A comparison of inhibition in orientation and spatial frequency selectivity of cat visual cortex

Neurones in the visual cortex are highly selective for orientation and spatial frequency of visual stimuli. There is strong neurophysiological evidence that orientation selectivity is enhanced by inhibitory interconnections between columns in the cortex which have different orientation sensitivities, an idea which is supported by experiments using neuropharmacological manipulation or complex visual stimuli. It has also been proposed that selectivity for spatial frequency is mediated in part by a similar mechanism to that for orientation, although evidence for this is based on special use of visual stimuli, which hampers interpretation of the findings. We have therefore examined selectivity for both orientation and spatial frequency using a technique which allows direct inferences about inhibitory processes. Our method uses microiontophoresis of an excitatory amino acid to elevate maintained discharge of single neurones in the visual cortex. We then present visual stimuli both within and outside the range of orientations and spatial frequencies which cause a cell to respond with increased discharge. Our results show that orientations presented on either side of the responsive range usually produce clear suppression of maintained discharge. In marked contrast, spatial frequencies shown to either side of the responsive range have little or no effect on maintained activity. We conclude that there is an intracortical organization of inhibitory connections between cells tuned to different orientations but not different spatial frequencies.     

Iso-orientation domains in cat visual cortex are arranged in pinwheel-like patterns

The mammalian cortex is organized in a columnar fashion: neurons lying below each other from the pia to the white matter usually share many functional properties. Across the cortical surface, cells with similar response properties are also clustered together, forming elongated bands or patches. Some response properties, such as orientation preference in the visual cortex, change gradually across the cortical surface forming 'orientation maps'. To determine the precise layout of iso-orientation domains, knowledge of responses not only to one but to many stimulus orientations is essential. Therefore, the exact depiction of orientation maps has been hampered by technical difficulties and remained controversial for almost thirty years. Here we use in vivo optical imaging based on intrinsic signals to gather information on the responses of a piece of cortex to gratings in many different orientations. This complete set of responses then provides detailed information on the structure of the orientation map in a large patch of cortex from area 18 of the cat. We find that cortical regions that respond best to one orientation form highly ordered patches rather than elongated bands. These iso-orientation patches are organized around 'orientation centres', producing pinwheel-like patterns in which the orientation preference of cells is changing continuously across the cortex. We have also analysed our data for fast changes in orientation preference and find that these 'fractures' are limited to the orientation centres. The pinwheels and orientation centres are such a prominent organizational feature that it should be important to understand their development as well as their function in the processing of visual information.     

Topography of contextual modulations mediated by short-range interactions in primary visual cortex.

Neurons in primary visual cortex (V1) respond differently to a simple visual element presented in isolation from when it is embedded within a complex image. This difference, a specific modulation by surrounding elements in the image, is mediated by short- and long-range connections within V1 and by feedback from other areas. Here we study the role of short-range connections in this process, and relate it to the layout of local inhomogeneities in the cortical maps of orientation and space. By measuring correlation between neuron pairs located in optically imaged maps of V1 orientation columns we show that the strength of local connections between cells is a graded function of lateral separation across cortex, largely radially symmetrical and relatively independent of orientation preferences. We then show the contextual influence of flanking visual elements on neuronal responses varies systematically with a neuron's position within the cortical orientation map. The strength of this contextual influence on a neuron can be predicted from a model of local connections based on simple overlap with particular features of the orientation map. This indicates that local intracortical circuitry could endow neurons with a graded specialization for processing angular visual features such as corners and T junctions, and this specialization could have its own functional cortical map, linked with the orientation map.     

Global and fine information coded by single neurons in the temporal visual cortex.

When we see a person's face, we can easily recognize their species, individual identity and emotional state. How does the brain represent such complex information? A substantial number of neurons in the macaque temporal cortex respond to faces. However, the neuronal mechanisms underlying the processing of complex information are not yet clear. Here we recorded the activity of single neurons in the temporal cortex of macaque monkeys while presenting visual stimuli consisting of geometric shapes, and monkey and human faces with various expressions. Information theory was used to investigate how well the neuronal responses could categorize the stimuli. We found that single neurons conveyed two different scales of facial information in their firing patterns, starting at different latencies. Global information, categorizing stimuli as monkey faces, human faces or shapes, was conveyed in the earliest part of the responses. Fine information about identity or expression was conveyed later, beginning on average 51 ms after global information. We speculate that global information could be used as a 'header' to prepare destination areas for receiving more detailed information.     

