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Receptive fields and response properties of neurons in layer 4 of ferret visual cortex.

The ferret has become a model animal for studies exploring the development of the visual system. However, little is known about the receptive-field structure and response properties of neurons in the adult visual cortex of the ferret. We performed single-unit recordings from neurons in layer 4 of adult ferret primary visual cortex to determine the receptive-field structure and visual-response properties of individual neurons. In particular, we asked what is the spatiotemporal structure of receptive fields of layer 4 neurons and what is the orientation selectivity of layer 4 neurons? Receptive fields of layer 4 neurons were mapped using a white-noise stimulus; orientation selectivity was determined using drifting, sine-wave gratings. Our results show that most neurons (84%) within layer 4 are simple cells with elongated, spatially segregated, ON and OFF subregions. These neurons are also selective for stimulus orientation; peaks in orientation-tuning curves have, on average, a half-width at half-maximum response of 21.5 +/- 1.2 degrees (mean +/- SD). The remaining neurons in layer 4 (16%) lack orientation selectivity and have center/surround receptive fields. Although the organization of geniculate inputs to layer 4 differs substantially between ferret and cat, our results demonstrate that, like in the cat, most neurons in ferret layer 4 are orientation-selective simple cells.

Animals↗

A synaptic explanation of suppression in visual cortex.

The responses of neurons in the primary visual cortex (V1) are suppressed by mask stimuli that do not elicit responses if presented alone. This suppression is widely believed to be mediated by intracortical inhibition. As an alternative, we propose that it can be explained by thalamocortical synaptic depression. This explanation correctly predicts that suppression is monocular, immune to cortical adaptation, and occurs for mask stimuli that elicit responses in the thalamus but not in the cortex. Depression also explains other phenomena previously ascribed to intracortical inhibition. It explains why responses saturate at high stimulus contrast, whereas selectivity for orientation and spatial frequency is invariant with contrast. It explains why transient responses to flashed stimuli are nonlinear, whereas spatial summation is primarily linear. These results suggest that the very first synapses into the cortex, and not the cortical network, may account for important response properties of V1 neurons.

Action Potentials↗

Split brain acutely and chronically induced in cats causes ipsilateral eye dominance and reduced excitability of cells in the visual cortex.

The ocular dominance distribution and the excitability level of single cells in the callosal projection zone of the visual cortex (area 17-18 boundary), were electrophysiologically studied in acute and in chronic cats following simultaneous (OCX-CCX) and separate transections of the optic chiasm (OCX) and corpus callosum (CCX). Except for a few cells (3.4%) in the acute OCX-CCX cats showing an interhemispheric transfer, as expressed by their contralateral eye response, all other cells had a monocular response to the ipsilateral eye. An ipsilateral monocular response was found in the chronic OCX-CCX cats, even for long survival periods (17.0 months). The result for the OCX cats was similar, as indicated by the major ipsilateral response and the small proportion of cells showing an interhemispheric transfer. No improvement was found with postoperative time; acute OCX cats had 5.0% cells with contralateral input and 1-7 months chronic cats had 1.7-6.5% of these cells. These animals have thus split brain from point of view of the visual cortex; each hemisphere is therefore independent of the other one as far as neuronal functions are concerned. A remarkable reduction in binocularity was found following callosal transection (CCX) both in acute (41.4% binocularly driven cells) and in 3-39 months chronic cats (45.5% cells), in comparison to the control cats (74.2%). This indicates that elimination of the corpus callosum as itself enhances the binocularity diminution in split brain cats. The reduction found in visual responsiveness in our split brain cats (total: 63.2% unresponsive cells), is attributed to the summation of the individual effects of the optic chiasm and corpus callosum transections. A consistent tendency was found in the long chronic in comparison to the acute OCX-CCX, OCX, and CCX cats for a decrease in the responsiveness level with survival time; however, the short chronic OCX-CCX and CCX cats had the maximal proportion of unresponsive cells. It was concluded that the split brain induced in adult cats has a permanent effect on interhemispheric transfer to visual cortex cells. The absence of interhemispheric interaction under these conditions is not compensated by either transfer through anterior parts of the corpus callosum or through other commissures.

Animals↗

Laminar processing of stimulus orientation in cat visual cortex.

