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Intrinsic timescales characterize dynamics of endogenous fluctuations in neural activity. Variation of intrinsic timescales across the neocortex reflects functional specialization of cortical areas, but less is known about how intrinsic timescales change during cognitive tasks. We measured intrinsic timescales of local spiking activity within columns of area V4 in male monkeys performing spatial attention tasks. The ongoing spiking activity unfolded across at least two distinct timescales, fast and slow. The slow timescale increased when monkeys attended to the receptive fields location and correlated with reaction times. By evaluating predictions of several network models, we found that spatiotemporal correlations in V4 activity were best explained by the model in which multiple timescales arise from recurrent interactions shaped by spatially arranged connectivity, and attentional modulation of timescales results from an increase in the efficacy of recurrent interactions. Our results suggest that multiple timescales may arise from the spatial connectivity in the visual cortex and flexibly change with the cognitive state due to dynamic effective interactions between neurons.

Significance Attention is thought to modulate sensory processing by changing communication between cortical areas within specific frequency bands. Using local field potential recordings, we tested this influential model through laminar recordings in macaque V1 and V4. Attention modulated communication unexpectedly. In V1, it decreased communication across spectral frequencies except for granular-to-supragranular interactions. In V4, it increased communication across all spectral frequencies. Critically, attention increased V1–V4 feedforward communication across all frequency bands, decreased V4–V1 feedback communication in low-frequency bands, and increased beta and gamma feedback communication. These findings challenge existing theories of frequency specificity of feedforward and feedback interactions., Achieving behavioral goals requires integration of sensory and cognitive information across cortical laminae and cortical regions. How this computation is performed remains unknown. Using local field potential recordings and spectrally resolved conditional Granger causality (cGC) analysis, we mapped visual information flow, and its attentional modulation, between cortical layers within and between macaque brain areas V1 and V4. Stimulus-induced interlaminar information flow within V1 dominated upwardly, channeling information toward supragranular corticocortical output layers. Within V4, information flow dominated from granular to supragranular layers, but interactions between supragranular and infragranular layers dominated downwardly. Low-frequency across-area communication was stronger from V4 to V1, with little layer specificity. Gamma-band communication was stronger in the feedforward V1-to-V4 direction. Attention to the receptive field of V1 decreased communication between all V1 layers, except for granular-to-supragranular layer interactions. Communication within V4, and from V1 to V4, increased with attention across all frequencies. While communication from V4 to V1 was stronger in lower-frequency bands (4 to 25 Hz), attention modulated cGCs from V4 to V1 across all investigated frequencies. Our data show that top-down cognitive processes result in reduced communication within cortical areas, increased feedforward communication across all frequency bands, and increased gamma-band feedback communication.

SummaryPerception and cognition require the integration of feed-forward sensory information with feedback signals. Feed-forward and feedback signals have been associated with specific cortical laminae and specific oscillatory frequencies. We used stimuli of different sizes to isolate spectral signatures of feedforward and feedback signals, and their effect on communication between layers in primary visual cortex of male macaque monkeys. Small stimuli, centered on the neurons’ receptive fields elicited broad band gamma frequency oscillations predominantly in the superficial layers. These Granger causal originated in upper layer 4 and lower supragranular layers, in line with existing feed-forward models of oscillatory responses. However, large stimuli extending into the far surround of neurons’ receptive fields, generated strong narrow band gamma oscillatory activity across cortical layers. They Granger causal arose in layer 5, were conveyed through layer 6 to superficial layers, and violated existing models of feedback spectral signatures. Equally surprising, with large stimuli, alpha band oscillatory activity arose predominantly in granular and supragranular layers, and communicated in a feed-forward direction. This shows that oscillations in specific frequency bands can be dynamically modulated to serve feedback and feed-forward communication and are not restricted to specific cortical layers in V1

Context affects the salience and visibility of image elements in visual scenes. Collinear flankers can enhance or decrease the perceptual and neuronal sensitivity to flanked stimuli. These effects are mediated through lateral interactions between neurons in the primary visual cortex (area V1), in conjunction with feedback from higher visual areas. The strength of lateral interactions is affected by cholinergic neuromodulation. Blockade of muscarinic receptors should increase the strength of lateral intracortical interactions, while nicotinic blockade should reduce thalamocortical feed-forward drive. Here we test this proposal through local iontophoretic application of the muscarinic receptor antagonist scopolamine and the nicotinic receptor antagonist mecamylamine, while recording single cells in parafoveal representations in awake fixating macaque V1. Collinear flankers generally reduced neuronal contrast sensitivity. Muscarinic and nicotinic receptor blockade equally reduced neuronal contrast sensitivity. Contrary to our hypothesis, flanker interactions were not systematically affected by either receptor blockade.

