Intracortical Connections Research Articles

Extraction of perceptually salient contours by striate cortical networks.

We present a cortical-based model for computing the perceptual salience of contours embedded in noisy images. It has been suggested that horizontal intra-cortical connections in primary visual cortex may modulate contrast detection thresholds and pre-attentive "pop-out". In our model, horizontal connections mediate context-dependent facilitatory and inhibitory interactions among oriented cells. Strongly facilitated cells undergo temporal synchronization; and perceptual salience is determined by the level of synchronized activity. The model accounts for a range of reported psychophysical and physiological effects of contour salience. In particular, the model proposes that intrinsic properties of synchronization account for the increased salience of smooth, closed contours. Application of the model to real images is demonstrated.

The influence of neural activity and intracortical connectivity on the periodicity of ocular dominance stripes

Several factors may interact to determine the periodicity of ocular dominance stripes in cat and monkey visual cortex. Previous theoretical work has suggested roles for the width of cortical interactions and the strength of between-eye correlations. Here, a model based on an explicit optimization is presented that allows a thorough characterization of how these and other parameters of the afferent input could affect ocular dominance stripe periodicity. The principle conclusions are that increasing the width of within-eye correlations leads to wider columns, and, surprisingly, that increasing the width of cortical interactions can sometimes lead to narrower columns.

Sensitive period for lesion-induced reorganization of intracortical projections within the vibrissae representation of rat's primary somatosensory cortex.

Previous experiments from this laboratory demonstrated that intracortical connections in lamina IV of the rat primary somatosensory cortex (SI) are most dense outside the patches of cytochrome oxidase (CO) staining that correspond to the mystacial vibrissae. This pattern of intracortical connections becomes apparent on postnatal day 4 (P-4), at least 2 days after the appearance of the vibrissae-related pattern of thalamocortical afferents. Transection of the infraorbital nerve (ION) on the day of birth (P-0) disrupts both the CO and intracortical projection patterns. This series of experiments was undertaken to determine whether the patterning of either thalamocortical afferents or intracortical projections defines the end of the period over which peripheral damage can alter intracortical projections in lamina IV of SI. The infraorbital nerve (ION) was transected in different cohorts of rats on P-1 through P-5, and animals were allowed to survive > or =45 days, at which time biotinylated dextran amine (BDA) injections were made into the SI. After 7 days, animals were killed, and alternate cortical sections were processed for the demonstration of BDA or CO. Transection of the ION on P-1 or P-2 altered the patterning of both CO and intracortical connections in the SI. In contrast, cutting the ION on P-3 left the pattern of CO densities in the SI intact, but significantly altered the patterning of intracortical connections. Transection of the nerve on P-5 resulted in qualitatively and quantitatively normal patterns of both CO densities and BDA-labelled intracortical projections. These results indicate that the establishment of a stable barrel pattern in layer IV of the SI is not sufficient for normal adult patterning of intracortical projections in this lamina. However, once the mature pattern of intracortical projections in layer IV is established, ION lesions can no longer alter it.

Intracortical connections are not required for oscillatory activity in the visual cortex

Synchronized oscillatory discharge in the visual cortex has been proposed to underlie the linking of retinotopically disparate features into perceptually coherent objects. These proposals have largely relied on the premise that the oscillations arise from intracortical circuitry. However, strong oscillations within both the retina and the lateral geniculate nucleus (LGN) have been reported recently. To evaluate the possibility that cortical oscillations arise from peripheral pathways, we have developed two plausible models of single cell oscillatory discharge that specifically exclude intracortical networks. In the first model, cortical oscillatory discharge near 50 Hz in frequency arises from the integration of signals from strongly oscillatory cells within the LGN. The model also predicts the incidence of 50-Hz oscillatory cells within the cortex. Oscillatory discharge around 30 Hz is explained in a second model by the presence of intrinsically oscillatory cells within cortical layer 5. Both models generate spike trains whose power spectra and mean firing rates are in close agreement with experimental observations of simple and complex cells. Considered together, the two models can largely account for the nature and incidence of oscillatory discharge in the cat's visual cortex. The validity of these models is consistent with the possibility that oscillations are generated independently of intracortical interactions. Because these models rely on intrinsic stimulus-independent oscillators within the retina and cortex, the results further suggest that oscillatory activity within the cortex is not necessarily associated with the processing of high-order visual information.

Intracortical connections are not required for oscillatory activity in the visual cortex: Erratum

Due to a software translation incompatibility, errors were introduced in the final version of the manuscript submitted for the above publication.

