective activations varies considerably across studies. Based on recent work on the motor cortex in monkeys, we suggest that these discrepancies result from the organization of the primate motor cortex (again, broadly construed), which probably includes maps of the coordinated actions making up the individual's motor repertoire, rather than a single, continuous map of the body. We review neurophysiological and neuroimaging data supporting this hypothesis and discuss ways in which this framework can be used to further test the links between neural mirroring and linguistic processing.


Visual field map clusters in macaque extrastriate visual cortex

H. Kolster and J. B. Mandeville and J. T. Arsenault and L. B. Ekstrom and L. L. Wald and W. Vanduffel

J Neurosci  29  7031-9  (2009)

The macaque visual cortex contains >30 different functional visual areas, yet surprisingly little is known about the underlying organizational principles that structure its components into a complete "visual" unit. A recent model of visual cortical organization in humans suggests that visual field maps are organized as clusters. Clusters minimize axonal connections between individual field maps that represent common visual percepts, with different clusters thought to carry out different functions. Experimental support for this hypothesis, however, is lacking in macaques, leaving open the question of whether it is unique to humans or a more general model for primate vision. Here we show, using high-resolution blood oxygen level-dependent functional magnetic resonance imaging data in the awake monkey at 7 T, that the middle temporal area (area MT/V5) and its neighbors are organized as a cluster with a common foveal representation and a circular eccentricity map. This novel view on the functional topography of area MT/V5 and satellites indicates that field map clusters are evolutionarily preserved and may be a fundamental organizational principle of the Old World primate visual cortex.


Cortical feature maps via geometric models

S. D. Pauls

J Physiol Paris  103  46-51  (2009)

We present a new model for feature map formation in the primary visual cortex, building on dimension reduction/wire length minimization techniques. We create a model space of feature parameters, endowed with various geometries picked to reflect physical or experimental data and search for a map from the parameter space to the cortical sheet which minimizes distortions. Upon simulating these maps, we find a family of Riemannian and sub-Riemannian geometries which give rise to feature maps which reflect known experimental data concerning (1) the qualitative arrangement of orientation maps and (2) the distribution of connections. One of the main findings is that experimental data showing both elongated and non-elongated connection patterns are represented within our family of models.


Emergence of a stable cortical map for neuroprosthetic control

K. Ganguly and J. M. Carmena

PLoS Biol  7  e1000153  (2009)

Cortical control of neuroprosthetic devices is known to require neuronal adaptations. It remains unclear whether a stable cortical representation for prosthetic function can be stored and recalled in a manner that mimics our natural recall of motor skills. Especially in light of the mixed evidence for a stationary neuron-behavior relationship in cortical motor areas, understanding this relationship during long-term neuroprosthetic control can elucidate principles of neural plasticity as well as improve prosthetic function. Here, we paired stable recordings from ensembles of primary motor cortex neurons in macaque monkeys with a constant decoder that transforms neural activity to prosthetic movements. Proficient control was closely linked to the emergence of a surprisingly stable pattern of ensemble activity, indicating that the motor cortex can consolidate a neural representation for prosthetic control in the presence of a constant decoder. The importance of such a cortical map was evident in that small perturbations to either the size of the neural ensemble or to the decoder could reversibly disrupt function. Moreover, once a cortical map became consolidated, a second map could be learned and stored. Thus, long-term use of a neuroprosthetic device is associated with the formation of a cortical map for prosthetic function that is stable across time, readily recalled, resistant to interference, and resembles a putative memory engram.


Creating abstract topographic representations: implications for coding, learning and reasoning

C. J. Tinsley

Biosystems  96  251-8  (2009)

Topographic maps are a fundamental and ubiquitous feature of the sensory and motor regions of the brain. There is less evidence for the existence of conventional topographic maps in associational areas of the brain such as the prefrontal cortex and parietal cortex. The existence of topographically arranged anatomical projections is far more widespread and occurs in associational regions of the brain as well as sensory and motor regions: this points to a more widespread existence of topographically organised maps within associational cortex than currently recognised. Indeed, there is increasing evidence that abstract topographic representations may also occur in these regions. For example, a topographic mnemonic map of visual space has been described in the dorsolateral prefrontal cortex and topographically arranged visuospatial attentional signals have been described in parietal association cortex. This article explores how abstract representations might be extracted from sensory topographic representations and subsequently code abstract information. Finally a simple model is presented that shows how abstract topographic representations could be integrated with other information within the brain to solve problems or form abstract associations. The model uses correlative firing to detect associations between different types of stimuli. It is flexible because it can produce correlations between information represented in a topographic or non-topographic coordinate system. It is proposed that a similar process could be used in high-level cognitive operations such as learning and reasoning.


