Phase locking of single neuron activity to theta oscillations during working memory in monkey extrastriate visual cortex

Working memory has been linked to elevated single neuron discharge in monkeys and to oscillatory changes in the human EEG, but the relation between these effects has remained largely unexplored. We addressed this question by measuring local field potentials and single unit activity simultaneously from multiple electrodes placed in extrastriate visual cortex while monkeys were performing a working memory task. We describe a significant enhancement in theta band energy during the delay period. Theta oscillations had a systematic effect on single neuron activity, with neurons emitting more action potentials near their preferred angle of each theta cycle. Sample-selective delay activity was enhanced if only action potentials emitted near the preferred theta angle were considered. Our results suggest that extrastriate visual cortex is involved in short-term maintenance of information and that theta oscillations provide a mechanism for structuring the recurrent interaction between neurons in different brain regions that underlie working memory.     

Visual attention mediated by biased competition in extrastriate visual cortex.

According to conventional neurobiological accounts of visual attention, attention serves to enhance extrastriate neuronal responses to a stimulus at one spatial location in the visual field. However, recent results from recordings in extrastriate cortex of monkeys suggest that any enhancing effect of attention is best understood in the context of competitive interactions among neurons representing all of the stimuli present in the visual field. These interactions can be biased in favour of behaviourally relevant stimuli as a result of many different processes, both spatial and non-spatial, and both bottom-up and top-down. The resolution of this competition results in the suppression of the neuronal representations of behaviourally irrelevant stimuli in extrastriate cortex. A main source of top-down influence may derive from neuronal systems underlying working memory.     

Some Golgi data on visual cortex of the rhesus monkey.

The rhesus monkey's visual cortex was studied on Golgi material. The terminal arborization of the geniculate fibres and non-specific vertical fibres have been analysed. The interneurons (intrinsic neurons) of the area described in detail and classified on the basis of their axonal and dendrite arborizations. The stellate neurons in layer IV are discussed.     

The effect of visual deprivation upon the basal dendrites of Meynert cells in the striate cortex of the monkey

The basal dendrites of Meynert cells in the striate cortex have been studied with the Golgi method in the brains of monkeys that had been reared for varying periods with the eyelids closed over one eye. The lengths and arrangement of the dendrites were compared with those in normal brains. In the visually deprived brain almost half of the cells had basal dendrites that were apparently normal with the dendritic fields in the form of an ellipse and the long axes parallel to the direction of the ocular dominance bands. The other cells had dendritic fields that have rarely been seen in normal material and two distinct types could be recognized. The 'lop-sided' cell had an ellipsoidal dendritic field with the major axis parallel to the ocular dominance bands, but the extents of the dendrites along the minor axis were very asymmetric; the ratio of the means of the long and short arms of the minor axis of the 'lop-sided' cell is 2.3:1 compared with 1.1:1 in normal brains. The 'perpendicular' type of cell also had an ellipsoidal dendritic field but the relation of the major and minor axes to the direction of the ocular dominance bands was the reverse of the normal cell, with the long axis of the ellipse being aligned perpendicular to the bands. 'Lop-sided' cells formed approximately 18% of the total of Meynert cells studied and the 'perpendicular' 32%. The proportion of the cells with abnormal basal dendritic fields, and particularly the 'perpendicular', increased with longer durations of eyelid closure. It is suggested that the alterations in the dendritic fields of the 'lop-sided' and 'perpendicular' cells may be correlated with the changes in width of the ocular dominance bands that are known to occur after monocular eyelid suture.     

Recognition of visual stimuli from multiple neuronal activity in monkey visual cortex

Response patterns recorded with 30 microelectrodes from area 17 of anaesthetized monkeys are analysed. A proportion of the patterns are used to define prototype response patterns. These in turn are used to recognize the stimulus from further non-averaged response patterns. In comparison, recognition by a feedforward neural network is much slower, and slightly inferior. The excitation time structure, with a resolution of about 20 ms, is found to contribute strongly to the recognition. There is some inter-ocular recognition for oriented moving bars, and for on and off phases of switched lights, but none for colours. Generalizations over some stimulus parameters (i.e. cases of confusion) are examined: If small jerking shapes are incorrectly recognized, in general the jerk direction often is the correct one. The onset of a response can most easily be found by determining the dissimilarity relative to spontaneous activity in a sliding window.     

Retinotopic organization of striate and extrastriate visual cortex in the golden hamster (Mesocricetus auratus).

The visual topography within striate and lateral extrastriate visual cortices was studied in adult hamsters. The cortical areas 17 and 18a in the left hemisphere were electrophysiologically mapped upon stimulation of the right eye, correlating receptive field positions in the visual field with cortical recording sites. Reference lesions were placed at selected cortical sites. Like in rats and other mammals, the lateral extrastriate cortex contained multiple representations of the visual field. Rostral area 18a contained the rostrolateral maps, with medial and lateral divisions. More caudally and sharing a common border with V1, maps in lateromedial, posterolateral and posterior areas were found. More laterally and forming a "third tier" of visual maps, anterolateral, laterolateral-anterior, laterolateral and laterolateral-posterior areas were found. There was also an indication of a possible pararhinal map. The plan so defined is virtually identical to that of rats. The results may be useful to understand a basic mammalian plan in the organization of the visual cortex.     

