Magnocellular and parvocellular contributions to the responses of neurons in macaque striate cortex

Anatomical and physiological studies of the primate visual system have suggested that the signals relayed by the magnocellular and parvocellular subdivisions of the LGN remain segregated in visual cortex. It has been suggested that this segregation may account for the known differences in visual function between the parietal and temporal cortical processing streams in extrastriate visual cortex. To test directly the hypothesis that the temporal stream of processing receives predominantly parvocellular signals, we recorded visual responses from the superficial layers of V1 (striate cortex), which give rise to the temporal stream, while selectively inactivating either the magnocellular or parvocellular subdivisions of the LGN. Inactivation of the parvocellular subdivision reduced neuronal responses in the superficial layers of V1, but the effects of magnocellular blocks were generally as pronounced or slightly stronger. Individual neurons were found to receive contributions from both pathways. We furthermore found no evidence that magnocellular contributions were restricted to either the cytochrome oxidase blobs or interblobs in V1. Instead, magnocellular signals made substantial contributions to responses throughout the superficial layers. Thus, the regions within V1 that constitute the early stages of the temporal processing stream do not appear to contain isolated parvocellular signals. These results argue against a direct mapping of the subcortical magnocellular and parvocellular pathways onto the parietal and temporal streams of processing in cortex.     

Gating of neuronal responses in macaque primary visual cortex by an attentional spotlight

Neuronal responses were recorded from the striate cortex of monkeys trained to perform visual discrimination at locations in the visual field to which their attention was drawn. A subset of neurons showed vigorous responses to visual stimuli for trials in which the monkey was directing its attention to the respective receptive field location. In trials where attention is directed elsewhere, responses to the same stimuli were significantly reduced. In some cells the early response component was not modulated by attention, but later components were affected by the locus of attention. The results suggest the operation of a feedback in the paradigm that spotlights a topographically restricted area of V1 for further processing at higher levels.     

The effects of V4 and middle temporal (MT) area lesions on visual performance in the rhesus monkey

The effects of V4, MT, and combined V4 + MT lesions were assessed on a broad range of visual capacities that included measures of contrast sensitivity, wavelength and brightness discrimination, form vision, pattern vision, motion and flicker perception, stereopsis, and the selection of stimuli that were less prominent than those with which they appeared in stimulus arrays. The major deficit observed was a loss in the ability, after V4 lesions, to select such less prominent stimuli; this was the case irrespective of the manner in which the stimulus arrays were made visible, using either luminance, chrominance, motion, or stereoscopic depth as surface media. In addition, V4 lesions yielded mild deficits in color, brightness, and form vision whereas MT lesions yielded mild to moderate deficits in motion and flicker perception. Both lesions produced mild deficits in contrast sensitivity, shape-from-motion perception, and yielded increased reaction times on many of the tasks. The impairment resulting from combined V4 and MT lesions was not greater than the sum of the deficits of either lesion. None of the lesions produced significant deficits in stereopsis. The findings suggest that (1) area V4 is part of a neural system that is involved in extracting stimuli from the visual scene that elicit less neural activity early in the visual system than do other stimuli with which they appear and (2) several other extrastriate regions and more than just two major cortical processing streams contribute to the processing of basic visual functions in the extrastriate cortex.     

The role of temporal cortical areas in perceptual organization

The visual areas of the temporal lobe of the primate are thought to be essential for the representation of visual objects. To examine the role of these areas in the visual awareness of a stimulus, we recorded the activity of single neurons in monkeys trained to report their percepts when viewing ambiguous stimuli. Visual ambiguity was induced by presenting incongruent images to the two eyes, a stimulation condition known to instigate binocular rivalry, during which one image is seen at a given time while the other is perceptually suppressed. Previous recordings in areas V1, V2, V4, and MT of monkeys experiencing binocular rivalry showed that only a small proportion of striate and early extrastriate neurons discharge exclusively when the driving stimulus is seen. In contrast, the activity of almost all neurons in the inferior temporal cortex and the visual areas of the cortex of superior temporal sulcus was found to be contingent upon the perceptual dominance of an effective visual stimulus. These areas thus appear to represent a stage of processing beyond the resolution of ambiguities--and thus beyond the processes of perceptual grouping and image segmentation--where neural activity reflects the brain's internal view of objects, rather than the effects of the retinal stimulus on cells encoding simple visual features or shape primitives.     