Endocannabinoid signaling is required for development and critical period plasticity of the whisker map in somatosensory cortex

L. Li and K. J. Bender and P. J. Drew and S. P. Jadhav and E. Sylwestrak and D. E. Feldman

Neuron  64  537-49  (2009)

Type 1 cannabinoid (CB1) receptors mediate widespread synaptic plasticity, but how this contributes to systems-level plasticity and development in vivo is unclear. We tested whether CB1 signaling is required for development and plasticity of the whisker map in rat somatosensory cortex. Treatment with the CB1 antagonist AM251 during an early critical period for layer (L) 2/3 development (beginning postnatal day [P] 12-16) disrupted whisker map development, leading to inappropriate whisker tuning in L2/3 column edges and a blurred map. Early AM251 treatment also prevented experience-dependent plasticity in L2/3, including deprivation-induced synapse weakening and weakening of deprived whisker responses. CB1 blockade after P25 did not disrupt map development or plasticity. AM251 had no acute effect on sensory-evoked spiking and only modestly affected field potentials, suggesting that plasticity effects were not secondary to gross activity changes. These findings implicate CB1-dependent plasticity in systems-level development and early postnatal plasticity of the whisker map.


The influence of restricted orientation rearing on map structure in primary visual cortex

C. E. Giacomantonio and M. R. Ibbotson and G. J. Goodhill

Neuroimage      (2009)

Visual experience is critical to the development of the structure of the primary visual cortex and, in turn, normal functional vision. The primary visual cortex contains maps of multiple features of the visual input, and these maps are characterised by specific types of geometric relationships. Manipulations of the visual environment during development in animals such as ferrets, cats and monkeys provide an opportunity to probe the rules governing map formation via their effect on these relationships. Here we use a computational model of map formation based on dimension-reduction principles to predict the effect on map relationships of presenting only a single orientation to one eye and the orthogonal orientation to the other eye. Since orientation preference and ocular dominance are now tightly coupled one might expect orientation and ocular dominance contours to lose their normally orthogonal relationship and instead run parallel to each other. However, surprisingly, the model predicts that orthogonal intersection can sometimes be preserved in this case. The model also predicts that orientation pinwheels can migrate from the centre to the borders of ocular dominance columns, and that the wavelengths of the ocular dominance and orientation maps can become coupled. These predictions provide a way to further test the adequacy of dimension reduction principles for explaining map structure under perturbed as well as normal rearing conditions, and thus allow us to deepen our understanding of the effect of the visual environment on visual cortical development.


Functional clustering of neurons in motor cortex determined by cellular resolution imaging in awake behaving mice

D. A. Dombeck and M. S. Graziano and D. W. Tank

J Neurosci  29  13751-60  (2009)

Macroscopic (millimeter scale) functional clustering is a hallmark characteristic of motor cortex spatial organization in awake behaving mammals; however, almost no information is known about the functional micro-organization (approximately 100 microm scale). Here, we optically recorded intracellular calcium transients of layer 2/3 neurons with cellular resolution over approximately 200-microm-diameter fields in the forelimb motor cortex of mobile, head-restrained mice during two distinct movements (running and grooming). We showed that the temporal correlation between neurons was statistically larger the closer the neurons were to each other. We further explored this correlation by using two separate methods to spatially segment the neurons within each imaging field: K-means clustering and correlations between single neuron activity and mouse movements. The two methods segmented the neurons similarly and led to the conclusion that the origin of the inverse relationship between correlation and distance seen statistically was twofold: clusters of highly temporally correlated neurons were often spatially distinct from one another, and (even when the clusters were spatially intermingled) within the clusters, the more correlated the neurons were to each other, the shorter the distance between them. Our results represent a direct observation of functional clustering within the microcircuitry of the awake mouse motor cortex.


Neural pattern formation via a competitive Hebbian mechanism

K. Obermayer and T. Sejnowski and G. G. Blasdel

Behav Brain Res  66  161-7  (1995)

In this contribution we investigate a simple pattern formation process [9,10] based on Hebbian learning and competitive interactions within cortex. This process generates spatial representations of afferent (sensory) information which strongly resemble patterns of response properties of neurons commonly called brain maps. For one of the most thoroughly studied phenomena in cortical development, the formation of topographic maps, orientation and ocular dominance columns in macaque striate cortex, the process, for example, generates the observed patterns of receptive field properties including the recently described correlations between orientation preference and ocular dominance. Competitive Hebbian learning has not only proven to be a useful concept in the understanding of development and plasticity in several brain areas, but the underlying principles have have been successfully applied to problems in machine learning [22]. The model's universality, simplicity, predictive power, and usefulness warrants a closer investigation.


