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.     

Receptive-field properties of neurons in different laminae of visual cortex of the cat

1. Receptive-field properties of neurons in the different layers of the visual cortex of normal adult cats were analyzed quantitatively. Neurons were classified into one of two groups: 1) S-cells, which have discrete on- and/or off-regions in their receptive fields and possess inhibitory side bands; 2) C-cells, which do not have discrete on- and off-regions in their receptive fields but display an on-off response to flashing stimuli. Neurons of this type rarely display side-band inhibition. 2. As a group, S-cells display lower relative degrees of binocularity and are more selective for stimulus orientation than C-cells. In addition, within a given lamina the S-cells have smaller receptive fields, lower cutoff velocities, lower peak responses to visual stimulation, and lower spontaneous activity than do the C-cells. 3. S-cells in all layers of the cortex display similar orientation sensitivities, mean spontaneous discharge rates, peak response to visual stimulation, and degrees of binocularity. 4. Many of the receptive-field properties of cortical cells vary with laminar location. Receptive-field sizes and cutoff velocities of S-cells and of C-cells are greater in layers V and VI than in layers II-IV. For S-cells, preferred velocities are also greater in layers V and VI than in layers II-IV. Furthermore, C-cells in layers V and VI display high mean spontaneous discharge rates, weak orientation preferences, high relative degrees of binocularity, and higher peak responses to visual stimulation when compared to C-cells in layers II and III. 5. The receptive-field properties of cells in layers V-VI of the striate cortex suggest that most neurons that have their somata in these laminae receive afferents from LGNd Y-cells. Hence, our results suggest that afferents from LGNd Y-cells may play a major part in the cortical control of subcortical visual functions.     

Thalamocortical specificity and the synthesis of sensory cortical receptive fields

A persistent and fundamental question in sensory cortical physiology concerns the manner in which receptive fields of layer-4 neurons are synthesized from their thalamic inputs. According to a hierarchical model proposed more than 40 years ago, simple receptive fields in layer 4 of primary visual cortex originate from the convergence of highly specific thalamocortical inputs (e.g., geniculate inputs with on-center receptive fields overlap the on subregions of layer 4 simple cells). Here, we summarize studies in the visual cortex that provide support for this high specificity of thalamic input to visual cortical simple cells. In addition, we review studies of GABAergic interneurons in the somatosensory "barrel" cortex with receptive fields that are generated by a very different mechanism: the nonspecific convergence of thalamic inputs with different response properties. We hypothesize that these 2 modes of thalamocortical connectivity onto subpopulations of excitatory and inhibitory neurons constitute a general feature of sensory neocortex and account for much of the diversity seen in layer-4 receptive fields.     

Functional connectivity between simple cells and complex cells in cat striate cortex

In the cat primary visual cortex, neurons are classified into the two main categories of simple cells and complex cells based on their response properties. According to the hierarchical model, complex receptive fields derive from convergent inputs of simple cells with similar orientation preferences. This model received strong support from anatomical studies showing that many complex cells lie within the range of layer IV simple-cell axons but outside the range of most thalamic axons. Physiological evidence for the model, however, has remained elusive. Here we demonstrate that layer IV simple cells and layer II and III complex cells show correlated firing consistent with monosynaptic connections. As expected from the hierarchical model, all connections were in the direction from the simple cell to the complex cell, most frequently between cells with similar orientation preferences.     

Dynamics of the orientation-tuned membrane potential response in cat primary visual cortex

Neurons in the primary visual cortex are highly selective for stimulus orientation, whereas their thalamic inputs are not. Much controversy has been focused on the mechanism by which cortical orientation selectivity arises. Although an increasing amount of evidence supports a linear model in which orientation selectivity is conferred upon visual cortical cells by the alignment of the receptive fields of their thalamic inputs, the controversy has recently been rekindled with the suggestion that late cortical input--delayed by multiple synapses--could lead to sharpening of orientation selectivity over time. Here we used intracellular recordings in vivo to examine temporal properties of the orientation-selective response to flashed gratings. Bayesian parameter estimation demonstrated that both preferred orientation and tuning width were stable throughout the response to a single stimulus.     