Sustained visual-spatial attention produces costs and benefits in response time and evoked neural activity

This study investigated the simple reaction time (RT) and event-related potential (ERP) correlates of biasing attention towards a location in the visual field. RTs and ERPs were recorded to stimuli flashed randomly and with equal probability to the left and right visual hemifields in the three blocked, covert attention conditions: (i) attention divided equally to left and right hemifield locations; (ii) attention biased towards the left location; or (iii) attention biased towards the right location. Attention was biased towards left or right by instructions to the subjects, and responses were required to all stimuli. Relative to the divided attention condition, RTs were significantly faster for targets occurring where more attention was allocated (benefits), and slower to targets where less attention was allocated (costs). The early P1 (100-140 msec) component over the lateral occipital scalp regions showed attentional benefits. There were no amplitude modulations of the occipital N1 (125-180 msec) component with attention. Between 200 and 500 msec latency, a late positive deflection (LPD) showed both attentional costs and benefits. The behavioral findings show that when sufficiently induced to bias attention, human observers demonstrate RT benefits as well as costs. The corresponding P1 benefits suggest that the RT benefits of spatial attention may arise as the result of modulations of visual information processing in the extrastriate visual cortex.     

Visual motion processing in the anterior ectosylvian sulcus of the cat

1. Neurons that are selectively sensitive to the direction of motion of elongated contours have been found in several cortical areas in many species. However, in the striate cortex of the cat and monkey, and the extrastriate posteromedial lateral suprasylvian visual area of the cat, such cells are generally component motion selective, signaling only the direction of movement orthogonal to the preferred orientation; a direction that is not necessarily the same as the motion of the entire pattern or texture of which the cell's preferred contour is part. The primate extrastriate middle temporal area is the only cortical region currently known to contain a substantial population of pattern-motion-selective cells that respond to the shared vector of motion of mixtures of contours. 2. From analyzing published data on the connectivity of the cat's cortex, we predicted that the anterior ectosylvian visual area (AEV), situated within the anterior ectosylvian sulcus, might be a higher-order motion processing area and thus likely to contain pattern-motion-selective neurons. This paper presents the results of a study on neuronal responses in AEV. 3. Ninety percent of AEV cells that responded strongly to drifting grating and/or plaid stimuli were directionally selective (directionality index > 0.5). For this group, the mean directionality index was 0.75. Moreover, 55% of these cells were unequivocally classified as pattern motion selective and only one neuron was classified as definitely component motion selective. Thus high-level pattern motion coding occurs in the cat extrastriate cortex and is not limited to the primate middle temporal area. 4. AEV contains a heterogeneous population of directionally selective cells. There was no clear relation between the degree of directional selectivity for plaids or gratings and the degree of selectivity for pattern motion or component motion. Nevertheless, 28% of the highly responsive cells were both more strongly modulated by plaids than gratings and more pattern motion selective than component motion selective. Such cells could correspond to a population of "selection units" signaling the salience of local motion information. 5. AEV lacks global retinotopic order but the preferred direction of motion of neurons (rather than axis of motion, as in the middle temporal area and the posteromedial lateral suprasylvian visual area) is mapped systematically across the cortex. Our data are compatible with AEV being a nonretinotopic, feature-mapped area in which cells representing similar parts of "motion space" are brought together on the cortical sheet.     

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.     