Coverage and the design of striate cortex.

N. Swindale

Biol Cybern  65  415-24  (1991)

Hubel and Wiesel (1977) suggested that ocular dominance and orientation columns in the macaque monkey striate cortex might be bands of uniform width that intersected orthogonally. They pointed out that if this were the case, there would be an equal allocation of cells of different orientation preference to each eye and to each point in visual space. However, orientation and ocular dominance columns have a more complex structural organization than is implied by this model: for example, iso-orientation domains do not intersect ocular dominance stripes at right angles and the two columnar systems have different periodicities. This raises the question as to how well the striate cortex manages to allocate equal numbers of neurons of different orientation preference to each eye and to each region of visual space, a factor referred to here as coverage. This paper defines a measure of uniformity of coverage, c', and investigates its dependence on several different parameters of columnar organisation. Calculations were done first using a simplified one-dimensional model of orientation and ocular dominance columns and were then repeated using more realistic two-dimensional models, generated with the algorithms described in the preceding paper (Swindale 1991). Factors investigated include the relative periodicities of the two columnar systems, the size of the cortical point image, the width of orientation tuning curves, whether columns are spatially anisotropic or not, and the role of the structural relationships between columns described by Blasdel and Salama (1986). The results demonstrate that coverage is most uniform when orientation hypercolumns are about half the size of ocular dominance hypercolumns. Coverage is most uneven when the hypercolumns are the same size, unless they are related in the way described by Blasdel and Salama, in which case coverage gets only slightly worse as the size ratio (ori/od) increases above 0.5. The minimum diameter of cortical point image that ensures reasonably uniform coverage is about twice the size of an ocular dominance hypercolumn i.e. about 1.5-2.0 mm.


Singularities in primate orientation maps.

K. Obermayer and G. Blasdel

Neural Comput  9  555-75  (1997)

We report the results of an analysis of orientation maps in primate striate cortex with focus on singularities and their distribution. Data were obtained from squirrel monkeys and macaque monkeys of different ages. We find the approximately 80\% of singularities that are nearest neighbors have the opposite sign and that the spatial distribution of singularities differs significantly from a random distribution of points. We do not find evidence for consistent geometric patterns that singularities may form across the cortex. Except for a different overall alignment of orientation bands and different periods of repetition, maps obtained from different animals and different ages are found similar with respect to the measures used. Orientation maps are then compared with two different pattern models that are currently discussed in the literature: bandpass-filtered white noise, which accounts very well for the overall map structure, and the field analogy model, which specifies the orientation map by the location of singularities and their properties. The bandpass-filtered noise approach to orientation patterns correctly predicts the sign correlations between singularities and accounts for the deviations in the spatial distribution of singularities away from a random dot pattern. The field analogy model can account for the structure of certain local patches of the orientation map but not for the whole map. Neither of the models is completely satisfactory, and the structure of the orientation map remains to be fully explained.


Influence of lateral connections on the structure of cortical maps

M. A. Carreira-Perpiñán and G. J. Goodhill

J Neurophysiol  92  2947-59  (2004)

Maps of ocular dominance and orientation in primary visual cortex have a highly characteristic structure. The factors that determine this structure are still largely unknown. In particular, it is unclear how short-range excitatory and inhibitory connections between nearby neurons influence structure both within and between maps. Using a generalized version of a well-known computational model of visual cortical map development, we show that the number of excitatory and inhibitory oscillations in this interaction function critically influences map structure. Specifically, we demonstrate that functions that oscillate more than once do not produce maps closely resembling those seen biologically. This strongly suggests that local lateral connections in visual cortex oscillate only once and have the form of a Mexican hat.


A computational model for the development of multiple maps in primary visual cortex

M. A. Carreira-Perpiñán and R. J. Lister and G. J. Goodhill

Cereb Cortex  15  1222-33  (2005)

Primary visual cortex contains multiple maps of features of the visual scene, including visual field position, orientation, direction, ocular dominance and spatial frequency. The complex relationships between these maps provide clues to the strategies the cortex uses for representing and processing information. Here we simulate the combined development of all these map systems using a computational model, the elastic net. We show that this model robustly produces combined maps of these four variables that bear a close resemblance to experimental maps. In addition we show that the experimentally observed effects of monocular deprivation and single-orientation rearing can be reproduced in this model, and we make some testable predictions. These results provide strong support for the hypothesis that cortical representations attempt to optimize a trade-off between coverage and continuity.