Neocortical activity is permeated with endogenously generated fluctuations, but how these dynamics affect goal-directed behavior remains a mystery. We found that ensemble neural activity in primate visual cortex spontaneously fluctuated between phases of vigorous (On) and faint (Off) spiking synchronously across cortical layers. These On-Off dynamics, reflecting global changes in cortical state, were also modulated at a local scale during selective attention. Moreover, the momentary phase of local ensemble activity predicted behavioral performance. Our results show that cortical state is controlled locally within a cortical map according to cognitive demands and reveal the impact of these local changes in cortical state on goal-directed behavior.

Summary Spontaneous fluctuations in cortical excitability influence sensory processing and behavior. These fluctuations, long thought to reflect global changes in cortical state, were recently found to be modulated locally within a retinotopic map during spatially selective attention. We report that periods of vigorous (On) and faint (Off) spiking activity, the signature of cortical state fluctuations, are coordinated across brain areas with retinotopic precision. Top-down attention enhanced interareal local state coordination, traversing along the reverse cortical hierarchy. The extent of local state coordination between areas was predictive of behavioral performance. Our results show that cortical state dynamics are shared across brain regions, modulated by cognitive demands and relevant for behavior., Highlights • Cortical excitability fluctuations are coordinated across visual areas • During selective attention, these fluctuations are driven in a top-down manner • The degree of coordination depends on shared spatial representation • Increased cortical state coordination predicts better behavioral performance, How do fluctuations in ongoing brain activity interact with cognitive functions? In this study, van Kempen et al. show that fluctuations in neural excitability are coordinated between visual areas with retinotopic precision. Top-down attention drives interareal coordination along the reverse cortical hierarchy, predicting better behavioral performance with increased coordination.

Attention affects neuronal processing and improves behavioural performance. In extrastriate visual cortex these effects have been explained by normalization models, which assume that attention influences the circuit that mediates surround suppression. While normalization models have been able to explain attentional effects, their validity has rarely been tested against alternative models. Here we investigate how attention and surround/mask stimuli affect neuronal firing rates and orientation tuning in macaque V1. Surround/mask stimuli provide an estimate to what extent V1 neurons are affected by normalization, which was compared against effects of spatial top down attention. For some attention/surround effect comparisons, the strength of attentional modulation was correlated with the strength of surround modulation, suggesting that attention and surround/mask stimulation (i.e. normalization) might use a common mechanism. To explore this in detail, we fitted multiplicative and additive models of attention to our data. In one class of models, attention contributed to normalization mechanisms, whereas in a different class of models it did not. Model selection based on Akaike's and on Bayesian information criteria demonstrated that in most cells the effects of attention were best described by models where attention did not contribute to normalization mechanisms. This demonstrates that attentional influences on neuronal responses in primary visual cortex often bypass normalization mechanisms.

Summary Attention improves perception by affecting different aspects of the neuronal code. It enhances firing rates, it reduces firing rate variability and noise correlations of neurons, and it alters the strength of oscillatory activity. Attention-induced rate enhancement in striate cortex requires cholinergic mechanisms. The neuropharmacological mechanisms responsible for attention-induced variance and noise correlation reduction or those supporting changes in oscillatory activity are unknown. We show that ionotropic glutamatergic receptor activation is required for attention-induced rate variance, noise correlation, and LFP gamma power reduction in macaque V1, but not for attention-induced rate modulations. NMDA receptors mediate attention-induced variance reduction and attention-induced noise correlation reduction. Our results demonstrate that attention improves sensory processing by a variety of mechanisms that are dissociable at the receptor level., Highlights • NMDA receptors aid variance and covariance reduction • Cholinergic and NMDA receptors serve different functions in attentional modulation • Attention affects second-order statistics of neuronal activity in V1 • NMDA and AMPA receptor blockade oppositely affect V1 gamma frequency oscillations, Attention improves neuronal processing by increasing response strength and fidelity. Herrero et al. show that NMDA receptor availability is selectively required for increased response fidelity. The study isolates attentional mechanisms at the receptor level.

