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Postnatal development of the human visual cortex is characterized by an overshooting growth pattern of its volume with a maximum at 8 postnatal months and by loss of a substantial proportion of its neurons. The highest rate of reduction in neuronal numbers is observed in layers II-IVa, with other layers showing a more gradual postnatal decrease.
When images are stabilized on the retina, visual perception fades. During voluntary visual fixation, however, constantly occurring small eye movements, including microsaccades, prevent this fading. We previously showed that microsaccades generated bursty firing in the primary visual cortex (area V-1) in the presence of stationary stimuli. Here we examine the neural activity generated by microsaccades in the lateral geniculate nucleus (LGN), and in the area V-1 of the awake monkey, for various functionally relevant stimulus parameters. During visual fixation, microsaccades drove LGN neurons by moving their receptive fields across a stationary stimulus, offering a likely explanation of how microsaccades block fading during normal fixation. Bursts of spikes in the LGN and area V-1 were associated more closely than lone spikes with preceding microsaccades, suggesting that bursts are more reliable than are lone spikes as neural signals for visibility. In area V-1, microsaccade-generated activity, and the number of spikes per burst, was maximal when the bar stimulus centered over a receptive field matched the cell's optimal orientation. This suggested burst size as a neural code for stimuli optimality (and not solely stimuli visibility). As expected, burst size did not vary with stimulus orientation in the LGN. To address the effectiveness of microsaccades in generating neural activity, we compared activity correlated with microsaccades to activity correlated with flashing bars. Onset responses to flashes were about 7 times larger than the responses to the same stimulus moved across the cells' receptive fields by microsaccades, perhaps because of the relative abruptness of flashes.
The morphology and laminar distribution of norepinephrine (NE) and serotonin (5-hydroxytryptamine, 5-HT) axons in the primary visual cortex of cynomolgus monkeys (Macaca fascicularis) have been analyzed by immunocytochemistry with antibodies directed against dopamine-beta-hydroxylase (DBH) and against 5-HT. The NE and 5-HT innervation of primary visual cortex (area 17) in the monkey exhibit highly differentiated laminar patterns. Both of these monoamine axonal systems form tangentially continuous laminar bands that differ in density, morphology, and predominant orientation of constituent fibers. Serotonin axons, present in all cortical layers, form two especially prominent, dense bands of arborizing fibers; one extending from midlayer III through IVC-alpha and the other from VA through VI. NE axons within cynomolgus visual cortex are markedly less dense than 5-HT axons, and laminar differences in NE density are less prominent. NE axons form two broad bands of moderate density extending through deep and superficial cortical layers, separated by layer IVC, which is conspicuously poor in NE fibers. The laminar complementarity of 5-HT and NE innervation that is a notable feature of the squirrel monkey visual cortex is not present in cynomolgus monkey; in this Old World monkey NE and 5-HT axons show considerable overlap such that the same cortical layers appear to be innervated by both neurotransmitters. By virtue of their laminar distribution, 5-HT and NE axons may each have a selective influence on the intrinsic circuitry of primate cerebral cortex, and, for 5-HT in particular, the specific cellular targets of this influence are likely to differ in New and Old World monkeys.
How do neurons in the primary visual cortex (V1) encode the contrast of a visual stimulus? In this paper, the information that V1 responses convey about the contrast of static visual stimuli is explicitly calculated. These responses often contain several easily distinguished temporal components, which will be called latency, transient, tonic, and off. Calculating the information about contrast conveyed in each component and in groups of components makes it possible to delineate aspects of the temporal structure that may be relevant for contrast encoding. The results indicate that as much or more contrast-related information is encoded into the temporal structure of spike train responses as into the firing rate and that the temporally coded information is manifested most strongly in the latency to response onset. Transient, tonic, and off responses contribute relatively little. The results also reveal that temporal coding is important for distinguishing subtle contrast differences, whereas firing rates are useful for gross discrimination. This suggests that the temporal structure of neurons' responses may extend the dynamic range for contrast encoding in the primate visual system.
The relationships between visual object configurations and interneuronal spike synchronization and gamma oscillations are examined in the present investigation. Cells were initially stimulated with moving, optimally oriented, single 20 degrees -long bars of light, centred on the compound receptive field of a pool of cortical neurons. When this kind of stimulus evoked intrinsic gamma oscillations and/or synchronization, we gradually fractured the original target. In addition, colinearity was ruptured by forming L- and T-shaped configurations. All fractures and discontinuities were introduced well outside the excitatory receptive field. Multiunit activity in the visual cortex (areas 17 and 18) was recorded in anaesthetized cats. Recording sites were separated by 0.4-1.2 mm. The data analysis indicates that gamma oscillations follow a rule by which unfractured bars yielded the highest S/N ratios. Synchronization strength, as revealed by the central peak in cross-correlograms, also seemed to depend upon stimulus configuration. However, the magnitude of the central peak failed to follow a consistent trend. For instance, the greatest magnitude of the central peak occurred for both colinear and orthogonal types of target. Our results support the notion that both gamma oscillations and neuronal synchronization are stimulus-dependent.