Identifying natural images from human brain activity

A challenging goal in neuroscience is to be able to read out, or decode, mental content from brain activity. Recent functional magnetic resonance imaging (fMRI) studies have decoded orientation, position and object category from activity in visual cortex. However, these studies typically used relatively simple stimuli (for example, gratings) or images drawn from fixed categories (for example, faces, houses), and decoding was based on previous measurements of brain activity evoked by those same stimuli or categories. To overcome these limitations, here we develop a decoding method based on quantitative receptive-field models that characterize the relationship between visual stimuli and fMRI activity in early visual areas. These models describe the tuning of individual voxels for space, orientation and spatial frequency, and are estimated directly from responses evoked by natural images. We show that these receptive-field models make it possible to identify, from a large set of completely novel natural images, which specific image was seen by an observer. Identification is not a mere consequence of the retinotopic organization of visual areas; simpler receptive-field models that describe only spatial tuning yield much poorer identification performance. Our results suggest that it may soon be possible to reconstruct a picture of a person's visual experience from measurements of brain activity alone.     

Cortical microstimulation influences perceptual judgements of motion direction

Neurons in the visual cortex respond selectively to perceptually salient features of the visual scene, such as the direction and speed of moving objects, the orientation of local contours, or the colour or relative depth of a visual pattern. It is commonly assumed that the brain constructs its percept of the visual scene from information encoded in the selective responses of such neurons. We have now tested this hypothesis directly by measuring the effect on psychophysical performance of modifying the firing rates of physiologically characterized neurons. We required rhesus monkeys to report the direction of motion in a visual display while we electrically stimulated clusters of directionally selective neurons in the middle temporal visual area (MT, or V5), an extrastriate area that plays a prominent role in the analysis of visual motion information. Microstimulation biased the animals' judgements towards the direction of motion encoded by the stimulated neurons. This result indicates that physiological properties measured at the neuronal level can be causally related to a specific aspect of perceptual performance.     

Experience-dependent representation of visual categories in parietal cortex

Categorization is a process by which the brain assigns meaning to sensory stimuli. Through experience, we learn to group stimuli into categories, such as 'chair', 'table' and 'vehicle', which are critical for rapidly and appropriately selecting behavioural responses. Although much is known about the neural representation of simple visual stimulus features (for example, orientation, direction and colour), relatively little is known about how the brain learns and encodes the meaning of stimuli. We trained monkeys to classify 360 degrees of visual motion directions into two discrete categories, and compared neuronal activity in the lateral intraparietal (LIP) and middle temporal (MT) areas, two interconnected brain regions known to be involved in visual motion processing. Here we show that neurons in LIP--an area known to be centrally involved in visuo-spatial attention, motor planning and decision-making-robustly reflect the category of motion direction as a result of learning. The activity of LIP neurons encoded directions of motion according to their category membership, and that encoding shifted after the monkeys were retrained to group the same stimuli into two new categories. In contrast, neurons in area MT were strongly direction selective but carried little, if any, explicit category information. This indicates that LIP might be an important nexus for the transformation of visual direction selectivity to more abstract representations that encode the behavioural relevance, or meaning, of stimuli.     

Visual behaviour mediated by retinal projections directed to the auditory pathway

An unresolved issue in cortical development concerns the relative contributions of intrinsic and extrinsic factors to the functional specification of different cortical areas. Ferrets in which retinal projections are redirected neonatally to the auditory thalamus have visually responsive cells in auditory thalamus and cortex, form a retinotopic map in auditory cortex and have visual receptive field properties in auditory cortex that are typical of cells in visual cortex. Here we report that this cross-modal projection and its representation in auditory cortex can mediate visual behaviour. When light stimuli are presented in the portion of the visual field that is 'seen' only by this projection, 'rewired' ferrets respond as though they perceive the stimuli to be visual rather than auditory. Thus the perceptual modality of a neocortical region is instructed to a significant extent by its extrinsic inputs. In addition, gratings of different spatial frequencies can be discriminated by the rewired pathway, although the grating acuity is lower than that of the normal visual pathway.     

Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties

A fundamental step in visual pattern recognition is the establishment of relations between spatially separate features. Recently, we have shown that neurons in the cat visual cortex have oscillatory responses in the range 40-60 Hz (refs 1, 2) which occur in synchrony for cells in a functional column and are tightly correlated with a local oscillatory field potential. This led us to hypothesize that the synchronization of oscillatory responses of spatially distributed, feature selective cells might be a way to establish relations between features in different parts of the visual field. In support of this hypothesis, we demonstrate here that neurons in spatially separate columns can synchronize their oscillatory responses. The synchronization has, on average, no phase difference, depends on the spatial separation and the orientation preference of the cells and is influenced by global stimulus properties.     

Two types of orientation-sensitive responses of amacrine cells in the mammalian retina.