One of the most salient features to emerge in visual cortex is sensitivity to stimulus orientation. Here we asked if orientation selectivity, once established, is altered by successive stages of cortical processing. We measured patterns of orientation selectivity at all depths of the cat's visual cortex by making whole-cell recordings with dye-filled electrodes. Our results show that the synaptic representation of orientation indeed changes with position in the microcircuit, as information passes from layer 4 to layer 2+3 to layer 5. At the earliest cortical stage, for simple cells in layer 4, orientation tuning curves for excitation (depolarization) and inhibition (hyperpolarization) had similar peaks (within 0-7 deg, n = 11) and bandwidths. Further, the sharpness of orientation selectivity covaried with receptive field geometry (r = 0.74) - the more elongated the strongest subregion, the shaper the tuning. Tuning curves for complex cells in layer 2+3 also had similar peaks (within 0-4 deg, n = 7) and bandwidths. By contrast, at a later station, layer 5, the preferred orientation for excitation and inhibition diverged such that the peaks of the tuning curves could be as far as 90 deg apart (average separation, 54 deg; n = 6). Our results support the growing consensus that orientation selectivity is generated at the earliest cortical level and structured similarly for excitation and inhibition. Moreover, our novel finding that the relative tuning of excitation and inhibition changes with laminar position helps resolve prior controversy about orientation selectivity at later phases of processing and gives a mechanistic view of how the cortical circuitry recodes orientation.

Action Potentials↗

[The study of the NMDA receptor function in the visual cortex. Summary of habilitation thesis].

PURPOSE: Finding the agents influencing the function of NMDA receptors in the visual cortex. MATERIAL AND METHODS: The experiments were performed on cats aged from three weeks to several years. Recordings were made from single neurons of the visual cortex after iontophoresis of N-methyl-D-aspartate acid, D-2-amino-5-phosphonovaleric acid, D-serine, 7-chlorokynurenic acid. RESULTS: It was found that: 1. Light is one of the factors which has an influence on the development of NMDA receptors in the visual cortex. Rearing cats in the dark is delaying the changes in the function of NMDA receptors, reducing the number of directional sensitive neurons, lowering the firing rate during the visual response. 2. Monocular deprivation is first creating the reduction of the NMDA receptors' contribution to the visual response and later the functional degradation of the synapse. 3. In the Brodmann's 17th area most glycine sites at the NMDA receptors are not saturated by endogenous glycine.

Animals↗

[Dynamic detection of light intensity by cat visual cortex neurons].

Dynamics of intensity functions of neurons in area 17 of the visual cortex was studied by the method of time slices on unanesthetized cats. The intensity functions of the neurons were estimated from successive fragments of responses. In 70% of cases during 40-200 ms after beginning of the stimulus action the preferred intensity changed from lesser to greater brightness. The possible role of this effect in the intensity of time coding by the visual cortex neurons is discussed.

Animals↗

Bottom-up and top-down dynamics in visual cortex.

A key emergent property of the primary visual cortex (V1) is the orientation selectivity of its neurons. Recent experiments demonstrate remarkable bottom-up and top-down plasticity in orientation networks of the adult cortex. The basis for such dynamics is the mechanism by which orientation tuning is created and maintained, by integration of thalamocortical and intracortical inputs. Intracellular measurements of excitatory and inhibitory synaptic conductances reveal that excitation and inhibition balance each other at all locations in the cortex. This balance is particularly critical at pinwheel centers of the orientation map, where neurons receive intracortical input from a wide diversity of local orientations. The orientation tuning of neurons in adult V1 changes systematically after short-term exposure to one stimulus orientation. Such reversible physiological shifts in tuning parallel the orientation tilt aftereffect observed psychophysically. Neurons at or near pinwheel centers show pronounced changes in orientation preference after adaptation with an oriented stimulus, while neurons in iso-orientation domains show minimal changes. Neurons in V1 of alert, behaving monkeys also exhibit short-term orientation plasticity after very brief adaptation with an oriented stimulus, on the time scale of visual fixation. Adaptation with stimuli that are orthogonal to a neuron's preferred orientation does not alter the preferred orientation but sharpens orientation tuning. Thus, successive fixation on dissimilar image patches, as happens during natural vision, combined with mechanisms of rapid cortical plasticity, actually improves orientation discrimination. Finally, natural vision involves judgements about where to look next, based on an internal model of the visual world. Experiments in behaving monkeys in which information about future stimulus locations can be acquired in one set of trials but not in another demonstrate that V1 neurons signal the acquisition of internal representations. Such Bayesian updating of responses based on statistical learning is fundamental for higher level vision, for deriving inferences about the structure of the visual world, and for the regulation of eye movements.

Adaptation, Psychological↗

Magnetic resonance imaging of the visual system in vivo: transsynaptic illumination of V1 and V2 visual cortex.