Layer 5 neurons in primary visual cortex make putative reciprocal feedback connections to the superficial layers. To test this hypothesis, we employed scanning laser photostimulation combined with intracellular dye injection to examine local functional excitatory inputs to and axonal projections from individual layer 5 neurons in brain slices from monkey V1. In contrast with previous studies of other V1 neurons, layer 5 neurons received significant input from nearly all of the cortical layers, suggesting individual layer 5 cells integrate information from a broad range of input sources. Nevertheless relative strengths of laminar inputs varied across neurons. Cluster analysis of relative strength of laminar inputs to individual layer 5 neurons revealed four discrete clusters representing recurring input patterns; each cluster included both excitatory and inhibitory neurons. Twenty-five of 40 layer 5 neurons fell into two clusters, both characterized by very strong input from superficial layers. These input patterns are consistent with layer 5 neurons providing feedback to superficial layers. The remaining 15 neurons received stronger input from deep layers. Differences in input from layer 4Calpha versus 4Cbeta also suggest specific associations of the magnocellular and parvocellular visual pathways, with populations receiving stronger input from deep versus superficial cortical layers.
Using synthetic aperture magnetometry (SAM) analyses of magnetoencephalographic (MEG) data, we investigated the variation in cortical response magnitude and frequency as a function of stimulus temporal frequency. In two separate experiments, a reversing checkerboard stimulus was used in the right or left lower visual field at frequencies from 0 to 21 Hz. Average temporal frequency tuning curves were constructed for regions-of-interest located within medial visual cortex and V5/MT. In medial visual cortex, it was found that both the frequency and magnitude of the steady-state response varied as a function of the stimulus frequency, with multiple harmonics of the stimulus frequency being found in the response. The maximum fundamental response was found at a stimulus frequency of 8 Hz, whilst the maximum broadband response occurred at 4 Hz. In contrast, the magnitude and frequency content of the evoked onset response showed no dependency on stimulus frequency. Whilst medial visual cortex showed a power increase during stimulation, extra-striate areas such as V5/MT exhibited a bilateral event-related desynchronisation (ERD). The frequency content of this ERD did not depend on the stimulus frequency but was a broadband power reduction across the 5-20 Hz frequency range. The magnitude of this ERD within V5/MT was strongly low-pass tuned for stimulus frequency, and showed only a moderate preference for stimuli in the contralateral visual field.
In the visual cortex some neurons respond more strongly to short stimuli than to long ones. This is referred to as "end-stopping" and has been generally attributed to inhibition. The role of inhibition, however, has been difficult to demonstrate. Moreover, modeling has shown that end-stopping can be created solely from excitation. The roles of excitation and inhibition were investigated using intracellular recordings (Anderson et al., 2001, J. Neurosci. 21: 2104-2112). The results of that study were interpreted in favor of inhibition. The present report re-examines these results and finds that they may be in good, perhaps even better, agreement with an excitation model of end-stopping.
Callosal afferents to the primary visual cortex (area Oc1) mainly originate in the border region between the lateral portion of the primary visual cortex (area Oc1) and the laterally positioned secondary visual cortex (area Oc2L) of the contralateral hemisphere. The extent of this region has been determined by retrograde labeling with horseradish peroxidase (HRP). In normal rats the width of the retrogradely labeled cortical strip is about 0.3 mm. In rats monocularly enucleated from the 23rd up to the 44th ontogenetic day and subsequently injected as adults with HRP into Oc1 ipsilateral to the remaining eye, the perikarya of the callosal afferents from the opposite hemisphere are labeled in the form of significantly wider columns (about 0.8 mm) than in animals enucleated from the 50th ontogenetic day onwards. The latter do not differ from controls.
Neurons in the visual cortex are selectively responsive to light or dark bars presented at particular orientations. On the basis of physiological data, this orientation selectivity is hypothesized as being due at least partially to intracortical inhibitory mechanisms. But this hypothesis has been challenged by intracellular recordings indicating that excitatory inputs themselves are orientation-selective, so inhibition may not contribute to the observed selectivity. Also, there is controversy about the presence of intracortical horizontal connections mediating inhibition for selectivity and about the theoretical validity of such inhibitory connections. Using cross-correlation analysis of the activities of two neurons recorded simultaneously, we find that inhibitory interactions exist between cells with somewhat different, but not orthogonal, orientation preferences. This suggests that intracortical horizontal inhibition operates between 'orientation columns' to sharpen the orientation tuning of cortical neurons.