Neurons sensitive to the orientation of light stimuli exist throughout the mammalian visual system, suggesting that this spatial feature is a fundamental cue used by the brain to decipher visual information. The most peripheral neurons known to show orientation sensitivity are the retinal ganglion cells. Considerable morphological and pharmacological data suggest that the orientation sensitivity of ganglion cells is formed, at least partly, by the amacrine cells, which are laterally oriented interneurons presynaptic to the ganglion cells in the inner plexiform layer. So far there have been few studies of the responses of amacrine cells to oriented visual stimuli and their role in forming orientation-sensitive responses in the retina remains unclear. Here I report the novel finding of a population of amacrine cells in the rabbit retina which are orientation-sensitive. These amacrine cells can be divided into two subtypes, whose orientation sensitivity is manufactured by two distinct mechanisms. The orientation sensitivity of the first subtype of amacrine cell is formed from the interactions of excitatory, centre-receptive field synaptic inputs and inhibitory inputs of opposite polarity, whereas that for cells of the second subtype seems to be the product of a marked asymmetry in their dendritic arbors.     

Orientation-specific cortical responses develop in early infancy

Neurones in the visual cortex of higher mammals differ from those elsewhere in the visual pathway in that the majority respond selectively to particular edge or bar orientations in the stimulus. We have developed a visually evoked potential (VEP) technique which isolates the response of orientation-selective mechanisms from that of cortical or sub-cortical neurones which lack orientation selectivity. We are unable to find such orientation-selective responses in newborn human infants within the sensitivity of our method, but repeated longitudinal testing of individual infants shows that measurable responses emerge around 6 weeks of age. This result is consistent with the idea that human cortical visual function is very immature at birth, but develops rapidly in the first two postnatal months.     

A dimension reduction framework for understanding cortical maps

We argue that cortical maps, such as those for ocular dominance, orientation and retinotopic position in primary visual cortex, can be understood in terms of dimension-reducing mappings from many-dimensional parameter spaces to the surface of the cortex. The goal of these mappings is to preserve as far as possible neighbourhood relations in parameter space so that local computations in parameter space can be performed locally in the cortex. We have found that, in a simple case, certain self-organizing models generate maps that are near-optimally local, in the sense that they come close to minimizing the neuronal wiring required for local operations. When these self-organizing models are applied to the task of simultaneously mapping retinotopic position and orientation, they produce maps with orientation vortices resembling those produced in primary visual cortex. This approach also yields a new prediction, which is that the mapping of position in visual cortex will be distorted in the orientation fracture zones.     

Functional specificity of local synaptic connections in neocortical networks

Neuronal connectivity is fundamental to information processing in the brain. Therefore, understanding the mechanisms of sensory processing requires uncovering how connection patterns between neurons relate to their function. On a coarse scale, long-range projections can preferentially link cortical regions with similar responses to sensory stimuli. But on the local scale, where dendrites and axons overlap substantially, the functional specificity of connections remains unknown. Here we determine synaptic connectivity between nearby layer 2/3 pyramidal neurons in vitro, the response properties of which were first characterized in mouse visual cortex in vivo. We found that connection probability was related to the similarity of visually driven neuronal activity. Neurons with the same preference for oriented stimuli connected at twice the rate of neurons with orthogonal orientation preferences. Neurons responding similarly to naturalistic stimuli formed connections at much higher rates than those with uncorrelated responses. Bidirectional synaptic connections were found more frequently between neuronal pairs with strongly correlated visual responses. Our results reveal the degree of functional specificity of local synaptic connections in the visual cortex, and point to the existence of fine-scale subnetworks dedicated to processing related sensory information.     

Feature-based attention influences motion processing gain in macaque visual cortex.

Changes in neural responses based on spatial attention have been demonstrated in many areas of visual cortex, indicating that the neural correlate of attention is an enhanced response to stimuli at an attended location and reduced responses to stimuli elsewhere. Here we demonstrate non-spatial, feature-based attentional modulation of visual motion processing, and show that attention increases the gain of direction-selective neurons in visual cortical area MT without narrowing the direction-tuning curves. These findings place important constraints on the neural mechanisms of attention and we propose to unify the effects of spatial location, direction of motion and other features of the attended stimuli in a 'feature similarity gain model' of attention.     

Functions of the ON and OFF channels of the visual system

In the mammalian eye, the ON-centre and OFF-centre retinal ganglion cells form two major pathways projecting to central visual structures from the retina. These two pathways originate at the bipolar cell level: one class of bipolar cells becomes hyperpolarized in response to light, as do all photoreceptor cells, and the other class becomes depolarized on exposure to light, thereby inverting the receptor signal. It has recently become possible to examine the functional role of the ON-pathway in vision by selectively blocking it at the bipolar cell level using the glutamate neurotransmitter analogue 2-amino-4-phosphonobutyrate (APB)1. APB application to monkey, cat and rabbit retinas abolishes ON responses in retinal ganglion cells, the lateral geniculate nucleus and the visual cortex but has no effect on the centre-surround antagonism of OFF cells or the orientation and direction selectivities in the cortex2-5. These and related findings6-11 suggest that the ON and OFF pathways remain largely separate through the lateral geniculate nucleus and that in the cortex, contrary to some hypotheses, they are not directly involved in mechanisms giving rise to orientation and direction selectivities. We have examined the roles of the ON and OFF channels in vision in rhesus monkeys trained to do visual detection and discrimination tasks. We report here that the ON channel is reversibly blocked by injection of APB into the vitreous. Detection of light increment but not of light decrement is severely impaired, and there is a pronounced loss in contrast sensitivity. The perception of shape, colour, flicker, movement and stereo images is only mildly impaired, but longer times are required for their discrimination. Our results suggest that two reasons that the mammalian visual system has both ON and OFF channels is to yield equal sensitivity and rapid information transfer for both incremental and decremental light stimuli and to facilitate high contrast sensitivity.     