Brain nuclei directly receiving retinal projections are readily labeled in magnetic resonance images following intraocular injection of manganese (Mn). To assess whether Mn in retinal ganglion cell axons can be transsynaptically delivered to visual cortex, mice that had previously received intraocular Mn injection were anesthetized with isoflurane, and T1-weighted data sets were acquired of the eyes and brain using a 7-T magnetic resonance imaging machine. Image intensity within contralateral brain structures was evaluated by assessing 1) signal-to-noise ratios, 2) mean image intensity, and 3) mean image intensity normalized to facial muscle intensity. Image intensity was increased throughout the visual pathway including within contralateral visual cortex areas V1 and V2L. Mean normalized image intensity was greater by 53% in the ipsilateral optic nerve and by 31% and 28% in the contralateral lateral geniculate nucleus and superior colliculus, respectively (N=5, P<0.02, paired t test). In contralateral visual cortex areas V1 and V2L, image intensity was increased by 7.5% and 6.8%, respectively (P<0.02 for both, paired t test). Power analysis of the different evaluation methods yielded evidence of superior sensitivity using the normalization method. Reconstruction of the visual system based upon threshold analysis allowed simultaneous visualization of all portions of the major retinal projections to the brain. These results support use of high magnetic field MRI imaging and data normalization for in vivo quantitative analysis of the mouse brain visual system including visual cortex.

Animals↗

Differential regulation of substance P and somatostatin in Martinotti cells of the developing cat visual cortex.

In order to determine their morphological development and ontogenetic fate, Martinotti neurons immunoreactive for substance P and somatostatin have been analysed in the cat visual cortex. Martinotti neurons are located in layers V and VI. They are multipolar to bitufted, and most dendrites remain in layers V and VI. Their typical features is the ascending axon, which emerges from an apical dendrite or from the upper pole of the soma. A number of collaterals branch off in layer V, forming a local terminal plexus. The axon then branches into 2-8 collaterals, which ascend as a bundle to layers III and II, where a second terminal plexus is formed. Some collaterals ascend to layer I where they adopt a horizontal course. Horizontal collaterals in the terminal layers V, III, II, and in layer I may reach up to 400 microns in length. Martinotti neurons begin to differentiate perinatally. The quantitative analysis reveals that the initial time course of differentiation of Martinotti cells is very similar in material stained for substance P and for somatostatin. Double immunofluorescence then confirms that the two peptides are colocalized in Martinotti cells of layers V and VI during the early postnatal period. Further, substance P is colocalized with GABA. Substance P expression in Martinotti cells can be observed only in the immature visual cortex. After postnatal day 15, the Martinotti neuron system becomes less and less detectable by substance P immunoreactivity. It declines to virtually undetectable levels after the third postnatal month. The adult visual cortex is almost devoid of substance P-immunoreactive cell bodies, processes and axon terminals. In situ hybridization confirms this finding, revealing beta-preprotachykinin mRNA-expressing cell bodies in layers V and IV at postnatal day (P)6 and P12, but not in the adult cortex. This suggests a downregulation of the substance P expression at the transcriptional level. In contrast, somatostatin-immunoreactive Martinotti cells, most of which have coexpressed substance P during early postnatal life, can still be observed in the adult cortex. Thus, the Martinotti neurons constitute a persisting cell type, although many individual neurons of this type disappear during the second postnatal month by degeneration and cell death. In summary, while somatostatin is permanently expressed in Martinotti neurons in the cat visual cortex, substance P peptide and mRNA are transiently expressed during an early postnatal period, and apparently are downregulated later in development.

Afferent Pathways↗

A computer model of the visual cortex.

A three-layered simulation of the visual cortex was constructed, receiving inputs from 252 retinal photoreceptors. Lateral geniculate body was taken as a simple relay station. In the cortical module afferent neurons with circular receptive fields, orientation selective simple cells, tuned complex cells, excentricity neurons and different kinds of inhibitory neurons were included. The model reproduces neuronal and network responses recorded in experiments and some sensory illusions, of which one is here demonstrated.

Afferent Pathways↗

Neuronal mechanisms underlying stereopsis: how do simple cells in the visual cortex encode binocular disparity?

Binocular neurons in the visual cortex are thought to form the neural substrate for stereoscopic depth perception. How are the receptive fields of these binocular neurons organized to encode the retinal position disparities that arise from binocular parallax? The conventional notion is that the two receptive fields of a binocular neuron have identical shapes, but are spatially offset from the point of retinal correspondence (zero disparity). We consider an alternative disparity-encoding scheme, in which the two receptive fields may differ in shape (or phase), but are centered at corresponding retinal locations. Using a reverse-correlation technique to obtain detailed spatiotemporal receptive-field maps, we provide support for the latter scheme. Specifically, we show that receptive-field profiles for the left and right eyes are matched for cells that are tuned to horizontal orientations of image contours. However, for neurons tuned to vertical orientations, the left and right receptive fields are predominantly dissimilar in shape. These results show that the striate cortex possesses a specialized mechanism for processing vertical contours, which carry the horizontal-disparity information needed for stereopsis. Thus, in a major modification to the traditional notion of the neural basis of stereopsis, we propose that binocular simple cells encode horizontal disparities in terms of phase at multiple spatial scales. Implications of this scheme are discussed with respect to the size-disparity correlation observed in psychophysical studies.