Contributions of theoretical modeling to the understanding of neural map development

G. J. Goodhill

Neuron  56  301-11  (2007)

Theoretical/computational models have played an important role in developing our understanding of the fundamental mechanisms involved in neural map formation. I review models based on both chemospecific and activity-dependent matching of inputs to targets, with a particular focus on map development in the optic tectum and primary visual cortex.


Natural scene statistics and the structure of orientation maps in the visual cortex

J. J. Hunt and C. E. Giacomantonio and H. Tang and D. Mortimer and S. Jaffer and V. Vorobyov and G. Ericksson and F. Sengpiel and G. J. Goodhill

Neuroimage  47  157-72  (2009)

Visual activity after eye-opening influences feature map structure in primary visual cortex (V1). For instance, rearing cats in an environment of stripes of one orientation yields an over-representation of that orientation in V1. However, whether such changes also affect the higher-order statistics of orientation maps is unknown. A statistical bias of orientation maps in normally raised animals is that the probability of the angular difference in orientation preference between each pair of points in the cortex depends on the angle of the line joining those points relative to a fixed but arbitrary set of axes. Natural images show an analogous statistical bias; however, whether this drives the development of comparable structure in V1 is unknown. We examined these statistics for normal, stripe-reared and dark-reared cats, and found that the biases present were not consistently related to those present in the input, or to genetic relationships. We compared these results with two computational models of orientation map development, an analytical model and a Hebbian model. The analytical model failed to reproduce the experimentally observed statistics. In the Hebbian model, while orientation difference statistics could be strongly driven by the input, statistics similar to those seen in experimental maps arose only when symmetry breaking was allowed to occur spontaneously. These results suggest that these statistical biases of orientation maps arise primarily spontaneously, rather than being governed by either input statistics or genetic mechanisms.


One-dimensional dynamics of attention and decision making in LIP

S. Ganguli and J. W. Bisley and J. D. Roitman and M. N. Shadlen and M. E. Goldberg and K. D. Miller

Neuron  58  15-25  (2008)

Where we allocate our visual spatial attention depends upon a continual competition between internally generated goals and external distractions. Recently it was shown that single neurons in the macaque lateral intraparietal area (LIP) can predict the amount of time a distractor can shift the locus of spatial attention away from a goal. We propose that this remarkable dynamical correspondence between single neurons and attention can be explained by a network model in which generically high-dimensional firing-rate vectors rapidly decay to a single mode. We find direct experimental evidence for this model, not only in the original attentional task, but also in a very different task involving perceptual decision making. These results confirm a theoretical prediction that slowly varying activity patterns are proportional to spontaneous activity, pose constraints on models of persistent activity, and suggest a network mechanism for the emergence of robust behavioral timing from heterogeneous neuronal populations.


Functional somatotopy in sensorimotor cortex

M. Flanders

Neuroreport  16  313-6  (2005)

In an effort to understand the highly distributed somatotopy of primary motor cortex, this review draws on principles derived from studies of auditory, visual and somatosensory cortical areas. In each case, a behaviorally important feature or function is overlaid in multiple locations on an underlying topographic map of the peripheral sensory surface. Recent studies of hand muscle synergies suggest the types of two-dimensional functional axes that might reasonably be mapped to the two-dimensional surface of the primary motor cortex. However, other research emphasizes that even a functional somatotopy must be extremely flexible.


Influences on the global structure of cortical maps.

G. Goodhill and K. Bates and P. Montague

Proc R Soc Lond B Biol Sci  264  649-55  (1997)

Cortical maps often contain global spatial structure: however, theoretical accounts for their development have generally concentrated on reproducing only local structure. We show that the elastic net model of cortical map formation can closely approximate the global structure of the ocular dominance column map observed in macaque primary visual cortex. A key component is the assumption of spatially non-uniform and anisotropic correlations in the retina. This work shows how genetic and epigenetic effects could combine to establish characteristic global structure in cortical maps.


Correlation-based development of ocularly matched orientation and ocular dominance maps: determination of required input activities.