The functional magnetic resonance imaging (fMRI) blood oxygenation level-dependent (BOLD) signal is regularly used to assign neuronal activity to cognitive function. Recent analyses have shown that the local field potential (LFP) gamma power is a better predictor of the fMRI BOLD signal than spiking activity. However, LFP gamma power and spiking activity are usually correlated, clouding the analysis of the neural basis of the BOLD signal. We show that changes in LFP gamma power and spiking activity in the primary visual cortex (V1) of the awake primate can be dissociated by using grating and plaid pattern stimuli, which differentially engage surround suppression and cross-orientation inhibition/facilitation within and between cortical columns. Grating presentation yielded substantial V1 LFP gamma frequency oscillations and significant multi-unit activity. Plaid pattern presentation significantly reduced the LFP gamma power while increasing population multi-unit activity. The fMRI BOLD activity followed the LFP gamma power changes, not the multi-unit activity. Inference of neuronal activity from the fMRI BOLD signal thus requires detailed a priori knowledge of how different stimuli or tasks activate the cortical network.

Attention increases our ability to detect behaviorally relevant stimuli. At the neuronal level this is supported by increased firing rates of neurons representing the attended object. In primary visual cortex an attention-mediated activity increase depends on the presence of the neuromodulator acetylcholine. Using a spiking network model of visual cortex we have investigated how acetylcholine interacts with biased feedback to enable attentional processing. Although acetylcholine affects cortical processing in a multitude of manners, we restricted our analysis to four of its main established actions. These were (i) a reduction in firing rate adaptation by reduction in M-currents (muscarinic), (ii) an increase in thalamocortical synaptic efficacy by nicotinic presynaptic receptors, (iii) a reduction in lateral interactions by muscarinic presynaptic receptors, and (iv) an increase in inhibitory drive by muscarinic receptors located on inhibitory interneurons. We found that acetylcholine contributes to feedback-mediated attentional modulation, mostly by reducing intracortical interactions and also to some extent by increasing the inhibitory drive. These findings help explain why acetylcholine is necessary for top‐down-driven attentional modulation, and suggest a close interdependence of cholinergic and feedback drive in mediating cognitive function.

Summary Rhythmic activity of neuronal ensembles has been proposed to play an important role in cognitive functions such as attention, perception, and memory. Here we investigate whether rhythmic activity in V1 of the macaque monkey (macaca mulatta) is affected by top-down visual attention. We measured the local field potential (LFP) and V1 spiking activity while monkeys performed an attention-demanding detection task. We show that gamma oscillations were strongly modulated by the stimulus and by attention. Stimuli that engaged inhibitory mechanisms induced the largest gamma LFP oscillations and the largest spike field coherence. Directing attention toward a visual stimulus at the receptive field of the recorded neurons decreased LFP gamma power and gamma spike field coherence. This decrease could reflect an attention-mediated reduction of surround inhibition. Changes in synchrony in V1 would thus be a byproduct of reduced inhibitory drive, rather than a mechanism that directly aids perceptual processing., Highlights ► Gamma synchronization in V1 depends on activation of normalization mechanisms ► Attention reduces strength of LFP gamma synchronization in V1 ► Attention reduces spike field coherence in V1 ► Increased gamma spike field coherence in is not a universal mechanism of attention

The visual system encodes the features of visual stimuli as well as their behavioral relevance. Stimuli with a high luminance contrast evoke more activity in the visual cortex than stimuli with a low contrast. At the same time, attended stimuli evoke more activity than nonattended stimuli. There is a debate about how visual features and attention jointly determine neuronal activity in the visual cortex. Some studies suggested that attention increases apparent contrast (Reynolds et al., 2000), others that attention amplifies responses by a constant factor (Williford and Maunsell, 2006), and yet others that attention and contrast have largely additive effects (Buracas and Boynton, 2007; Thiele et al., 2009). The influence of attention on contrast sensitivity differs between neurons, raising the possibility that attention and contrast could be coded conjointly in a population of neurons. Here we investigate this possibility by recording neuronal activity at multiple sites in the primary visual cortex of macaque monkeys using multielectrode recording techniques and support vector machines to decode attended stimuli as well as stimulus contrast. We find that many, but not all, V1 neurons are influenced by attention and that the effects of attention and contrast are additive on average. Stimulus contrast can be decoded from neuronal responses not strongly modulated by attention, whereas the attended stimulus can be decoded as the difference in activity of cells that are influenced by attention and cells that are not. The success of the approach suggests that visual attention and stimulus contrast are represented by largely separable codes. Copyright © 2010 the authors.