Effects of attention on the reliability of individual neurons in monkey visual cortex.

To determine the physiological mechanisms underlying the enhancement of performance by attention, we examined how attention affects the ability of isolated neurons to discriminate orientation by investigating the reliability of responses with and without attention. Recording from 262 neurons in cortical area V4 while two rhesus macaques did a delayed match-to-sample task with oriented stimuli, we found that attention did not produce detectable changes in the variability of neuronal responses but did improve the orientation discriminability of the neurons. We also found that attention did not change the relationship between burst rate and response rate. Our results are consistent with the idea that attention selects groups of neurons for a multiplicative enhancement in response strength.     

Instructive effect of visual experience in mouse visual cortex

We describe a form of experience-dependent response enhancement in the visual cortex of awake mice. Repeated presentations of grating stimuli of a single orientation result in a persistent enhancement of responses evoked by the test stimulus. Response potentiation is specific to the orientation of the test stimulus, develops gradually over the course of several training sessions, and occurs in both juvenile and adult mice. The stimulus-selective response potentiation (SRP) can mask deprivation-induced response depression in adult mice. SRP requires NMDA receptor activation and is prevented by viral delivery of a peptide that interferes with AMPA receptor trafficking. SRP may reveal the mechanisms involved in certain forms of perceptual learning.     

Anterior regions of monkey parietal cortex process visual 3D shape

The intraparietal cortex is involved in the control of visually guided actions, like reach-to-grasp movements, which require extracting the 3D shape and position of objects from 2D retinal images. Using fMRI in behaving monkeys, we investigated the role of the intraparietal cortex in processing stereoscopic information for recovering the depth structure and the position in depth of objects. We found that while several areas (CIP, LIP, and AIP on the lateral bank; PIP and MIP on the medial bank) are activated by stereoscopic stimuli, AIP and an adjoining portion of LIP are sensitive only to depth structure. Furthermore, only these two regions are sensitive to both the depth structure and the 2D shape of small objects. These results indicate that extracting 3D spatial information from stereo involves several intraparietal areas, among which AIP and anterior LIP are more specifically engaged in extracting the 3D shape of objects.     

Structure and function come unglued in the visual cortex

In this issue of Neuron, Chowdhury and DeAngelis report that training monkeys to perform a fine depth discrimination abolishes the contribution of signals from area MT to the execution of a different, coarse depth discrimination. This result calls into question the principle of associating particular visual areas with particular visual functions, by showing that such associations are modifiable by experience.     

Perceptual learning and dynamic changes in primary visual cortex

Perceptual learning is the improved performance that follows practice in a perceptual task. In this issue of Neuron, Yotsumoto et al. use fMRI to show that stimuli presented at the location used in training initially evoke greater activation in primary visual cortex than stimuli presented elsewhere, but this difference disappears once learning asymptotes.     

Perceptual learning reduces interneuronal correlations in macaque visual cortex

Responses of neurons in early visual cortex change little with training and appear insufficient to account for perceptual learning. Behavioral performance, however, relies on population activity, and the accuracy of a population code is constrained by correlated noise among neurons. We tested whether training changes interneuronal correlations in the dorsal medial superior temporal area, which is involved in multisensory heading perception. Pairs of single units were recorded simultaneously in two groups of subjects: animals trained extensively in a heading discrimination task, and "naive" animals that performed a passive fixation task. Correlated noise was significantly weaker in trained versus naive animals, which might be expected to improve coding efficiency. However, we show that the observed uniform reduction in noise correlations leads to little change in population coding efficiency when all neurons are decoded. Thus, global changes in correlated noise among sensory neurons may be insufficient to account for perceptual learning.     

Distributed neural plasticity for shape learning in the human visual cortex

Expertise in recognizing objects in cluttered scenes is a critical skill for our interactions in complex environments and is thought to develop with learning. However, the neural implementation of object learning across stages of visual analysis in the human brain remains largely unknown. Using combined psychophysics and functional magnetic resonance imaging (fMRI), we show a link between shape-specific learning in cluttered scenes and distributed neuronal plasticity in the human visual cortex. We report stronger fMRI responses for trained than untrained shapes across early and higher visual areas when observers learned to detect low-salience shapes in noisy backgrounds. However, training with high-salience pop-out targets resulted in lower fMRI responses for trained than untrained shapes in higher occipitotemporal areas. These findings suggest that learning of camouflaged shapes is mediated by increasing neural sensitivity across visual areas to bolster target segmentation and feature integration. In contrast, learning of prominent pop-out shapes is mediated by associations at higher occipitotemporal areas that support sparser coding of the critical features for target recognition. We propose that the human brain learns novel objects in complex scenes by reorganizing shape processing across visual areas, while taking advantage of natural image correlations that determine the distinctiveness of target shapes.