Highly ordered arrangement of single neurons in orientation pinwheels

In the visual cortex of higher mammals, neurons are arranged across the cortical surface in an orderly map of preferred stimulus orientations. This map contains 'orientation pinwheels', structures that are arranged like the spokes of a wheel such that orientation changes continuously around a centre. Conventional optical imaging first demonstrated these pinwheels, but the technique lacked the spatial resolution to determine the response properties and arrangement of cells near pinwheel centres. Electrophysiological recordings later demonstrated sharply selective neurons near pinwheel centres, but it remained unclear whether they were arranged randomly or in an orderly fashion. Here we use two-photon calcium imaging in vivo to determine the microstructure of pinwheel centres in cat visual cortex with single-cell resolution. We find that pinwheel centres are highly ordered: neurons selective to different orientations are clearly segregated even in the very centre. Thus, pinwheel centres truly represent singularities in the cortical map. This highly ordered arrangement at the level of single cells suggests great precision in the development of cortical circuits underlying orientation selectivity.     

Sustained firing in auditory cortex evoked by preferred stimuli

It has been well documented that neurons in the auditory cortex of anaesthetized animals generally display transient responses to acoustic stimulation, and typically respond to a brief stimulus with one or fewer action potentials. The number of action potentials evoked by each stimulus usually does not increase with increasing stimulus duration. Such observations have long puzzled researchers across disciplines and raised serious questions regarding the role of the auditory cortex in encoding ongoing acoustic signals. Contrary to these long-held views, here we show that single neurons in both primary (area A1) and lateral belt areas of the auditory cortex of awake marmoset monkeys (Callithrix jacchus) are capable of firing in a sustained manner over a prolonged period of time, especially when they are driven by their preferred stimuli. In contrast, responses become more transient or phasic when auditory cortex neurons respond to non-preferred stimuli. These findings suggest that when the auditory cortex is stimulated by a sound, a particular population of neurons fire maximally throughout the duration of the sound. Responses of other, less optimally driven neurons fade away quickly after stimulus onset. This results in a selective representation of the sound across both neuronal population and time.     

Retinal ganglion cells act largely as independent encoders

Correlated firing among neurons is widespread in the visual system. Neighbouring neurons, in areas from retina to cortex, tend to fire together more often than would be expected by chance. The importance of this correlated firing for encoding visual information is unclear and controversial. Here we examine its importance in the retina. We present the retina with natural stimuli and record the responses of its output cells, the ganglion cells. We then use information theoretic techniques to measure the amount of information about the stimuli that can be obtained from the cells under two conditions: when their correlated firing is taken into account, and when their correlated firing is ignored. We find that more than 90% of the information about the stimuli can be obtained from the cells when their correlated firing is ignored. This indicates that ganglion cells act largely independently to encode information, which greatly simplifies the problem of decoding their activity.     

Mapping multiple features in the population response of visual cortex

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

Vernier acuity of neurones in cat visual cortex

The ability of human observers to detect Vernier breaks of as little as 5 s arc has been termed hyperacuity as this distance is substantially less than the angular separation of the bars of the highest spatial frequency of grating (approximately 1 arc min) that can be detected. Although the visual cortex is a likely candidate for the location of detectors involved in this performance, it is not known whether there are cells sensitive enough to detect deviations from co-linearity that are small compared with their spatial resolution (defined in terms of the highest spatial frequency that the cell can detect). We report here the results of physiological experiments on single units in area 17 of the cat visual cortex in which we studied the effect of introducing a Vernier break into a bar stimulus moved across the receptive field of the cell at a constant velocity. Our results show that the responses of most simple and complex cells are significantly reduced by the introduction of a Vernier break that is substantially smaller than the spatial resolution of the cell. The most sensitive cells in our sample could discriminate Vernier offsets of 3-6 arc min with a reliability of approximately 70%. This was much smaller than their spatial resolution, which was in the range 25-30 arc min. We interpret these results in terms of mechanisms that could underly the orientation selectivity of cortical neurones and suggest how our results relate to human Vernier acuity.