Attention can selectively enhance neuronal responses and exclude external noise, but the neuronal computations that underlie these effects remain unknown. At the neuronal level, noise exclusion might result in altered spatial integration properties. We tested this proposal by recording neuronal activity and length tuning in neurons of the primary visual cortex of the macaque when attention was directed toward or away from stimuli presented in each neuron's classical receptive field. For cells with central-parafoveal receptive fields, attention reduced spatial integration, as demonstrated by a reduction in preferred stimulus length and in the size of the spatial summation area. Conversely, in cells that represented more peripheral locations, attention increased spatial integration by increasing the cell's summation area. This previously unknown dichotomy between central and peripheral vision could support accurate analysis of attended foveal objects and target selection for impending eye movements to peripheral objects.

In normal vision, visual scenes are predictable, as they are both spatially and temporally redundant. Evidence suggests that the visual system may use the spatio-temporal regularities of the external world, available in the retinal signal, to extract information from the visual environment and better reconstruct current and future stimuli. We studied this by recording neuronal responses of primary visual cortex (area V1) in anaesthetized and paralysed macaques during the presentation of dynamic sequences of bars, in which spatio-temporal regularities and local information were independently manipulated. Most V1 neurons were significantly modulated by events prior to and distant from stimulation of their classical receptive fields (CRFs); many were more strongly tuned to prior and distant events than they were to CRFs bars; and several showed tuning to prior information without any CRF stimulation. Hence, V1 neurons do not simply analyse local contours, but impute local features to the visual world, on the basis of prior knowledge of a visual world in which useful information can be distributed widely in space and time.

Cortical processing is strongly influenced by the actions of neuromodulators such as acetylcholine (ACh). Early studies in anaesthetized cats argued that acetylcholine can cause a sharpening of orientation tuning functions and an improvement of the signal-to-noise ratio (SNR) of neuronal responses in primary visual cortex (V1). Recent in vitro studies have demonstrated that acetylcholine reduces the efficacy of feedback and intracortical connections via the activation of muscarinic receptors, and increases the efficacy of feed-forward connections via the activation of nicotinic receptors. If orientation tuning is mediated or enhanced by intracortical connections, high levels of acetylcholine should diminish orientation tuning. Here we investigate the effects of acetylcholine on orientation tuning and neuronal responsiveness in anaesthetized marmoset monkeys. We found that acetylcholine caused a broadening of the orientation tuning in the majority of cells, while tuning functions became sharper in only a minority of cells. Moreover, acetylcholine generally facilitated neuronal responses, but neither improved signal-to-noise ratio, nor reduced trial-to-trial firing rate variance systematically. Acetylcholine did however, reduce variability of spike occurrences within spike trains. We discuss these findings in the context of dynamic control of feed-forward and lateral ⁄ feedback connectivity by acetylcholine.

We develop new data-robust lower-bound methods to quantify the information carried by the timing of spikes emitted by neuronal populations. These methods have better sampling properties and are tighter than previous bounds based on neglecting correlation in the noise entropy. Our new lower bounds are precise also in the presence of strongly correlated firing. They are not precise only if correlations are strongly stimulus modulated over a long time range. Under conditions typical of many neurophysiological experiments, these techniques permit precise information estimates to be made even with data samples that are three orders of magnitude smaller than the size of the response space.

Spatial and temporal regularities commonly exist in natural visual scenes. The knowledge of the probability structure of these regularities is likely to be informative for an efficient visual system. Here we explored how manipulating the spatio–temporal prior probability of stimuli affects human orientation perception. Stimulus sequences comprised four collinear bars (predictors) which appeared successively towards the foveal region, followed by a target bar with the same or different orientation. Subjects' orientation perception of the foveal target was biased towards the orientation of the predictors when presented in a highly ordered and predictable sequence. The discrimination thresholds were significantly elevated in proportion to increasing prior probabilities of the predictors. Breaking this sequence, by randomising presentation order or presentation duration, decreased the thresholds. These psychophysical observations are consistent with a Bayesian model, suggesting that a predictable spatio–temporal stimulus structure and an increased probability of collinear trials are associated with the increasing prior expectation of collinear events. Our results suggest that statistical spatio–temporal stimulus regularities are effectively integrated by human visual cortex over a range of spatial and temporal positions, thereby systematically affecting perception.