Optically imaged maps of orientation preference in primary visual cortex of cats and ferrets

Feature maps in the cerebral cortex constitute orderly representations of response features created within the cortex; an example is the mapping of orientation-selective neurons in visual cortex. We have compared the properties of orientation maps in area 17 of cats and ferrets, obtained by optical imaging of intrinsic signals. Orientation maps in both species contain a quasi-periodic distribution of iso-orientation domains that are organized into a lattice of pinwheels. However, the spatial density of orientation domains and of pinwheels in ferret area 17 is nearly twice that in cat area 17. The ferret map also contains more discontinuities, or fractures, where orientation changes abruptly. The size of orientation domains scales with interdomain spacing, so that the ratio of the two is approximately the same in both species. Consistent with this finding, the orientation tuning width of individual pixels is similar in the two. The magnitude of orientation preference, however, is much lower in ferret compared to cat. The greater incidence of fractures in ferret appears to be due to proportionately greater overlap between domains of different orientations, particularly along fracture lines that link pinwheel centers. We hypothesize that a key determinant of orientation maps, the relationship between orientation domain size and spacing, expresses an anatomical link between sizes of thalamocortical arbors and horizontal intracortical connections in area 17.

How do wiring molecules specify cortical connections?

The laminar and columnar organization of the cortex is reflected in the projections to and from the cortex and in the intracortical connections. During development of the cerebral cortex, growing axons are able to distinguish between the different cortical layers, and cortical axons originating from different laminae respond to different layer-specific signals. Here we consider some experimental systems for identifying mechanisms that contribute to the elaboration of layer-specific cortical connections.

Intracortical connections are not required for oscillatory activity in the visual cortex

Synchronized oscillatory discharge in the visual cortex has been proposed to underlie the linking of retinotopically disparate features into perceptually coherent objects. These proposals have largely relied on the premise that the oscillations arise from intracortical circuitry. However, strong oscillations within both the retina and the lateral geniculate nucleus (LGN) have been reported recently. To evaluate the possibility that cortical oscillations arise from peripheral pathways, we have developed two plausible models of single cell oscillatory discharge that specifically exclude intracortical networks. In the first model, cortical oscillatory discharge near 50 Hz in frequency arises from the integration of signals from strongly oscillatory cells within the LGN. The model also predicts the incidence of 50-Hz oscillatory cells within the cortex. Oscillatory discharge around 30 Hz is explained in a second model by the presence of intrinsically oscillatory cells within cortical layer 5. Both models generate spike trains whose power spectra and mean firing rates are in close agreement with experimental observations of simple and complex cells. Considered together, the two models can largely account for the nature and incidence of oscillatory discharge in the cat's visual cortex. The validity of these models is consistent with the possibility that oscillations are generated independently of intracortical interactions. Because these models rely on intrinsic stimulus-independent oscillators within the retina and cortex, the results further suggest that oscillatory activity within the cortex is not necessarily associated with the processing of high-order visual information.

Hand/Face Border as a Limiting Boundary in the Body Representation in Monkey Somatosensory Cortex

Horizontal intracortical connections may form one substrate for representational plasticity in somatosensory cortex. Electrophysiological mapping demonstrated the finer details of the representations of the hand, lower jaw, neck, and face in area 3b of normal macaque monkeys. Injections of two fluorescent tracers then defined the extent to which horizontal connections crossed from the face into the hand representations and vice versa in area 3b. Connections are widely distributed within cortical representations of skin areas innervated by cervical nerves or by the trigeminal nerve but do not cross a border defined by the anterior limit of the representation of skin innervated by the second cervical nerve. This border separates the representation of the muzzle, innervated only by the mandibular nerve, and the representation of the lower jaw and neck region, innervated by the second and third cervical nerves but overlapped by the mandibular nerve. Thus, the muzzle representation lacks connections with the hand and with the lower jaw and neck representations, but the representations of the hand and of the lower jaw and neck are strongly interconnected. Overlap of the hand and of the lower jaw and neck representations and of their horizontal intracortical connections may form one basis for expansions of the lower jaw representation into that of the hand when peripheral input from the hand is lost. Lack of connections with the rest of the face representation may limit this spread.