Neurons in the cat primary visual cortex are selective for particular contour orientations but their responsiveness can vary under certain conditions. After prolonged stimulation (adaptation), the contrast sensitivity of cortical cells is reduced and the 'gain' (the strength of response as a function of contrast) falls. The response to an optimal contour is also reduced when a different stimulus is superimposed on the receptive field in the same eye. Here we report that the sudden appearance of an inappropriate stimulus in one eye can interocularly suppress the activity of cortical neurons if they are already responding to an optimally oriented stimulus in the other eye. In strabismic cats, whose cortical neurons lack binocular facilitation, even contours of similar orientation shown to the two eyes trigger such suppression. This interocular control of cortical responsiveness could serve to veto signals from one eye under conditions that would otherwise cause double vision and perceptual confusion.
Layers II/III of the primary visual cortex contain a regular pattern of histochemically detectable cytochrome oxidase (CO)-rich "puffs," which differ from the interpuff regions in their thalamo-cortical and cortico-cortical connectivity, receptive-field properties, and the density of inhibitory GABA-containing synaptic terminals. We used an immunocytochemical method, in combination with cytochrome oxidase histochemistry, to analyze the spatial relationship between neurons that contain neuropeptide Y (NPY) and the CO puffs. Of a total of 606 neurons, only 2.6% of the NPY-containing cells are located in the puffs, whereas the rest are situated in the interpuffs, or at the interface between puffs and interpuffs. The number of NPY-containing neurons in the puffs is substantially less than that expected in an equal volume of the interpuffs (X2 = 13.86; df = 1; P less than 0.001). These observations indicate that columns containing the puffs may differ also from those in the interpuff regions in that they contain a unique array of chemically and morphologically distinct local circuit neurons.
One hundred cells of the visual cortex were studied using flashes, clicks and light-sound combinations with different delays. Forty nine neurons changed the total number of spikes to click stimulation. Twenty eight cells responded to clicks with specific response pattern. In 23 cells the initial discharge occurred at 60-70 ms after the onset of clicks. In 39 cells the responses to light-sound combinations differed from the responses to flashes. While 16 cells decreased their responses, the addition of sound increased firing in 23 cells. The specific modification of the light-evoked responses under acoustic stimulation were classified into three main categories: 22 cells generated new response patterns, 18 cells showed a re-distribution of peaks in the PTS histogram and three cells demonstrated a desynchronization of the spike discharge. The study of the heteromodal recovery cycle revealed that the majority of the cells increased their firing during 0-100 ms and decreased firing during 200-300 ms of the response time scale. The critical delays between light and sound, resulting in the modification of the response for the majority of the cells, were within 100 ms in both directions.
Whereas single cells in the visual cortex prefer moving light bars, mass-action responses are evoked better by diffuse luminance changes. This discrepancy was investigated by quantitatively comparing the response properties of individual cells with those of a representative group of cells. The latter responses were derived from the single-cell responses, which were obtained from recording in the rabbit. These quantitative estimates of mean responses resolve the discrepancy between the single-cell domain and the mass-action domain: from the single-cell point of view, a properly oriented moving-bar stimulus is much more effective than a diffuse-light stimulus. The corresponding mass-action response to one common moving-bar stimulus, however, is as small as the mean response to a diffuse-light stimulus (which may even be presented at retinotopically non-corresponding sites). The peak intensities of these mass responses are even much stronger with the diffuse-light stimuli. The same conclusions are valid for the cat, as could be verified from published data. The restrictions of the local receptive field concept that may be implied by the mass-action view of cortical activity and the potential functional relevance of mass activities are discussed.
Primary visual coding can be characterized by the receptive field (RF) properties of single neurons. Subject of this paper is our search for a global, second coding step beyond the RF-concept that links related features in a visual scene. In recent models of visual coding, oscillatory activities have been proposed to constitute such linking signals. We tested the neurophysiological relevance of this hypothesis for the visual system. Single and multiple spikes as well as local field potentials were recorded simultaneously from several locations in the primary visual cortex (A17 and A18) using 7 or 19 individually advanceable fiber-microelectrodes (250 or 330 microns apart). Stimulus-evoked (SE)-resonances of 35-85 Hz were found in these three types of signals throughout the visual cortex when the primary coding channels were activated by their specific stimuli. Stimulus position, orientation, movement direction and velocity, ocularity and stationary flicker caused specific SE-resonances. Coherent SE-resonances were found at distant cortical positions when at least one of the primary coding properties was similar. Coherence was found 1) within a vertical cortex column, 2) between neighbouring hypercolumns, and 3) between two different cortical areas. We assume that the coherence of SE-resonances is mediated by recurrent excitatory intra- and inter-areal connections via phase locking between assemblies that represent the linking features of the actual visual scene. Visually related activities are, thus, transiently labelled by a temporal code that signalizes their momentary association.