Inhibitory mechanisms contribute to directional tuning in primary visual cortex, and it has been suggested that, in the primate brain, the middle temporal area (MT) inherits most of its directional information from primary visual cortex (V1). To test the validity of this hierarchical scheme, we investigated whether directional tuning in MT was present upon blockade of local γ-aminobutyratergic (GABAergic) inhibitory mechanisms. Direction selectivity during the initial 50 ms after response onset was abolished in many MT cells when the local inhibitory network was inactivated whereas direction selectivity in later response periods was largely unaffected. Thus, direction selectivity during early response periods is often generated autonomously within MT whereas direction selectivity during later response periods is either inherited from other visual areas or locally mediated by mechanisms other than γ-aminobutyric acid type A receptor (GABA A ) inhibition. GABAergic inhibition may also mediate contrast normalization. Our data suggest that GABA A inhibition implements a local direction-selective static nonlinearity, rather than a full normalization in MT. These findings put constraints on strict hierarchical models according to which MT performs more complex computations based on local motion measurements provided by earlier areas, arguing for more distributed and independent information processing.

Human psychophysical studies have demonstrated that, for stimuli near the threshold of visibility, detection of motion in one direction is unaffected by the superimposition of motion in the opposite direction. To investigate the neural basis for this perceptual phenomenon, we recorded from directionally selective neurons in macaque visual area MT (middle temporal visual area). Contrast thresholds obtained for single gratings moving in a neuron's preferred direction were compared with those obtained for motion presented simultaneously in the neuron's preferred and anti–preferred directions. A simple model based on probability summation between neurons tuned to opposite directions could sufficiently account for contrast thresholds revealed psychophysically, suggesting that area MT is likely to provide the neural basis for contrast detection of stimuli modulated in time.

One adult monkey (Macaca fascicularis) was investigated psychophysically and electrophysiologically after at least 5 years of late onset esotropic macrostrabismus (squint angle 52 deg). Behavioural tests revealed normal monocular visual and visuomotor functions. No indications of deep amblyopia or oculomotor asymmetry were found. The monkey used the left or right eye alternately at about equal frequencies. Single unit recordings from area V1 disclosed a normal ocular dominance distribution. Most V1 neurons from both hemispheres received binocular input. Thus, discordant visual information from corresponding retinal locations of the two eyes converged onto the cortical neurons. No evidence for anomalous retinal correspondence was found. Diplopia and confusion must therefore be avoided by suppression of vision through one eye to allow stable, unambiguous perception. Possible suppression was investigated by stimulating a neuron through the same eye when it was actively used for fixation in one set of trials, and when it was not used for fixation in another set of trials. Significant differences in these two stimulus conditions were found in 2039 neurons from area V1 and in 1134 motion sensitive neurons recorded in the middle superior temporal area (MT). The normalized population activity in V1 and MT was higher if cells were stimulated through the fixating eye. The data are discussed with respect to possible suppressive mechanisms helping to prevent double vision in strabismus and in binocular rivalry. © 1997 Elsevier Science Ltd. All rights reserved.

SINGLE units in the middle temporal area (MT), the middle superior temporal area (MST) and the upper part of the superior temporal polysensory area (STP p ) of the monkey's brain were recorded during the discrimination of direction of visual motion near contrast threshold. In addition to stimulus-related decisions the monkeys often made stimulus-independent decisions while stimuli were well below detection threshold (contrast

Our ability to make fine visual discriminations improves with practice, and so at some level so must our visual system. A new paper reports that the receptive field structure of a neuron can be fine-tuned for different visual tasks. These findings raise important questions about the circuitry and mechanisms that underly perceptual learning.