E. Erwin and K. Miller

J Neurosci  18  9870-95  (1998)

We extend previous models for separate development of ocular dominance and orientation selectivity in cortical layer 4 by exploring conditions permitting combined organization of both properties. These conditions are expressed in terms of functions describing the degree of correlation in the firing of two inputs from the lateral geniculate nucleus (LGN), as a function of their retinotopic separation and their 'type' (ON center or OFF center and left eye or right eye). The development of ocular dominance requires that the correlations of an input with other inputs of the same eye be stronger than or equal to its correlations with inputs of the opposite eye and strictly stronger at small retinotopic separations. This must be true after summing correlations with inputs of both center types. The development of orientation-selective simple cells requires that (1) an input's correlations with other inputs of the same center type be stronger than its correlations with inputs of the opposite center type at small retinotopic separation; and (2) this relationship reverse at larger retinotopic separations within an arbor radius (the radius over which LGN cells can project to a common cortical point). This must be true after summing correlations with inputs serving both eyes. For orientations to become matched in the two eyes, correlated activity within the receptive fields must be maximized by specific between-eye alignments of ON and OFF subregions. Thus the correlations between the eyes must differ depending on center type, and this difference must vary with retinotopic separation within an arbor radius. These principles are satisfied by a wide class of correlation functions. Combined development of ocularly matched orientation maps and ocular dominance maps can be achieved either simultaneously or sequentially. In the latter case, the model can produce a correlation between the locations of orientation map singularities and local ocular dominance peaks similar to that observed physiologically. The model's main prediction is that the above correlations should exist among inputs to cortical layer 4 simple cells before vision. In addition, mature simple cells are predicted to have certain relationships between the locations of the ON and OFF subregions of the left and right eyes' receptive fields.


Multimodal output mapping of human central motor representation on different spatial scales.

J. Classen and U. Knorr and K. Werhahn and G. Schlaug and E. Kunesch and L. Cohen and R. Seitz and R. Benecke

J Physiol (Lond)  512 ( Pt 1)  163-79  (1998)

1. Non-invasive mapping by focal transcranial magnetic stimulation (TMS) is frequently used to investigate cortical motor function in the intact and injured human brain. We examined how TMS-derived maps relate to the underlying cortical anatomy and to cortical maps generated by functional imaging studies. 2. The centres of gravity (COGs) of TMS maps of the first dorsal intersosseus muscle (FDI) were integrated into 3-D magnetic resonance imaging (MRI) data sets in eleven subjects. In seven of these subjects the TMS-derived COGs were compared with the COG of regional cerebral blood flow increases using positron emission tomography (PET) in an index finger flexion protocol. 3. Mean TMS-derived COG projections were located on the posterior lip of the precentral gyrus and TMS-derived COG projections were in close proximity to the mean PET-derived COG, suggesting that the two methods reflect activity of similar cortical elements. 4. Criteria for a reliable assessment of the COG and the number of positions with a minimum amplitude of two-thirds of the maximum motor-evoked potential (T3Ps) were determined as a function of the number of stimuli and extension of the stimulation field. COGs and T3Ps were compared with an estimate of the size of the human motor cortex targeting alpha-motoneurons of forearm muscles. This comparison suggests that TMS can retrieve spatial information on cortical organization below the macroanatomic scale of cortical regions. 5. Finally, we studied the cortical representation of hand muscles in relation to facial and foot muscle representations and investigated hemispherical asymmetries. We did not find any evidence for a different ipsi- or contralateral representation of the mentalis muscle. Also, no difference was found between FDI representations on the dominant versus the non-dominant hemisphere.


Where the abstract feature maps of the brain might come from.

T. Kohonen and R. Hari

Trends Neurosci  22  135-9  (1999)

Three types of neuronal organization can be called 'brain maps': sets of feature-sensitive cells, ordered projections between neuronal layers and ordered maps of abstract features.The latter are most intriguing as they reflect the central properties of an organism's experiences and environment. It is proposed that such feature maps are learned in a process that involves parallel input to neurons in a brain area and adaptation of neurons in the neighborhood of the cells that respond most strongly to this input.This article presents a new mathematical formulation for such adaptation and relates it to physiological functions.


Can {H}ebbian volume learning explain discontinuities in cortical maps?