Anatomical evidence of subcortical contributions to the orientation selectivity and columns of the cat's primary visual cortex

Physiological studies have demonstrated a subcortical origin for orientation selectivity and the orientation columns of the primary visual cortex. However, there are no anatomical data showing how subcortical cells contribute to this important property. Optical imaging, combined with 1,1'-dioctadecyl-3,3,3,3'-tetramethylin-docarbocyanine perchlolate (DiI) and biocytin retrograde tracing, reveals that relay cells projecting to a single orientation column representing the horizontal meridian were clustered within 300 microm in the dorsal lateral geniculate nucleus (LGN). Interestingly, some labeled cells were located on a line parallel to an iso-elevation line in the LGN. Thus, according to the quantitative projection of the visual field to the LGN (J. Comp. Neurol. 143 (1971) 101), their receptive fields must distribute horizontally in alignment in the visual field providing the first anatomical evidence for Hubel and Wiesel's model of simple cell receptive fields (J. Physiol. 160 (1962) 106).     

Visual receptive-field properties of cells in area 18 of cat's cerebral cortex before and after acute lesions in area 17.

1. Receptive-field properties of single neurons in cat's cortical area 18 were studied before and after partial bilateral lesions of area 17. 2. The majority of cells recorded from animals with intact visual cortex exhibited orientation selectivity, directional selectivity, and could be independently activated through either eye. All cells responded well to moving targets and nearly all of them exhibited broadly tuned preferences with respect to speed of the target. Over 45% of cells responded optimally or exclusively at very fast (above 50 degrees/s) speeds. 3. The majority of neurons recorded from animals with intact visual cortex responded weakly but clearly to appropriately oriented localized stationary stimuli flashed on and off. About one-third of the cells responded with mixed on-off discharges from all over their receptive field. In the receptive fields of 10% of cells, separate on- and off-discharge regions could be revealed. In the receptive fields of the remaining cells, only on- or only off-discharge regions could be revealed. 4. The majority of neurons recorded after ablation of area 17 were orientation selective; 50% of the cells were also direction selective. All neurons responded well to moving targets; about 65% of them responded optimally or exclusively at very fast target speeds. 5. Destruction of the dorsolateral part of contralaterial area 17 and most of contralateral area 18 caused significant reduction in proportion of cells in area 18 which could be activated through either eye. 6. The majority of neurons recorded after ablation responded to appropriately oriented localized stationary stimuli flashed on and off. Cells with mixed on-off discharge regions all over the receptive field with separate on- and off-discharge regions and with only on- or only off-discharge regions were found. 7. It is concluded that the processing of afferent visual information in area 18 is, to a great extent, independent of the information carried to this area by associational fibers from cells of area 17.     

基于视通路多感受野朝向性关联的轮廓检测方法

基于视通路中各层次的感受野特性以及层次间感受野的关联特性,提出一种图像轮廓检测新方法。根据神经元的放射状树突接收特性,构建检测空间差异性信息的视网膜神经元网络,对轮廓信息进行前级编码;建立LGN细胞的非经典感受野调节机制,结合感受野的层次变换特性,对前级编码结果进行全局调节;提出简单细胞的多感受野朝向性关联模型,模拟初级视皮层简单细胞的方向选择特性;融合多个方向上的轮廓响应,经过非极大值抑制和阈值处理,得到轮廓检测结果。以RuG图库40幅图片为实验对象,检测结果与基准轮廓图的平均P指标为0.43,结果显示该方法能够有效凸显主体轮廓,强化轮廓与纹理边缘的区分度。利用多感受野的层次关联特性,实现图像轮廓信息的编码与检测应用,为研究高级视皮层的图像理解和视觉认知提供新的思路。     

On and off domains of geniculate afferents in cat primary visual cortex

On- and off-center geniculate afferents form two major channels of visual processing that are thought to converge in the primary visual cortex. However, humans with severely reduced on responses can have normal visual acuity when tested in a white background, which indicates that off channels can function relatively independently from on channels under certain conditions. Consistent with this functional independence of channels, we demonstrate here that on- and off-center geniculate afferents segregate in different domains of the cat primary visual cortex and that off responses dominate the cortical representation of the area centralis. On average, 70% of the geniculate afferents converging at the same cortical domain had receptive fields of the same contrast polarity. Moreover, off-center afferents dominated the representation of the area centralis in the cortex, but not in the thalamus, indicating that on- and off-center afferents are balanced in number, but not in the amount of cortical territory that they cover.     