Previous studies have investigated the effects of acetylcholine (ACh) on neuronal tuning, coding, and attention in primary visual cortex, but its contribution to coding in extrastriate cortex is unexplored. Here we investigate the effects of ACh on tuning properties of macaque middle temporal area MT neurons and contrast them with effects of gabazine, a GABAAreceptor blocker. ACh increased neuronal activity, it had no effect on tuning width, but it significantly increased the direction discriminability of a neuron. Gabazine equally increased neuronal activity, but it widened tuning curves and decreased the direction discriminability of a neuron. Although gabazine significantly reduced response reliability, ACh application had little effect on response reliability. Finally, gabazine increased noise correlation of simultaneously recorded neurons, whereas ACh reduced it. Thus, both drugs increased firing rates, but only ACh application improved neuronal tuning and coding in line with effects seen in studies in which attention was selectively manipulated.

The perceptual salience and visibility of image elements is influenced by other elements in their vicinity. The perceptual effect of image elements on an adjacent target element depends on their relative orientation. Collinear flanking elements usually improve sensitivity for the target element, whereas orthogonal elements have a weaker effect. It is believed that the collinear flankers exert these effects through lateral interactions between neurons in the primary visual cortex (area V1), but the precise mechanisms underlying these contextual interactions remain unknown. Here, we directly examined this question by recording the effects of flankers on the responses of V1 neurons at parafoveal representations while monkeys performed a fixation task or a contrast detection task. We found, unexpectedly, that collinear flankers reduce the monkeys' perceptual sensitivity for a central target element. This behavioral effect was explained by a flanker-induced increase in the activity of V1 neurons in the absence of the central target stimulus, which reduced the amplitude of the target response. Our results indicate that the dominant effect of collinear flankers in parafoveal vision is suppression and suggest that these suppressive effects are caused by a decrease in the dynamic range of neurons coding the central target. Copyright © 2010 the authors.

Previous studies have proposed a variety of mechanisms by which attention influences neuronal activity. Here we investigated the mechanisms of attention in the striate cortex of monkeys performing a spatial or an object-based attention task at various stimulus contrasts and compared neuronal contrast response functions with and without attention. Our data are best described by an “additive” interaction: The influence of attention on the neuronal response is relatively independent of the stimulus contrast, at least when the stimulus has enough contrast to become visible. This shows that attention adds to the neuronal responses in a largely contrast invariant manner. These data support recent functional magnetic resonance imaging studies and suggest that feedback from higher areas exerts a constant attentional drive that is mostly task not stimulus driven.

Attention can selectively enhance neuronal responses and exclude external noise. To investigate these effects and their neuronal mechanisms we investigated spatial integration and the underlying neuronal mechanisms in primary visual cortex. We found evidence for spatial filtering mechanisms, whereby attention reduced spatial integration in macaque V1 neurons. To study possible mechanisms of this effect, we measured length tuning in V1 in the presence and absence of externally applied acetylcholine. The effects of acetylcholine application and attention in V1 were largely similar. Acetylcholine reduced spatial integration by reducing the neuron’s summation area. Thus, attention can alter perceptual and neuronal spatial integration, and acetylcholine may contribute to these task dependent receptive field dynamics.

Neurons in primary visual cortex exhibit well documented centre-surround receptive field organization, whereby the centre is dominated by excitatory influences and the surround is generally dominated by inhibitory influences. These effects have largely been established by measuring the output of neurons, i.e. their spiking activity. How excitation and inhibition are reflected in the local field potential (LFP) is little understood. As this can bear on the interpretation of human fMRI BOLD data and on our understanding of the mechanisms of local field potential oscillations, we measured spatial integration and centre-surround properties in single- and multiunit recordings of V1 in the awake fixating macaque monkey, and compared these to spectral power in different frequency bands of simultaneously recorded LFPs. We quantified centre-surround organization by determining the size of the summation and suppression area in spiking activity as well as in different frequency bands of the LFP, with the main focus on the gamma band. Gratings extending beyond the summation area usually inhibited spiking activity while the LFP gamma-band activity increased monotonically for all grating sizes. This increase was maximal for stimuli infringing upon the near classical receptive field surround, where suppression started to dominate spiking activity. Thus, suppressive influences in primary cortex can be inferred from spiking activity, but they also seem to affect specific features of gamma-band LFP activity.