G. Mitchison and N. Swindale

Neural Comput  11  1519-26  (1999)

It has recently been shown that orientation and retinotopic position, both of which are mapped in primary visual cortex, can show correlated jumps (Das \& Gilbert, 1997). This is not consistent with maps generated by Kohonen's algorithm (Kohonen, 1982), where changes in mapped variables tend to be anticorrelated. We show that it is possible to obtain correlated jumps by introducing a Hebbian component (Hebb, 1949) into Kohonen's algorithm. This correspondents to a volume learning mechanism where synaptic facilitation depends not only on the spread of a signal from a maximally active neuron but also requires postsynaptic activity at a synapse. The maps generated by this algorithm show discontinuities across which both orientation and retinotopic position change rapidly, but these regions, which include the orientation singularities, are also aligned with the edges of ocular dominance columns, and this is not a realistic feature of cortical maps. We conclude that cortical maps are better modeled by standard, non-Hebbian volume learning, perhaps coupled with some other mechanism (e.g., that of Ernst, Pawelzik, Tsodyks, \& Sejnowski, 1999) to produce receptive field shifts.


Is the development of orientation selectivity instructed by activity?

K. Miller and E. Erwin and A. Kayser

J Neurobiol  41  44-57  (1999)

Is the development of orientation selectivity in visual cortex instructed by the patterns of neural activity of input neurons? We review evidence as to the role of activity, review models of activity-instructed development, and discuss how these models can be tested. The models can explain the normal development of simple cells with binocularly matched orientation preferences, the effects of monocular deprivation and reverse suture on the orientation map, and the development of a full intracortical circuit sufficient to explain mature response properties including the contrast-invariance of orientation tuning. Existing experiments are consistent with the models, in that (a) selective blockade of ON-center ganglion cells, which will degrade or eliminate the information predicted to drive development of orientation selectivity, in fact prevents development of orientation selectivity; and (b) the spontaneous activities of inputs serving the two eyes are correlated in the lateral geniculate nucleus at appropriate developmental times, as was predicted to be required to achieve binocular matching of preferred orientations. However, definitive tests remain to be done to firmly establish the instructive rather than simply permissive role of activity and determine whether the retinotopically and center type-specific patterns of activity predicted by the models actually exist. We conclude by critically examining alternative scenarios for the development of orientation selectivity and maps, including the idea that maps are genetically prespecified. Copyright 1999 John Wiley \& Sons, Inc.


Learning through maps: functional significance of topographic organization in primary sensory cortex.

M. Diamond and R. Petersen and J. Harris

J Neurobiol  41  64-8  (1999)

The presence of 'maps' in sensory cortex is a hallmark of the mammalian nervous system, but the functional significance of topographic organization has been called into question by physiological studies claiming that patterns of neural behavioral activity transcend topographic boundaries. This paper discusses recent behavioral and physiological studies suggesting that, when animals or human subjects learn perceptual tasks, the neural modifications associated with the learning are distributed according to the spatial arrangement of the primary sensory cortical map. Topographical cortical representations of sensory events, therefore, appear to constitute a true structural framework for information processing and plasticity. Copyright 1999 John Wiley \& Sons, Inc.


Structured long-range connections can provide a scaffold for orientation maps.

H. Shouval and D. Goldberg and J. Jones and M. Beckerman and L. Cooper

J Neurosci  20  1119-28  (2000)

In the visual cortex of the cat and ferret, it is established that maturation of orientation selectivity is shaped by experience-dependent plasticity. However, recent experiments indicate that orientation maps are remarkably stable and experience-independent. We present a model to account for these seemingly paradoxical results. In this model, a scaffold consisting of non-isotropic lateral connections is laid down in horizontal circuitry before visual experience. These lateral connections provide an experience-independent framework for the developing orientation maps by inducing a broad orientation tuning bias in the model neurons. Experience-dependent plasticity of the thalamocortical connections sharpens the tuning while the preferred orientation of the neurons remains unchanged. This model is verified by computer simulations in which the scaffolds are generated both artificially and inferred from experimental optical imaging data. The plasticity is modeled by the BCM synaptic plasticity rule, and the input environment consists of natural images. We use this model to provide a possible explanation of the recent observation in which two eyes without common visual experience develop similar orientation maps. Finally, we propose an experiment involving the disruption of lateral connections to distinguish this model from models proposed by others.


Visual cortex maps are optimized for uniform coverage

N. Swindale and D. Shoham and A. Grinvald and T. Bonhoeffer and M. Hubener

Nat Neurosci  3  822-6  (2000)

Cat visual cortex contains a topographic map of visual space, plus superimposed, spatially periodic maps of ocular dominance, spatial frequency and orientation. It is hypothesized that the layout of these maps is determined by two constraints: continuity or smooth mapping of stimulus properties across the cortical surface, and coverage uniformity or uniform representation of combinations of map features over visual space. Here we use a quantitative measure of coverage uniformity (c') to test the hypothesis that cortical maps are optimized for coverage. When we perturbed the spatial relationships between ocular dominance, spatial frequency and orientation maps obtained in single regions of cortex, we found that cortical maps are at a local minimum for c'. This suggests that coverage optimization is an important organizing principle governing cortical map development.