A subcortical pathway to the right amygdala mediating "unseen" fear

Neuroimaging studies have shown differential amygdala responses to masked ("unseen") emotional stimuli. How visual signals related to such unseen stimuli access the amygdala is unknown. A possible pathway, involving the superior colliculus and pulvinar, is suggested by observations of patients with striate cortex lesions who show preserved abilities to localize and discriminate visual stimuli that are not consciously perceived ("blindsight"). We used measures of right amygdala neural activity acquired from volunteer subjects viewing masked fear-conditioned faces to determine whether a colliculo-pulvinar pathway was engaged during processing of these unseen target stimuli. Increased connectivity between right amygdala, pulvinar, and superior colliculus was evident when fear-conditioned faces were unseen rather than seen. Right amygdala connectivity with fusiform and orbitofrontal cortices decreased in the same condition. By contrast, the left amygdala, whose activity did not discriminate seen and unseen fear-conditioned targets, showed no masking-dependent changes in connectivity with superior colliculus or pulvinar. These results suggest that a subcortical pathway to the right amygdala, via midbrain and thalamus, provides a route for processing behaviorally relevant unseen visual events in parallel to a cortical route necessary for conscious identification.     

Spatial attention effects in macaque area V4

Focal visual attention typically produces enhanced perceptual processing at the psychological level and relatively stronger neural responses at the physiological level. A longstanding mechanistic question is whether these attentional effects pertain specifically to the attended (target) object or to the region of space it occupies. We show here that attentional response enhancement in macaque area V4 extends to behaviorally irrelevant objects in the vicinity of the target object, indicating that focal attention has a strong spatial component at the physiological level. In addition, we find that spatial attention effects typically show a striking directional asymmetry. The direction of the asymmetry varies between cells, so that some cells respond best when attention is directed to the left of the stimulus, some when attention is directed to the right, etc. Thus, attention involves not only enhanced responses to behavioral targets but also a complex modulation of responses to other stimuli in the surrounding visual space.     

Magnetoencephalographic evidence for non-geniculostriate visual input to human cortical area V5

The aim of this study was to establish whether there is non-geniculostriate input to the extrastriate motion-sensitive area V5 in humans. Responses were measured with a SQUID neuro-magnetometer to motion stimuli presented within the blind hemifield of GY, a well-documented subject with a complete absence of the left primary visual cortical area V1. The motion stimulus was a 0.5c/deg, rapidly drifting (16Hz) achromatic sinusoidal grating. With this stimulus, the magnetic responses recorded over the temporo-parieto-occipital region in normals are well modelled by localized current sources in areas V1 and V5 (Anderson, S. J. et al., Proceedings of the Royal Society, London, Series B, 1996, 263, 423-431). As a control, evoked responses were measured to a 1.0 c/deg, stationary, photometrically isoluminant red/green sinusoidal grating. With the chromatic stimulus, the principal component of the magnetic responses recorded over the occipital pole in normals is well modelled by a current source in area V1 (Fylan, F. et al., Investigative Ophthalmology and Visual Science, 1995, 36, s1053). Both stimuli subtended 4 deg vertically by 6 deg horizontally, positioned such that the stimulus extended beyond the area of macular sparing into the lower field quadrant of the blind (or sighted) hemifield. Chromatic stimuli failed to evoked responses from GY's blind (contralateral) hemifield, consistent with there being no V1 activity in his left cortical hemisphere. However, motion stimuli did evoke responses from GY's blind hemifield, originating from a location consistent with activity in area V5. We further observed that both colour and motion stimuli evoked responses from GY's sighted (ipsilateral) hemifield. We conclude that there is non-geniculostriate input to extrastriate motion-sensitive areas in the human visual system, and that this pathway subserves the residual visual sensitivity to motion in the blind hemifield that has been demonstrated psychophysically in observer GY.     