Dynamic Spatiotemporal Restructuring of Visual Receptive Fields through Selective Attention: A Model

Cells in the lateral geniculate nucleus (LGN) strongly change their behaviour covarying with different EEG states. During sleep and drowsiness (synchronised alpha, delta-wave EEG) short transient responses prevail whereas during a desynchronised ‘alert’ EEG (beta-waves) long-lasting tonic responses are observed. We propose that this is part of a mechanism used to restructure the spatial and temporal characteristics of the receptive fields in LGN and cortex reflecting changing states of selective attention. To this end we present a model of the primary visual pathway using integrate-and-fire neurons to simulate the afferent signal flow (retina, LGN, V1). The model also implements excitatory topographically arranged lateral intracortical and corticofugal connections which act as a positive feedback and trigger spatial winner-takes-all (WTA) mechanisms enhanced by lateral inhibition at both levels. Furthermore, the LGN membrane characteristic can switch from phasic (hyperpolarised) low-threshold Ca2+ bursting mode to tonic (depolarised) signal-transmission mode. Switching is triggered by feedback and amplified by intracellular intrinsic positive-feedback mechanisms in the model LGN. All positive-feedback mechanisms are subject to damping such that they remain ineffective below a certain threshold. Salient stimuli which ‘attract attention’ will push the system above threshold and a self-amplifying process is started which sharpens the cortical receptive fields spatially (by spatial WTA) and drives the winners in the LGN into signal transmission mode (by intrinsic intracellular mechanisms). These results predicted by the model are in accordance with LGN cell behaviour. In addition, the model predicts that cortical receptive fields should be wider during synchronised EEG than during desynchronised EEG.

Functional Specificity of Long-Range Intrinsic and Interhemispheric Connections in the Visual Cortex of Strabismic Cats

The development of both long-range intracortical and interhemispheric connections depends on visual experience. Previous experiments showed that in strabismic but not in normal cats, clustered horizontal axon projections preferentially connect cell groups activated by the same eye. This indicates that there is selective stabilization of fibers between neurons exhibiting correlated activity. Extending these experiments, we investigated in strabismic cats: (1) whether tangential connections remain confined to columns of similar orientation preference within the subsystems of left and right eye domains; and (2) whether callosal connections also extend predominantly between neurons activated by the same eye and preferring similar orientations. To this end, we analyzed in strabismic cats the topographic relationships between orientation preference domains and both intrinsic and callosal connections of area 17. Red and green latex microspheres were injected into monocular iso-orientation domains identified by optical imaging of intrinsic signals. Additionally, domains sharing the ocular dominance and orientation preference of the neurons at the injection sites were visualized by 2-deoxyglucose (2-DG) autoradiography. Quantitative analysis revealed that 56% of the retrogradely labeled cells within the injected area 17 and 60% of the transcallosally labeled neurons were located in the 2-DG-labeled iso-orientation domains. This indicates: (1) that strabismus does not interfere with the tendency of long-range horizontal fibers to link predominantly neurons of similar orientation preference; and (2) that the selection mechanisms for the stabilization of callosal connections are similar to those that are responsible for the specification of the tangential intrinsic connections.

The perceptual grouping criterion of colinearity is reflected by anisotropies of connections in the primary visual cortex.

An important step in the processing of visual patterns is the segmentation of the retinal image. Neuronal responses evoked by the contours of individual objects need to be identified and associated for further joint processing. These grouping operations are based on a number of Gestalt criteria. Here we report that connections in the visual cortex of the cat exhibit a highly significant anisotropy, preferentially linking neurons activated by contours that have similar orientation and are aligned colinearly. These anatomical data suggest a close relation between the perceptual grouping criterion of colinearity and the topology of tangential intracortical connections. We propose that tangential intracortical connections support perceptual grouping by modulating the saliency of distributed cortical responses in a context-dependent way. The present data are compatible with the hypothesis that the criteria for this grouping operation are determined by the architecture of the tangential connections.

The columnar organization of the neocortex.

The modular organization of nervous systems is a widely documented principle of design for both vertebrate and invertebrate brains of which the columnar organization of the neocortex is an example. The classical cytoarchitectural areas of the neocortex are composed of smaller units, local neural circuits repeated iteratively within each area. Modules may vary in cell type and number, in internal and external connectivity, and in mode of neuronal processing between different large entities; within any single large entity they have a basic similarity of internal design and operation. Modules are most commonly grouped into entities by sets of dominating external connections. This unifying factor is most obvious for the heterotypical sensory and motor areas of the neocortex. Columnar defining factors in homotypical areas are generated, in part, within the cortex itself. The set of all modules composing such an entity may be fractionated into different modular subsets by different extrinsic connections. Linkages between them and subsets in other large entities form distributed systems. The neighborhood relations between connected subsets of modules in different entities result in nested distributed systems that serve distributed functions. A cortical area defined in classical cytoarchitectural terms may belong to more than one and sometimes to several distributed systems. Columns in cytoarchitectural areas located at some distance from one another, but with some common properties, may be linked by long-range, intracortical connections.