In adult primary visual cortex (V1), dendritic spines are more persistent than during development. Brain-derived neurotrophic factor (BDNF) increases synaptic strength, and its levels rise during cortical development. We therefore asked whether postsynaptic BDNF signaling through its receptor TrkB regulates spine persistence in adult V1. This question has been difficult to address because most methods used to alter TrkB signaling in vivo affect cortical development or cannot distinguish between pre- and postsynaptic mechanisms. We circumvented these problems by employing transgenic mice expressing a dominant negative TrkB-EGFP fusion protein in sparse pyramidal neurons of the adult neocortex and hippocampus, producing a Golgi-staining-like pattern. In adult V1, expression of dominant negative TrkB-EGFP resulted in reduced mushroom spine maintenance and synaptic efficacy, accompanied by an increase in long and thin spines and filopodia. In contrast, mushroom spine maintenance was unaffected in CA1, indicating that TrkB plays fundamentally different roles in structural plasticity in these brain areas.
The receptive fields of simple cells in visual cortex are composed of elongated on and off subregions. This spatial arrangement is widely thought to be responsible for the generation of orientation selectivity. Neurons with similar orientation preferences cluster in "columns" that tile the cortical surface and form a map of orientation selectivity. It has been proposed that simple cell receptive fields are constructed by the selective pooling of geniculate receptive fields aligned in space. A recent analysis of monosynaptic connections between geniculate and cortical neurons appears to reveal the existence of "wiring rules" that are in accordance with the classical model. The precise origin of the orientation map is unknown, but both genetic and activity-dependent processes are thought to contribute. Here, we put forward the hypothesis that statistical sampling from the retinal ganglion cell mosaic may contribute to the generation of simple cells and provide a blueprint for orientation columns. Results from computer simulations show that the "haphazard wiring" model is consistent with data on the probability of monosynaptic connections and generates orientation columns and maps resembling those found in the cortex. The haphazard wiring hypothesis could be tested by measuring the correlation between the orientation map and the structure of the retinal ganglion cell mosaic of the contralateral eye.
Extending previous investigations of the topographic relationship between ocular dominance and orientation columns in the cat visual cortex the two systems were visualized with transneuronally transported [3H]proline and with activity-dependent uptake of [14C]2-deoxyglucose, respectively. In addition, we used the 2-deoxyglucose method for a functional assay of both columnar systems. To this end, cats were injected with [3H]proline in the right eye. Two weeks later, they were stimulated monocularly through this eye by presenting contours of only a single orientation in the left and contours of many different orientations in the right visual hemifield while 2-deoxyglucose was injected. The patterns of increased 2-deoxyglucose uptake and of terminal labelling were analysed in flat-mount sections of the visual cortices and in frontal sections of the lateral geniculate nuclei. In the lateral geniculate nucleus, regions of increased 2-deoxyglucose uptake are in register with the [3H]proline-labelled laminae of the open eye. In the visual cortex, the hemispheres stimulated with many different orientations showed a rather homogeneous accumulation of 2-deoxyglucose over the entire extent and throughout all layers of area 17. The hemispheres stimulated with a single orientation displayed columnar patterns of orientation domains essentially similar to those obtained with binocular presentation of a single orientation. In particular and despite monocular stimulation, regions of increased 2-deoxyglucose uptake were neither in register with the [3H]proline-labelled terminals of the increased 2-deoxyglucose uptake were neither in register with the [3H]proline-labelled terminals of the stimulated eye in layer IV nor confined to columns of neural tissue above and below these terminals. The maximal horizontal offset between the termination sites of thalamic afferents and activated orientation columns was in the order of 400 microns. These findings suggest several conclusions. (i) In the cat visual cortex, binocular convergence seems to occur so early in cortical processing that monocular stimulation with many orientations leads to a rather homogeneous activation of cortical tissue. (ii) From the termination zones of geniculate afferents activity is apparently distributed already within layer IV to the respective orientation columns. (iii) This horizontal spread of activity could be assured by target cells with radially extending dendrites and/or tangentially oriented fibres.