In normal vision, visual scenes are predictable, as they are both spatially and temporally redundant. Evidence suggests that the visual system may use the spatio-temporal regularities of the external world, available in the retinal signal, to extract information from the visual environment and better reconstruct current and future stimuli. We studied this by recording neuronal responses of primary visual cortex (area V1) in anaesthetized and paralysed macaques during the presentation of dynamic sequences of bars, in which spatio-temporal regularities and local information were independently manipulated. Most V1 neurons were significantly modulated by events prior to and distant from stimulation of their classical receptive fields (CRFs); many were more strongly tuned to prior and distant events than they were to CRFs bars; and several showed tuning to prior information without any CRF stimulation. Hence, V1 neurons do not simply analyse local contours, but impute local features to the visual world, on the basis of prior knowledge of a visual world in which useful information can be distributed widely in space and time.

We move our eyes more often than our heart beats. Our brain seems to cope effortlessly with the consequences of these rapid visual alterations, but a new study shows that similar scene changes in the absence of eye movements delay the speed of information processing. So are there costs in constantly shifting our focus of gaze?

Recent in vitro studies have shown that acetylcholine (ACh) selectively reduces the efficacy of lateral cortical connections via a muscarinic mechanism, while boosting the efficacy of thalamocortical/feed-forward connections via a nicotinic mechanism. This suggests that high levels of ACh should reduce center-surround interactions of neurons in primary visual cortex, making cells more reliant on feed-forward information. In line with this hypothesis, we show that local iontophoretic application of ACh in primate primary visual cortex reduced the extent of spatial integration, assessed by recording a neurons' length tuning. When ACh was externally applied, neurons' preferred length shifted toward shorter bars, showing reduced impact of the extra-classical receptive field. We fitted a difference and a ratio of Gaussian model to these data to determine the underlying mechanisms of this dynamic change of spatial integration. These models assume overlapping summation and suppression areas with different widths and gains to be responsible for spatial integration and size tuning. ACh significantly reduced the extent of the summation area, but had no significant effect on the extent of the suppression area. In line with previous studies, we also show that applying ACh enhanced the response in the majority of cells, especially in the later (sustained) part of the response. These findings are similar to effects of attention on neuronal activity. The natural release of ACh is strongly linked with states of arousal and attention. Our results may therefore be relevant to the neurobiological mechanism of attention.

Our ability to perceive, attend, and memorize depends on bidirectional information exchange between hierarchically organized brain areas. Areas lower in the hierarchy send information through feedforward connections to higher areas. Higher areas modulate the activity in lower areas by means of feedback connections, and thereby influence the local processing as well as the information they receive. Although this scheme is well accepted, the exact role of feedforward and feedback connections in cognition is still poorly understood, let alone the mechanisms by which they mediate their effects. A report by Self et al. (1) in PNAS sheds light on the mechanisms involved. They delineate the different receptor types that contribute to feedforward and to feedback processing. They recorded neuronal activity from macaque primary visual cortex (V1) while animals performed a figure-ground detection task. V1 neurons in awake animals show differential activity depending on whether they represent the figure (2, 3) or whether they represent the background, even if the image within their receptive field is identical under both conditions. This differential activity is known as figure-ground modulation, and it depends …

We have shown previously that neurons in the middle temporal (MT) area of primate cortex have inseparable spatiotemporal receptive fields—their response profiles exhibit a ridge that is oriented in the spatiotemporal frequency domain, and this orientation predicts the neurons' preferred speed. When measured in spatiotemporal frequency space, such MT spectral receptive field (SRF) properties are closely matched to the spectrum generated by a moving edge. In contrast, V1 neurons have SRF properties that are poorly matched to moving edge spectra, indicating that V1 neurons are not tuned to a particular image speed but rather to specific spatial and temporal frequencies. Here we describe a neural mechanism based directly on the properties of V1 neurons that is able to explain the SRF change that occurs between V1 and MT. We outline the theory behind this transformation and posit an explanation for how the visual system extracts true speed (independent of spatial frequency) from retinal image motion. We tested this speed model against our MT neuron data and found that it provides an excellent account of speed tuning in MT.

Knowing the direction and speed of moving objects is often critical for survival. However, it is poorly understood how cortical neurons process the speed of image movement. Here we tested MT neurons using moving sine-wave gratings of different spatial and temporal frequencies, and mapped out the neurons' spatiotemporal frequency response profiles. The maps typically had oriented ridges of peak sensitivity as expected for speed-tuned neurons. The preferred speed estimate, derived from the orientation of the maps, corresponded well to the preferred speed when moving bars were presented. Thus, our data demonstrate that MT neurons are truly sensitive to the object speed. These findings indicate that MT is not only a key structure in the analysis of direction of motion and depth perception, but also in the analysis of object speed.