Random dots blinking: a new approach to elucidate the activities of the extrastriate cortex in humans

To investigate cortical activities related to the visual recognition of characters, we recorded the magnetoencephalography (MEG) in six normal subjects who were encouraged to discriminate capital English letters displayed for a brief period. To reduce the primary responses evoked by the luminance change in the striate cortex (V1), we used a novel stimulus method, random dots blinking (RDB), by means of the temporal changes of patterns using a large number of small random dots. Along with the MEG recording, we also measured the discrimination accuracy rate (%) to know how well the subjects recognized the letters. One clear component, about 300 ms in peak latency, was identified in all six subjects. Its peak amplitude and the discrimination accuracy rate increased similarly as the character display duration became longer. Its signal source was estimated in the extrastriate cortex, around the fusiform gyrus, in the right hemisphere. We suspect that the activity in these cortical areas has strong relation to the conscious perception of characters.     

Reflections on blindsight: Neuroimaging and behavioural explorations clarify a case of reversed localisation in the blind field of a patient with hemianopia.

Blindsight refers to residual visual abilities of patients with primary visual cortex lesions. Most of this research uses single case studies, most famously patient GY. We examined a patient (DC) after surgical resection of V1 who demonstrated robust but reversed blind field target localisation, mislocalising midline blind field targets to the periphery and vice versa. This pattern was reliable across multiple sessions and was not because of extraocular light scatter. We then used functional magnetic resonance imaging to examine neural responses to blind field motion stimuli with no evidence of motion-selective activation in DC's extrastriate cortex in the damaged hemisphere, in stark contrast to GY who showed robust bilateral activation in response to blind field stimuli. This suggests that DC's blind field performance may not represent true blindsight. Follow-up testing with the target—background contrast reversed (i.e., black targets/white background), eliminated DC's reversed localisation, strongly suggesting that she was employing an unusual decision criterion based on intraocular light scatter. DC's failure to demonstrate true blindsight may be related to the age at which she acquired her lesion—much later in life than GY. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Selective attention in the primate visual system.

A series of single unit PET and behavioural studies is described addressing the functions and neurophysiology of visual attention. Beyond striale cortex, visual information is processed in a network of separate cortical areas, specialized in part for analysis of different visual attributes. Issues arising in such a modular system include the nature of the attentional state in extrastriate cortex, its flexible control by the requirements of current behaviour, and the coordination between areas implied by attention to whole objects. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

The organization of visual corticocortical connections in early postnatal kittens

We tested the hypothesis that, in newborn kittens, superficial layers of the extrastriate cortex receive more specific patterns of corticocortical innervation from the striate cortex than deep layers. First, we injected retrogradely transported tract-tracers at a range of depths in area 18 to label area 17. All injections were of similar tangential diameter and were in the same region of rostral area 18, where the visual field 10-20 degrees below the horizontal meridian is represented. Injections that involved only the superficial layers of area 18 labelled cells mainly in the superficial layers (future layers 2-4) of area 17, across a region that was 2-3 mm wider than the diameter of the injection site in the rostrocaudal direction. Injections that involved all layers of area 18 labelled cells in both superficial and deep layers (5 and 6) of area 17, across a region that was 6-9 mm wider than the diameter of the injection site in the rostrocaudal direction. These values demonstrate that, in neonates, the convergence of projections from area 17 to the superficial layers of area 18 is less than that to the deep layers of area 18. The lower values for convergence obtained by injecting only the superficial layers of area 18 in kittens were similar to those obtained by injecting all layers of area 18 in adult cats; the values obtained by injecting all layers of area 18 in kittens were much higher. Second, we injected the full depth of area 17 in newborn kittens with labels that travel anterogradely and retrogradely. Confirming the conclusions from the use of retrograde tracers, these focal injections produced very widespread labelling of the deep layers of area 18, but much more localized and topographically organized labelling of its superficial layers. These results indicate that there is a considerable postnatal improvement in the accuracy with which corticocortical cells in striate visual cortex target appropriate regions in extrastriate cortex, in agreement with previous findings. They also demonstrate that this change occurs mainly among those striate cortical neurons that innervate a wide region of the deep layers of extrastriate cortex at birth. The innervation of the superficial layers of extrastriate cortex is much more accurate from the outset.     