A Function of Neural Networks Generating End- and Side-inhibition in the Primary Visual Cortex

Considering results of recent neurophysiological experiments (Deangelis et al. (1994), Length and width tuning of neurons in the cat's primary visual cortex, Journal of Neurophysiology, 71, 347–374) a model and a function of neural networks generating end- and side-inhibition in the primary visual cortex are proposed. The proposed neural network model consists of intracortical connections, and is the extension of a model proposed by Bolz et al. (Bolz et al. (1989)), Pharmacological analysis of cortical circuitry, Trends in Neuroscience, 12, 292–296). The proposed function is to extract important neuronal responses which represent main visual informations, for example, lines and edges which construct visual objects, removing excess neuronal responses before they are transmitted to higher visual areas in the cortex. © 1997 Elsevier Science Ltd. All Rights Reserved.

Functional periodic intracortical couplings induced by structured lateral inhibition in a linear cortical network.

The spatial organization of cortical axon and dendritic fields could be an interesting structural paradigm to obtain a functional specificity without postulating highly specific feedforward connections. In this article, we investigate the functional implications of recurrent intracortical inhibition when it occurs through clustered medium-range interconnection schemes (Wörgötter & Koch, 1991; Somogyi, 1989; Kritzer, Cowey, & Somogyi, 1992). Moreover, the interaction between the inhibitory schemes and visual orientation maps is explored. Assuming linearity, we show that clustered inhibitory mechanisms can trigger a propagation process that allows the development of extra (i.e., induced) interactions among the cortical sites involved in the recurrent loops. In addition, we point out how these interactions functionally modify the response of cortical simple cells and yield to highly structured Gabor-like receptive fields. This study should be considered not as a realistic biological model of the primary visual cortex but as an attempt to explain possible computational principles related to intracortical connectivity and to the underlying single-cell properties.

A computational model of acute focal cortical lesions.

Determining how cerebral cortex adapts to sudden focal damage is important for gaining a better understanding of stroke. In this study we used a computational model to examine the hypothesis that cortical map reorganization after a simulated infarct is critically dependent on perilesion excitability and to identify factors that influence the extent of poststroke reorganization. A previously reported artificial neural network model of primary sensorimotor cortex, controlling a simulated arm, was subjected to acute focal damage. The perilesion excitability and cortical map reorganization were measured over time and compared. Simulated lesions to cortical regions with increased perilesion excitability were associated with a remapping of the lesioned area into the immediate perilesion cortex, where responsiveness increased with time. In contrast, when lesions caused a perilesion zone of decreased activity to appear, this zone enlarged and intensified with time, with loss of the perilesion map. Increasing the assumed extent of intracortical connections produced a wider perilesion zone of inactivity. These effects were independent of lesion size. These simulation results suggest that functional cortical reorganization after an ischemic stroke is a two-phase process in which perilesion excitability plays a critical role.

PARALLEL ORGANIZATION OF SOMATOSENSORY CORTICAL AREAS I AND II FOR TACTILE PROCESSING

1. The two principal tactile processing areas in the cerebral cortex, somatosensory areas I and II, receive direct projections from the thalamus and, as well, are linked through intracortical reciprocal connections. Tactile information may therefore be conveyed to SII, for example, over either a direct path from the thalamus or an indirect, or serial, path from the thalamus via SI. 2. Reports in recent years that tactile responsiveness within the hand area of SII was abolished by surgical ablation of the hand area of the postcentral, or SI area of the cortex in the macaque and marmoset monkeys indicated that a serial processing scheme may operate at least in primates. However, as the surgical ablation is clearly irreversible and precludes examination of individual SII neurons in both the control and test circumstances, that is, when SI is intact and when it is inactivated, we have examined in the cat, the rabbit and the marmoset monkey the behaviour of SII neurons before, during and after the selective, rapidly-reversible inactivation of SI by means of localized cooling. 3. The results demonstrate that in the cat and rabbit, SII responsiveness is never abolished and infrequently affected by SI inactivation and that tactile inputs to SII therefore traverse a direct path from thalamus, organized in parallel with that to SI. In the marmoset (Callithrix jacchus), in contrast to earlier studies based on ablation of SI we found that with reversible inactivation of SI, SII responsiveness was unaffected in 25% of neurons and, although reduced in the remainder, was rarely abolished (< 10% of SII neurons). 4. The results indicate that there is substantial direct thalamic input to SII, even in this simian primate, and therefore necessitate revision of the hypothesis that tactile processing at the thalamocortical level in simian primates is based on a strict serial scheme in which tactile information is conveyed from the thalamus to SI and thence to SII.