The human spectral luminosity function (V(lambda)) can be modeled as the linear sum of signals from long-wavelength-selective (L) and middle-wavelength-selective (M) cones, with L cones being weighted by a factor of approximately 2. This factor of approximately 2 is thought to reflect an approximate 2:1 ratio of L:M cones in the human retina, which has been supported by studies that allow for more direct counting of different cone types in the retina. In contrast to humans, several lines of retinally based evidence in macaques suggest an L:M ratio closer to 1:1. To investigate the consequences of differences in L:M cone ratios between humans and macaques, red-green equiluminance matches obtained psychophysically in humans (n = 11) were compared with those obtained electrophysiologically from single neurons in the extrastriate middle temporal visual area of macaques (M. mulatta, n = 5). Neurons in the middle temporal visual area were tested with sinusoidal red-green moving gratings across a range of luminance contrasts, with equiluminance being defined as the red-green contrast yielding a response minimum. Human subjects were tested under analogous conditions, by a minimally distinct motion technique, to establish psychophysical equiluminance. Although red-green equiluminance points in both humans and macaques were found to vary across individuals, the means across species differed significantly; compared with humans, macaque equiluminance points reflected relatively greater sensitivity to green. By means of a simple model based on equating the weighted sum of L and M cone signals, the observed red-green equiluminance points were found to be consistent with L:M cone ratios of approximately 2:1 in humans and 1:1 in macaques. These data thus support retinally based estimates of L:M cone ratios and further demonstrate that the information carried in the cone mosaic has functional consequences for red-green spectral sensitivity revealed perceptually and in the dorsal stream of visual cortex.

Neurones in higher visual motion areas in the superior temporal sulcus (STS) of the macaque monkey respond to abstract random dot optic flow stimuli. Higher motion areas may not only represent, but in a next computational stage also analyse the flow field to determine, for instance, the direction of heading for navigation purposes. Real world visual scenes differ in several aspects from these abstract optic flow stimuli. We tested the neuronal response to naturalistic optic flow stimuli which simulated egomotion in different virtual environments and contained different numbers of visual cues. Neuronal activity depended mainly on the position of the focus of expansion rather than on other visual cues. This finding supports the hypothesis that higher motion areas within the STS analyse optic flow in natural scenes and can thus signal the direction of heading.

We developed a novel design of an electrode–pipette combination (EPC) which allows access to brain structures in awake behaving primates without the need for guide tubes or to mechanically open the dura prior to electrode insertion. The EPC consists of an etched tungsten in glass electrode flanked by two pipettes which allow for local and highly controlled iontophoretic administration of neuroactive substances. These EPCs have excellent single cell isolation properties and are sturdy enough to penetrate the primate dura for up to 8 weeks following either a craniotomy or a dura scrape (i.e. even after substantial built up of fibrous scar tissue). We show that the EPCs can be used to selectively manipulate the cholinergic system in primate V1 during passive fixation and while animals perform an attentionally demanding task.

Non-human-primate fMRI is becoming increasingly recognised as the missing link between the widely applied methods of human imaging and intracortical animal electrophysiology. A crucial requirement for the optimal application of this method is the precise knowledge of the time course of the Blood Oxygenation Level Dependent (BOLD) signal. We mapped the BOLD signal time course in the inferior colliculus (IC), medial geniculate body (MGB) and in tonotopically defined fields in the auditory cortex of two macaques. The results show little differences in the BOLD-signal time courses within the auditory pathway. However, we observed systematic differences in the magnitude of the change in the BOLD signal with significantly stronger signal changes in field A1 of the auditory cortex compared to field R. The measured time course of the signal was in good agreement with similar studies in human auditory cortex but showed considerable differences to data reported from macaque visual cortex. Consistent with the studies in humans we measured a peak in the BOLD response around 4 s after the onset of 2-s broadband noise stimuli while previous studies recorded from the primary visual cortex of the same species reported the earliest peaks to short visual stimuli several seconds later. The comparison of our results with previous studies does not support differences in haemodynamic responses within the auditory system between human and non-human primates. Furthermore, the data will aid optimal design of future auditory fMRI studies in non-human primates.