Haphazard wiring of simple receptive fields and orientation columns in visual cortex

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.     

Development of orientation tuning in simple cells of primary visual cortex

Orientation selectivity and its development are basic features of visual cortex. The original model of orientation selectivity proposes that elongated simple cell receptive fields are constructed from convergent input of an array of lateral geniculate nucleus neurons. However, orientation selectivity of simple cells in the visual cortex is generally greater than the linear contributions based on projections from spatial receptive field profiles. This implies that additional selectivity may arise from intracortical mechanisms. The hierarchical processing idea implies mainly linear connections, whereas cortical contributions are generally considered to be nonlinear. We have explored development of orientation selectivity in visual cortex with a focus on linear and nonlinear factors in a population of anesthetized 4-wk postnatal kittens and adult cats. Linear contributions are estimated from receptive field maps by which orientation tuning curves are generated and bandwidth is quantified. Nonlinear components are estimated as the magnitude of the power function relationship between responses measured from drifting sinusoidal gratings and those predicted from the spatial receptive field. Measured bandwidths for kittens are slightly larger than those in adults, whereas predicted bandwidths are substantially broader. These results suggest that relatively strong nonlinearities in early postnatal stages are substantially involved in the development of orientation tuning in visual cortex.     

Gating and control of primary visual cortex by pulvinar

The primary visual cortex (V1) receives its driving input from the eyes via the lateral geniculate nucleus (LGN) of the thalamus. The lateral pulvinar nucleus of the thalamus also projects to V1, but this input is not well understood. We manipulated lateral pulvinar neural activity in prosimian primates and assessed the effect on supra-granular layers of V1 that project to higher visual cortex. Reversibly inactivating lateral pulvinar prevented supra-granular V1 neurons from responding to visual stimulation. Reversible, focal excitation of lateral pulvinar receptive fields increased the visual responses in coincident V1 receptive fields fourfold and shifted partially overlapping V1 receptive fields toward the center of excitation. V1 responses to regions surrounding the excited lateral pulvinar receptive fields were suppressed. LGN responses were unaffected by these lateral pulvinar manipulations. Excitation of lateral pulvinar after LGN lesion activated supra-granular layer V1 neurons. Thus, lateral pulvinar is able to powerfully control and gate information outflow from V1.     

Diverse receptive fields in the lateral geniculate nucleus during thalamocortical development

Most models of thalamocortical development in the visual system assume a homogeneous population of thalamic inputs to the cortex, each with concentric on- or off-center receptive fields. To test this, we made high-resolution spatial maps of receptive fields in the developing ferret lateral geniculate nucleus (LGN). Developing receptive fields (RFs), had a variety of shapes: some concentric, others elongated (like adult cortical receptive fields) and some with 'hot spots' of sensitivity. These receptive fields seemed to arise from convergence of multiple retinal afferents onto LGN neurons. We present a Hebbian model whereby imprecise retinogeniculate connections help refine geniculocortical connections, sharpening both thalamocortical topography and perhaps orientation selectivity.     

Innate and environmental factors in the development of the kitten's visual cortex.

1. This is a study of the receptive fields of 771 cells recorded in the visual cortex of twenty-five kittens reared normally or subjected to various kinds of visual deprivation or environmental manipulation. 2. Kittens deprived of patterned visual experience, by dark rearing or diffuse occlusion of the eyes, have a majority of cirtical neurones with little or no specificity for the orientation or axis of movement of visual stimuli. However, in such deprived animals, especially those younger than 3 weeks, there are a number of genuinely orientation selective cells. They are broadly "turned" (by adult standards), they are almost always of the simple type, are heavily dominated by one eye, and are found mainly in the deeper layers of the cortex, especially layer IV. 3...     