Control of spatiotemporal coherence of a thalamic oscillation by corticothalamic feedback.

The mammalian thalamus is the gateway to the cortex for most sensory modalities. Nearly all thalamic nuclei also receive massive feedback projections from the cortical region to which they project. In this study, the spatiotemporal properties of synchronized thalamic spindle oscillations (7 to 14 hertz) were investigated in barbiturate-anesthetized cats, before and after removal of the cortex. After complete ipsilateral decortication, the long-range synchronization of thalamic spindles in the intact cortex hemisphere changed into disorganized patterns with low spatiotemporal coherence. Local thalamic synchrony was still present, as demonstrated by dual intracellular recordings from nearby neurons. In the cortex, synchrony was insensitive to the disruption of horizontal intracortical connections. These results indicate that the global coherence of thalamic oscillations is determined by corticothalamic projections.

Functional GABAergic Synaptic Connection in Neonatal Mouse Barrel Cortex

Intracortical inhibition is crucial to proper functioning of the mature neocortex, yet, paradoxically, is reported to be rare or absent in the neonatal animal. We reexamined this issue by recording whole-cell postsynaptic currents (PSCs) of barrel cortex neurons in thalamocortical brain slices from neonatal mice. Monosynaptic, excitatory thalamocortical responses were elicited in layers V/VI neurons as early as postnatal day 0 (P0, the first 24 hr after birth) and in presumptive layer IV as early as P2. At very low stimulation frequencies, the monosynaptic response was invariably followed by a prolonged (up to 1 sec) synaptic barrage, which fatigued at stimulus repetition rates of 2/min or higher. This barrage consisted of postsynaptic responses to spiking activity in neighboring cortical cells, because (1) it could also be evoked by intracortical stimulation in coronal slices and (2) it was abolished by antagonists to NMDA receptors (NMDARs), even when NMDARs on the recorded cell were under a voltage-dependent block. Some of the larger polysynaptic events changed polarity at a negative reversal potential and were blocked by GABAA receptor (GABAAR) antagonists, with a concurrent enhancement of the extracellular field potential, indicating that they were GABAAR- mediated, CI-dependent inhibitory PSCs (IPSCs). We conclude that a network of functional intracortical GABAAR-mediated synaptic connections exists from the earliest postnatal ages, although it gives rise to responses that differ from mature IPSCs in reversal potential and latency.

Development and plasticity of local intracortical projections within the vibrissae representation of the rat primary somatosensory cortex.

Labelling with 1,1'-dioctadecyl-3,3,3',3'-tetramethylindocarbocyanine perchlorate (Di-A) was used to assess the development of projections within the primary somatosensory cortex (SI) of rats aged between postnatal day 2 and 8 (P-2 and P-8). 1,1'-Dioctadecyl-3,3,3,"3'-tetramethylindocarbocyanine perchlorate (Di-I) was used in these same animals to label thalamocortical afferents. Particular attention was paid to the emergence of lamina IV intracortical projections that form a pattern complementary to vibrissae-related thalamocortical afferents. A vibrissae-related pattern of Di-A-labelled cells and fibers that was restricted largely to the septa regions was not apparent in rats killed on P-2, but it was visible in animals killed on P-4 and later ages. Tracing with biotinylated dextran amine (BDA) was used to assess intra-SI projections of adult rats that sustained transection of the infraorbital nerve (ION) on P-0 or P-7 or implantation of a tetrodotoxin (TTX)-impregnated polymer chip over the cortex on P-0. Rats that sustained ION transection on P-7 or that had TTX implants demonstrated normal patterns of projections within SI. The patterns of labelling in the supra- and infragranular layers of the cortices of the rats that sustained ION transection on P-0 were generally similar to those in the other groups evaluated. However, in lamina IV, there was no organization that could be related to the distribution of the vibrissae. These results indicate that the vibrissae-related pattern of intracortical projections within SI develops shortly after birth and that two manipulations that alter cortical activity, but not the patterning of thalamocortical afferents (application of TTX and transection of the ION after thalamocortical afferent patterns are established), have no significant effect on it. However, a manipulation that alters thalamocortical development (transection of the ION on P-0) profoundly affects the patterning of intracortical connections.