Analysis of the elastic net model applied to the formation of ocular dominance and orientation columns.

G. J. Goodhill and A. Cimponeriu

Network  11  153-68  (2000)

The development and structure of orientation (OR) and ocular dominance (OD) maps in the primary visual cortex of cats and monkeys can be modelled using the elastic net algorithm, which attempts to find an 'optimal' cortical representation of the input features. Here we analyse this behaviour in terms of parameters of the feature space. We derive expressions for the OR periodicity, and the first bifurcation point as a function of the annealing parameter using the methods of Durbin et al (Durbin R, Szeliski R and Yuille A 1989 Neural Computation 1 348-58). We also investigate the effect of the relative order of OR and OD development on overall map structure. This analysis suggests that developmental order can be predicted from the final OR and OD periodicities. In conjunction with experimentally measured values for these periodicities, the model predicts that (i) in normal macaques OD develops first, (ii) in normal cats OR develops first and (iii) in strabismic cats OD develops first.


How many maps are there in visual cortex?

N. Swindale

Cereb Cortex  10  633-43  (2000)

In addition to a topographic map of the retina, mammalian visual cortex contains superimposed, orderly periodic maps of features such as orientation, eye dominance, direction of motion and spatial frequency. There is evidence that these maps are overlaid so as to ensure that all combinations of the different parameters are represented as uniformly as possible across visual space. However, it is unknown to what extent geometrical factors limit the number of periodic maps which might simultaneously be present, given this constraint. This paper attempts to investigate the question by using a dimension reduction model to generate maps of simple, many- dimensional feature spaces onto a model two-dimensional cortex. The feature space included a model retina, plus N binary variables, corresponding to parameters such as ocular dominance or spatial frequency. The results suggest that geometrical factors do not sharply limit the ability of the cortex to represent combinations of parameters in spatially superimposed maps of similar periodicity. Considerations of uniform coverage suggest an upper limit of six or seven maps. A higher limit, of about nine or ten, may be imposed by the numbers of neurons (or minicolumns) available to represent each of 2(N) features within a given small region of cortex.


Cortical development and remapping through spike timing-dependent plasticity.

S. Song and L. F. Abbott

Neuron  32  339-50  (2001)

Long-term modification of synaptic efficacy can depend on the timing of pre- and postsynaptic action potentials. In model studies, such spike timing-dependent plasticity (STDP) introduces the desirable features of competition among synapses and regulation of postsynaptic firing characteristics. STDP strengthens synapses that receive correlated input, which can lead to the formation of stimulus-selective columns and the development, refinement, and maintenance of selectivity maps in network models. The temporal asymmetry of STDP suppresses strong destabilizing self-excitatory loops and allows a group of neurons that become selective early in development to direct other neurons to become similarly selective. STDP, acting alone without further hypothetical global constraints or additional forms of plasticity, can also reproduce the remapping seen in adult cortex following afferent lesions.


Are visual cortex maps optimized for coverage?

M. A. Carreira-Perpinan and G. J. Goodhill

Neural Comput  14  1545-60  (2002)

The elegant regularity of maps of variables such as ocular dominance, orientation, and spatial frequency in primary visual cortex has prompted many people to suggest that their structure could be explained by an optimization principle. Up to now, the standard way to test this hypothesis has been to generate artificial maps by optimizing a hypothesized objective function and then to compare these artificial maps with real maps using a variety of quantitative criteria. If the artificial maps are similar to the real maps, this provides some evidence that the real cortex may be optimizing a similar function to the one hypothesized. Recently, a more direct method has been proposed for testing whether real maps represent local optima of an objective function (Swindale, Shoham, Grinvald, Bonhoeffer, \& Hubener, 2000). In this approach, the value of the hypothesized function is calculated for a real map, and then the real map is perturbed in certain ways and the function recalculated. If each of these perturbations leads to a worsening of the function, it is tempting to conclude that the real map is quite likely to represent a local optimum of that function. In this article, we argue that such perturbation results provide only weak evidence in favor of the optimization hypothesis.


Mapping multiple features in the population response of visual cortex.