Inhibitory contributions to spatiotemporal receptive-field structure and direction selectivity in simple cells of cat area 17

Intracortical inhibition contributes to direction selectivity in primary visual cortex, but how it acts has been unclear. We investigated this problem in simple cells of cat area 17 by taking advantage of the link between spatiotemporal (S-T) receptive-field structure and direction selectivity. Most cells in layer 4 have S-T-oriented receptive fields in which gradients of response timing across the field confer a preferred direction of motion. Linear summation of responses across the receptive field, followed by a static nonlinear amplification, has been shown previously to account for directional tuning in layer 4. We tested the hypotheses that inhibition acts by altering S-T structure or the static nonlinearity or both. Drifting and counterphasing sine wave gratings were used to measure direction selectivity and S-T structure, respectively, in 17 layer 4 simple cells before and during iontophoresis of bicuculline methiodide (BMI), a GABAA antagonist. S-T orientation was quantified from fits to response temporal phase versus stimulus spatial phase data. Bicuculline reduced direction selectivity and S-T orientation in nearly all cells, and reductions in the two measures were well correlated (r = 0.81) and reversible. Using conventional linear predictions based on response phase and amplitude, we found that BMI-induced changes in S-T structure also accounted well for absolute changes in the amplitude and phase of responses to gratings drifting in the preferred and nonpreferred direction. For each cell we also calculated an exponent used to estimate the static nonlinearity. Bicuculline reduced the exponent in most cells, but the changes were not correlated with reductions in direction selectivity. We conclude that GABAA-mediated inhibition influences directional tuning in layer 4 primarily by sculpting S-T receptive-field structure. The source of the inhibition is likely to be other simple cells with certain spatiotemporal relationships to their target. Despite reductions in the two measures, most receptive fields maintained some directional tuning and S-T orientation during BMI. This suggests that their excitatory inputs, arising from the lateral geniculate nucleus and within area 17, are sufficient to create some S-T orientation and that inhibition accentuates it. Finally, BMI also reduced direction selectivity in 8 of 10 simple cells tested in layer 6, but the reductions were not accompanied by systematic changes in S-T structure. This reflects the fact that S-T orientation, as revealed by our first-order measures of the receptive field, is weak there normally. Inhibition likely affects layer 6 cells via more complex, nonlinear interactions.     

Binocular interaction fields of single units in the cat striate cortex

1. Based on average response histograms to an optimal stimulus, binocular interaction field plots were obtained from twenty-five simple neurones in the striate cortex of the cat. Each binocularly activated cell has two interaction fields, one for each eye. The binocular interaction field for one eye plots the changes in the amplitude of the response from the other eye as the two receptive fields of the binocularly activated cell are moved across one another, first into and then out of alignment in the plane of the optimal stimulus (tangent screen).2. The binocular interaction field provides an important clue to the nature of the spatial organization of the excitatory and inhibitory regions of the monocular receptive field. The commonest type of receptive field organization has regions of inhibition (inhibitory side bands) to either side of the discharge centre in the direction at right angles to the optimal stimulus orientation. As well as inhibition, there are subliminal excitatory effects.3. Binocular interaction fields differ with the various cell types, i.e. cells that are discharged only from the one eye, cells binocularly discharged with very weak or absent monocular responses and cells showing binocularly opposite direction selectivity.4. Marked facilitation to an optimal stimulus occurs when the two receptive fields of a binocularly activated neurone are in accurate alignment. Facilitation switches to depression for very small degrees of receptive field misalignment in a direction at right angles to the optimal stimulus orientation. These observations are of importance in relation to mechanisms for binocular single vision and depth discrimination.     

Direction selectivity in V1 of alert monkeys: evidence for parallel pathways for motion processing

In primary visual cortex (V1) of macaque monkeys, motion selective cells form three parallel pathways. Two sets of direction selective cells, one in layer 4B, and the other in layer 6, send parallel direct outputs to area MT in the dorsal cortical stream. We show that these two outputs carry different types of spatial information. Direction selective cells in layer 4B have smaller receptive fields than those in layer 6, and layer 4B cells are more selective for orientation. We present evidence for a third direction selective pathway that flows through V1 layers 4Cm (the middle tier of layer 4C) to layer 3. Cells in layer 3 are very selective for orientation, have the smallest receptive fields in V1, and send direct outputs to area V2. Layer 3 neurons are well suited to contribute to detection and recognition of small objects by the ventral cortical stream, as well as to sense subtle motions within objects, such as changes in facial expressions.     