Episodic multiregional cortical coherence at multiple frequencies during visual task performance

The way in which the brain integrates fragmentary neural events at multiple locations to produce unified perceptual experience and behaviour is called the binding problem. Binding has been proposed to involve correlated activity at different cortical sites during perceptuomotor behaviour, particularly by synchronization of narrow-band oscillations in the gamma-frequency range (30-80 Hz). In the rabbit olfactory system, inhalation induces increased gamma-correlation between sites in olfactory bulb and cortex. In the cat visual system, coherent visual stimuli increase gamma-correlation between sites in both the same and different visual cortical areas. In monkeys, some groups have found that gamma-oscillations transiently synchronize within striate cortex, superior temporal sulcus and somatosensorimotor cortex. Others have reported that visual stimuli produce increased broad-band power, but not gamma-oscillations, in several visual cortical areas. But the absence of narrow-band oscillations in itself does not disprove interregional synchronization, which may be a broad-band phenomenon. We now describe episodes of increased broad-band coherence among local field potentials from sensory, motor and higher-order cortical sites of macaque monkeys performing a visual discrimination task. Widely distributed sites become coherent without involving other intervening sites. Spatially selective multiregional cortical binding, in the form of broad-band synchronization, may thus play a role in primate perceptuomotor behaviour.     

Neural mechanisms of global and local processing. A combined PET and ERP study

The neural mechanisms of hierarchical stimulus processing were investigated using a combined event-related potentials (ERPs) and positron emission tomography (PET) approach. Healthy subjects were tested under two conditions that involved selective or divided attention between local and global levels of hierarchical letter stimuli in order to determine whether and where hemispheric differences might exist in the processing of local versus global information. When attention was divided between global and local levels, the N2 component of the ERPs (260- to 360-msec latency) elicited by the target stimuli showed asymmetries in amplitude over the two hemispheres. The N2 to local targets was larger over the left hemisphere, but the N2 to global targets tended to be slightly larger over the right hemisphere. However, the shorter-latency, sensory-evoked P1 component (90- to 150-msec latency) was not different for global versus local targets under conditions of divided attention. In contrast, during selective attention to either global or local targets, asymmetries in the N2 component were not observed. But under selective attention conditions, the sensory-evoked P1 components in the extrastriate cortex were enlarged for global versus local attention. Increased regional cerebral blood flow in the posterior fusiform gyrus bilaterally was observed in the PET data during selective attention to either global or local targets, but neither these nor the P1 component showed any tendency toward hemispheric difference for global versus local attention. Neither were there any activations observed in the parietal lobe during selective attention to global versus local targets. Together these data indicate that early sensory inputs are not modulated to gate global versus local information differentially into the two hemispheres. Rather, later stages of processing that may be asymmetrically organized in the left and right hemispheres operate in parallel to process global and local aspects of complex stimuli (i.e., the N2 effect of the ERPs). This pattern of results supports models proposing that spatial frequency analysis is only asymmetric at higher stages of perceptual processing and not at the earliest stages of visual cortical analysis.     

Reduction of a pattern-induced motion aftereffect by binocular rivalry suggests the involvement of extrastriate mechanisms

Previous research suggests that plaid-induced motion aftereffects (MAEs) involve extrastriate mechanisms (Wenderoth et al., 1988). There is evidence also that binocular rivalry occurs beyond V1 and that it disrupts the processing of MAEs which are believed to be based upon extrastriate mechanisms (e.g. the spiral MAE) but not MAEs, such as linear MAE induced by a drifting grating, which are thought to arise in striate cortex (Wiesenfelder & Blake, 1990). The logical inference is that binocular rivalry during drifting plaid-induced adaptation should reduce the MAEs which result. We report experiments which confirm this prediction.     