A. Basole and L. E. White and D. Fitzpatrick

Nature  423  986--990  (2003)

Stimulus features such as edge orientation, motion direction and spatial frequency are thought to be encoded in the primary visual cortex by overlapping feature maps arranged so that the location of neurons activated by a particular combination of stimulus features can be predicted from the intersections of these maps. This view is based on the use of grating stimuli, which limit the range of stimulus combinations that can be examined. We used optical imaging of intrinsic signals in ferrets to assess patterns of population activity evoked by the motion of a texture (a field of iso-oriented bars). Here we show that the same neural population can be activated by multiple combinations of orientation, length, motion axis and speed. Rather than reflecting the intersection of multiple maps, our results indicate that population activity in primary visual cortex is better described as a single map of spatiotemporal energy.


The development of retinotectal maps: a review of models based on molecular gradients.

G. J. Goodhill and J. Xu

Network  16  5-34  (2005)

Information about the world is often represented in the brain in the form of topographic maps. A paradigm example is the topographic representation of the visual world in the optic tectum/superior colliculus. This map initially forms during neural development using activity-independent molecular cues, most notably some type of chemospecific matching between molecular gradients in the retina and corresponding gradients in the tectum/superior colliculus. Exactly how this process might work has been studied both experimentally and theoretically for several decades. This review discusses the experimental data briefly, and then in more detail the theoretical models proposed. The principal conclusions are that (1) theoretical models have helped clarify several important ideas in the field, (2) earlier models were often more sophisticated than more recent models, and (3) substantial revisions to current modelling approaches are probably required to account for more than isolated subsets of the experimental data.


Alteration of visual input results in a coordinated reorganization of multiple visual cortex maps.

B. J. Farley and H. Yu and D. Z. Jin and M. Sur

J Neurosci  27  10299--10310  (2007 Sep 19)

In the adult visual cortex, multiple feature maps exist and have characteristic spatial relationships with one another. The relationships can be reproduced by "dimension-reduction" computational models, suggesting that the principles of continuity and coverage may underlie cortical map organization. However, the mechanisms responsible for establishing these relationships are unknown. We explored whether removing one feature map during development causes a coordinated reorganization of the remaining maps or whether the remaining maps are unaffected. We removed the ocular dominance map by monocular enucleation in newborn ferrets, so that single eye stimulation drove the cortex in a more spatially uniform manner in adult monocular animals compared with normal animals. Maps of orientation, spatial frequency, and retinotopy formed in monocular ferrets, but their structures and spatial relationships differed from those in normal ferrets. The wavelength of the orientation map increased, so that the average orientation gradient across the cortex decreased. The decrease in the orientation gradient in monocular animals was most prominent in the high gradient regions of the spatial frequency map, indicating a coordinated reorganization between these two maps. In monocular animals, the orthogonal relationship between the orientation and spatial frequency maps was preserved, and the orthogonal relationship between the orientation and retinotopic maps became more pronounced. These results were consistent with detailed predictions of a dimension-reduction model of cortical organization. Thus, the number of feature maps in a cortical area influences the relationships between them, and inputs to the cortex have a significant role in generating these relationships.


Neuronal selectivity and local map structure in visual cortex.

I. Nauhaus and A. Benucci and M. Carandini and D. L. Ringach

Neuron  57  673--679  (2008)

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.


Spatial relationships among three columnar systems in cat area 17.

M. Hubener and D. Shoham and A. Grinvald and T. Bonhoeffer

J Neurosci  17  9270-84  (1997)

In the primary visual cortex, neurons with similar response properties are arranged in columns. As more and more columnar systems are discovered it becomes increasingly important to establish the rules that govern the geometric relationships between different columns. As a first step to examine this issue we investigated the spatial relationships between the orientation, ocular dominance, and spatial frequency domains in cat area 17. Using optical imaging of intrinsic signals we obtained high resolution maps for each of these stimulus features from the same cortical regions. We found clear relationships between orientation and ocular dominance columns: many iso-orientation lines intersected the borders between ocular dominance borders at right angles, and orientation singularities were concentrated in the center regions of the ocular dominance columns. Similar, albeit weaker geometric relationships were observed between the orientation and spatial frequency domains. The ocular dominance and spatial frequency maps were also found to be spatially related: there was a tendency for the low spatial frequency domains to avoid the border regions of the ocular dominance columns. This specific arrangement of the different columnar systems might ensure that all possible combinations of stimulus features are represented at least once in any given region of the visual cortex, thus avoiding the occurrence of functional blind spots for a particular stimulus attribute in the visual field.