Classification of receptive field properties in cat visual cortex

Summary The properties of the receptive fields of visual cortex neurons of cats were studied manually and by a computer controlled system using single lines, double lines and multiple lines (gratings). The multiple selectivities of each of the receptive fields studied make it necessary to abandon the concept that each cell functions as a feature detector. Instead, an attempt was made to classify the receptive field properties with the aim to delineate the transfer functions (of the total networks) served by each property. When tested with one-line stimulus, cells with simple receptive field properties diffefed from cells with complex receptive field properties as to their velocity selectivity (simple: 1 ° to 3 °/s; complex: 4 ° to 10 °/s), spontaneous activity (lower for cells with simple properties), optimal firing rate (lower for cells with simple properties) and receptive field size (smaller for cells with simple properties) but not for orientation and direction selectivity. When tested with a 2-lines moving stimulus, the responses of cells with simple properties were facilitated by the progressive separation of the lines whereas the responses of cells with complex receptive field properties were inhibited. When multiple lines, i.e. gratings, were used, an equivalence between simple and X properties and complex and Y properties was shown, while the sustained/transient classification proved to be independent of the simple/complex (X/Y) classification. Thus, receptive field properties can be classified into three categories: one reflects the input to the receptive fields; a second deals with the interactive properties of the fields; while a third appears more related to the overall properties of the network.This research was supported by a postdoctoral fellowship from the Medical Research Council of Canada to Maurice Ptito, a predoctoral fellowship from the National Research Council of Canada to Maryse C. Lassende and NIMH Grant MH12970 and NIMH Career Research Award MH15214 to Karl H. Pribram     

Corticogeniculate neurons, corticotectal neurons, and suspected interneurons in visual cortex of awake rabbits: receptive-field properties, axonal properties, and effects of EEG arousal

The intrinsic stability of the rabbit eye was exploited to enable receptive-field analysis of antidromically identified corticotectal (CT) neurons (n = 101) and corticogeniculate (CG) neurons (n = 124) in visual area I of awake rabbits. Eye position was monitored to within 1/5 degrees. We also studied the receptive-field properties of neurons synaptically activated via electrical stimulation of the dorsal lateral geniculate nucleus (LGNd). Whereas most CT neurons had either complex (59%) or motion/uniform (15%) receptive fields, we also found CT neurons with simple (9%) and concentric (4%) receptive fields. Most complex CT cells were broadly tuned to both stimulus orientation and velocity, but only 41% of these cells were directionally selective. We could elicit no visual responses from 6% of CT cells, and these cells had significantly lower conduction velocities than visually responsive CT cells. The median spontaneous firing rates for all classes of CT neurons were 4-8 spikes/s. CG neurons had primarily simple (60%) and concentric (9%) receptive fields, and none of these cells had complex receptive fields. CG simple cells were more narrowly tuned to both stimulus orientation and velocity than were complex CT cells, and most (85%) were directionally selective. Axonal conduction velocities of CG neurons (mean = 1.2 m/s) were much lower than those of CT neurons (mean = 6.4 m/s), and CG neurons that were visually unresponsive (23%) had lower axonal conduction velocities than did visually responsive CG neurons. Some visually unresponsive CG neurons (14%) responded with saccadic eye movements. The median spontaneous firing rates for all classes of CG neurons were less than 1 spike/s. All neurons synaptically activated via LGNd stimulation at latencies of less than 2.0 ms had receptive fields that were not orientation selective (89% motion/uniform, 11% concentric), whereas most cells with orientation-selective receptive fields had considerably longer synaptic latencies. Most short-latency motion/uniform neurons responded to electrical stimulation of the LGNd (and visual area II) with a high-frequency burst (500-900 Hz) of three or more spikes. Action potentials of these neurons were of short duration, thresholds of synaptic activation were low, and spontaneous firing rates were the highest seen in rabbit visual cortex. These properties are similar to those reported for interneurons in several regions in mammalian central nervous system. Nonvisual sensory stimuli that resulted in electroencephalographic arousal (hippocampal theta activity) had a profound effect on the visual responses of many visual cortical neurons.(ABSTRACT TRUNCATED AT 400 WORDS)