Algorithms↗

The role of retinogeniculate afferents in the development of connections between visual cortex and the dorsal lateral geniculate nucleus.

The role of retinogeniculate afferents in the development of patterns of connections between visual cortex and the lateral geniculate nucleus (LGN) was addressed by studying the effect of bilateral enucleation at birth on those patterns of connections in tree shrew. In normal adult tree shrews there are six LGN cell layers separated by cell-sparse interlaminar spaces. The reciprocal connections between the LGN and visual cortex are restricted to a column running across all six LGN layers; the geniculocortical projection arises from the cell layers while the corticogeniculate projection terminates primarily in the interlaminar spaces. At birth, when the experimental animals were bilaterally enucleated, the retinogeniculate fibers have begun to segregate by eye but neither the cytological characteristics of individual layers nor the interlaminar spaces have yet formed, and the corticogeniculate fibers have not entered the nucleus. Bilateral enucleation does not prevent the development of the cytological characteristics of individual layers but the interlaminar spaces do not develop. The results of [3H]proline/HRP injections into visual cortex in animals bilaterally enucleated at birth indicate that in the absence of retinogeniculate fibers, and thus interlaminar spaces, the corticogeniculate fibers do not concentrate at the laminar borders but instead spread across all six LGN cell layers. Despite the failure of this projection to concentrate at laminar borders, the corticogeniculate fibers do terminate within a restricted projection column.

Animals↗

Geometry of orientation columns in the visual cortex.

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

Electric Stimulation↗

A quantitative study of neuronal and glial numerical density in the visual cortex of the bottlenose dolphin: evidence for a specialized subarea and changes with age.

Neuronal and glial numerical densities were measured in the lateral gyrus of the cerebral hemisphere of dolphins (Tursiops truncatus) from the neonatal period to adulthood. The cortex studied is the area known to be visually excitable in evoked potential studies. Two distinct parts of the adult lateral gyrus are identifiable, one relatively anterior, in which neuronal density is 23,000/mm3, the other more posterior, with almost double this density. In a neonate, the neuronal density in the anterior lateral gyrus was found to be more than double that of the adult. No samples from the immature posterior area were available. Glial density varies much less than neuronal density, both with age and between areas. Soon after birth the glia/neuron ratio is 1.6 in anterior lateral gyrus, rising to around 3 in the adult anterior lateral area, and rather less in the posterior region, where neuronal density is high. We speculate that the existence of a high numerical density of neurons in the posterior part of the dolphin visual cortex could perhaps indicate a specialized area corresponding to the primate primary visual cortex, also known to have high neuronal density.

Age Factors↗

Immunocytochemical localization of enkephalin in the cat visual cortex.

The localization of enkephalin-immunoreactivity in the cat visual cortex (area 17) was analyzed by using immunohistochemical methods with a monoclonal antibody directed against enkephalin. The majority of the immunoreactive product was localized in neuronal processes. The density of immunopositive fibers was greatest in layer VI, with moderate staining in layers I, II, III and V, and the least dense staining in layer IV. Layer IVab neurons showed a striking concentration of immunopositive puncta around their cell bodies. Immunopositive neurons were scarcely present in the visual cortex. They were found in all cortical layers, but mostly in layer VI. The immunopositive neurons were non-pyramidal, mostly multipolar in shape and occasionally bipolar. The results provide anatomical evidence that enkephalin may have modulatory effects on visual cortical neurons.

Animals↗

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.

Animals↗

Photically evoked potentials and afterpotentials recorded from the visual cortex of the unanesthetized hedgehog.

Evoked potentials to visual stimuli (VEP) were recorded from the visual cortex of the unanesthetized hedgehog (Erinaceus europaeus), a primitive placental mammal with relatively little differentiation of cortex and thalamus. The VEPs consisted of several distinct positive and negative voltage deflections. Reproducibility of the response was high, as indicated from the small intrasession and intersession response variability. Rhythmic afterpotentials (AP), previously reported for higher mammals, were readily elicited. They had a lower frequency (3/sec) than APs observed in other mammals. The use of the hedgehog in electrophysiological and psychophysiological research is suggested because data obtained from this primitive placental mammal may shed light on CNS functions of higher mammals, as well as mammalian forms 'lower' on the evolutionary scale.

Animals↗