Fast visual evoked potential input into human area V5

Studies of the human visual cortex have demonstrated that an area for motion processing (V5) is located in the lateral occipito-temporal cortex. To study the timing of arrival of signals in V5 we recorded multi-channel visual evoked potentials (VEPs) to checkerboard stimuli. We then applied dipole source analysis which was computed on a grand average of 10 subjects, and on five individual subjects, respectively. We demonstrate an early VEP component with onset before 30 ms and with a peak around 45 ms, located in the vicinity of V5. This early component was independent of a second activity, which started around 50 ms and peaked around 70 ms, and was located within the striate cortex (V1). These results provide further evidence for a very fast input to V5 before activation of V1.     

Neural evidence linking visual object enumeration and attention

Visual object enumeration is rapid and accurate for four or fewer items but slow and error-prone for over four items. This dichotomy has recently been linked to visual attentional phenomena by findings suggesting that 'subitizing' of small sets of objects is preattentive whereas 'counting' of over four items demands spatial shifts of attention. We evaluated this link at a neural level, using H2 15-O positron emission tomography to measure changes in regional cerebral blood flow while subjects enumerated the number of target vertical bars that 'popped out' of a 16-bar visual display consisting of both horizontal and vertical bars. Relative to a condition with a single target, subitizing (one to four targets) activated foci in the occipital extrastriate cortex, consistent with involvement of early, preattentive visual processes. Relative to subitizing, counting (five to eight targets) activated a widespread network of brain regions, including multiple foci implicated in shifting visual attention-large regions of the superior parietal cortex bilaterally and a focus in the right inferior frontal cortex. These results offer the first direct neural support for mapping the subitizing-counting dichotomy onto separable processes mediating preattentive vision and shifts of visual attention.     

In vivo tracing of pathways and spatio-temporal activity patterns in rat visual cortex using voltage sensitive dyes

We monitored optical signals from cortex stained with a voltage sensitive dye to study activity evoked by intracortical electrical stimulation. The objectives were to study the spatial and temporal spread of activity from intrinsic connections near the stimulating electrode and to develop a new technique to study extrinsic projections from striate cortex to extrastriate target areas. Various measures were made of the time course of the optical signal (latency, rise time, decay time, temporal summation, facilitation versus depression, and presence or absence of a slow undershoot); in general, these measures were found to vary significantly across different response positions, different experiments, and even different runs within the same experiment. The spatial distribution of responses near the stimulating electrode in striate cortex was usually elliptical and was most often elongated along the anterior-posterior axis, with a typical size (full width at 75% max) of 1.3 mm (anterior-posterior axis) by 0.75 mm (medio-lateral axis). In some cases, complex spatio-temporal patterns were observed, in which the position of the maximum optical signal shifted with time or split into multiple peaks. In eight experiments, a response focus was found in extrastriate cortex at an expected location within the lateromedial area (LM). The response focus in LM was typically about half the size of that in striate cortex. In some experiments we observed additional focal responses in the anterolateral visual area (AL). The extrastriate responses showed a significant delay (3-10 ms) in onset and time to peak relative to the striate response. The validity of this technique for determining extrinsic projections was tested in two types of experiments. In the first, stimulation from two electrodes in striate cortex generated response foci consistent with the known topographic organization of area LM. In the second, the optically measured response focus was shown to correlate with the histologically reconstructed projection of a chemical tracer injected near the site of stimulation. We discuss the chain of neurophysiological events that occur during and after focal electrical stimulation and how they relate to the observed optical signal. We conclude that direct passive responses were a small component of our signal, that the component due to action potentials in directly stimulated neurons should have occurred in the first 1-2 ms post stimulus and is small compared to the peak signal, and that overall our signals were probably dominated by a combination of asynchronously occurring action potentials and excitatory and inhibitory synaptic potentials.(ABSTRACT TRUNCATED AT 400 WORDS)