Selective attention sharpens population receptive fields in human auditory cortex.

Selective attention enables the preferential processing of relevant stimulus aspects. Invasive animal studies have shown that attending a sound feature rapidly modifies neuronal tuning throughout the auditory cortex. Human neuroimaging studies have reported enhanced auditory cortical responses with selective attention. To date, it remains unclear how the results obtained with functional magnetic resonance imaging (fMRI) in humans relate to the electrophysiological findings in animal models. Here we aim to narrow the gap between animal and human research by combining a selective attention task similar in design to those used in animal electrophysiology with high spatial resolution ultra-high field fMRI at 7 Tesla. Specifically, human participants perform a detection task, whereas the probability of target occurrence varies with sound frequency. Contrary to previous fMRI studies, we show that selective attention resulted in population receptive field sharpening, and consequently reduced responses, at the attended sound frequencies. The difference between our results to those of previous fMRI studies supports the notion that the influence of selective attention on auditory cortex is diverse and may depend on context, stimulus, and task.

Micropools of reliable area MT neurons explain rapid motion detection.

Many models of perceptually based decisions postulate that actions are initiated when accumulated sensory signals reach a threshold level of activity. These models have received considerable neurophysiological support from recordings of individual neurons while animals are engaged in motion discrimination tasks. These experiments have found that the activity of neurons in a particular visual area strongly associated with motion processing (MT), when pooled over hundreds of milliseconds, is sufficient to explain behavioral timing and performance. However, this level of pooling may be problematic for urgent perceptual decisions in which rapid detection dictates temporally precise integration. In this paper, we explore the physiological basis of one such task in which macaques detected brief (~70 ms) transients of coherent motion within ~240 ms. We find that a simple linear summation model based on realistic stimulus responses of as few as 40 correlated neurons can predict the reliability and timing of rapid motion detection. The model naturally reproduces a distinctive physiological relationship observed in rapid detection tasks in which the individual neurons with the most reliable stimulus responses are also the most predictive of impending behavioral choices. Remarkably, we observed this relationship across our simulated neuronal populations even when all neurons within the pool were weighted equally with respect to readout. These results demonstrate that small numbers of reliable sensory neurons can dominate perceptual judgments without any explicit reliability based weighting and are sufficient to explain the accuracy, latency, and temporal precision of rapid detection. NEW & NOTEWORTHY Computational and psychophysical models suggest that performance in many perceptual tasks may be based on the preferential sampling of reliable neurons. Recent studies of MT neurons during rapid motion detection, in which only those neurons with the most reliable sensory responses were strongly predictive of the animals' decisions, seemingly support this notion. Here we show that a simple threshold model without explicit reliability biases can explain both the behavioral accuracy and precision of these detections and the distribution of sensory- and choice-related signals across neurons.

Population coding in area V4 during rapid shape detections.

While previous studies have suggested that neuronal correlations are common in visual cortex over a range of timescales, the effect of correlations on rapid visually based decisions has received little attention. We trained Macaca mulatta to saccade to a peripherally presented shape embedded in dynamic noise as soon as the shape appeared. While the monkeys performed the task, we recorded from neuronal populations (5-29 cells) using a microelectrode array implanted in area V4, a visual area thought to be involved in form perception. While modest correlations were present between cells during visual stimulation, their magnitude did not change significantly subsequent to the appearance of a shape. We quantified the reliability and temporal precision with which neuronal populations signaled the appearance of the shape and predicted the animals' choices using mutual information analyses. To study the impact of correlations, we shuffled the activity from each cell across observations while retaining stimulus-dependent modulations in firing rate. We found that removing correlations by shuffling across trials minimally affected the reliability or timing with which pairs, or larger groups of cells, signaled the presence of a shape. To assess the downstream impact of correlations, we also studied how shuffling affected the ability of V4 populations to predict behavioral choices. Surprisingly, shuffling created a modest increase in the accuracy of such predictions, suggesting that the reliability of downstream neurons is slightly compromised by activity correlations. Our findings are consistent with neuronal correlations having a minimal effect on the reliability and timing of rapid perceptual decisions.

Temporal production signals in parietal cortex.

We often perform movements and actions on the basis of internal motivations and without any explicit instructions or cues. One common example of such behaviors is our ability to initiate movements solely on the basis of an internally generated sense of the passage of time. In order to isolate the neuronal signals responsible for such timed behaviors, we devised a task that requires nonhuman primates to move their eyes consistently at regular time intervals in the absence of any external stimulus events and without an immediate expectation of reward. Despite the lack of sensory information, we found that animals were remarkably precise and consistent in timed behaviors, with standard deviations on the order of 100 ms. To examine the potential neural basis of this precision, we recorded from single neurons in the lateral intraparietal area (LIP), which has been implicated in the planning and execution of eye movements. In contrast to previous studies that observed a build-up of activity associated with the passage of time, we found that LIP activity decreased at a constant rate between timed movements. Moreover, the magnitude of activity was predictive of the timing of the impending movement. Interestingly, this relationship depended on eye movement direction: activity was negatively correlated with timing when the upcoming saccade was toward the neuron's response field and positively correlated when the upcoming saccade was directed away from the response field. This suggests that LIP activity encodes timed movements in a push-pull manner by signaling for both saccade initiation towards one target and prolonged fixation for the other target. Thus timed movements in this task appear to reflect the competition between local populations of task relevant neurons rather than a global timing signal.

Inattention blindness to motion in middle temporal area.

Subjects naturally form and use expectations to solve familiar tasks, but the accuracy of these expectations and the neuronal mechanisms by which these expectations enhance behavior are unclear. We trained animals (Macaca mulatta) in a challenging perceptual task in which the likelihood of a very brief pulse of motion was consistently modulated over time and space. Pulse likelihood had dramatic effects on behavior: unexpected pulses were nearly invisible to the animals. To examine the neuronal basis of such inattention blindness, we recorded from single neurons in the middle temporal (MT) area, an area related to motion perception. Fluctuations in how reliably MT neurons both signaled stimulus events and predicted behavioral choices were highly correlated with changes in performance over the course of individual trials. A simple neuronal pooling model reveals that the dramatic behavioral effects of attention in this task can be completely explained by changes in the reliability of a small number of MT neurons.

Spatial summation can explain the attentional modulation of neuronal responses to multiple stimuli in area V4.

Although many studies have shown that the activity of individual neurons in a variety of visual areas is modulated by attention, a fundamental question remains unresolved: can attention alter the visual representations of individual neurons? One set of studies, primarily relying on the attentional modulations observed when a single stimulus is presented within the receptive field of a neuron, suggests that neuronal selectivities, such as orientation or direction tuning, are not fundamentally altered by attention (Salinas and Abbott, 1997; McAdams and Maunsell, 1999; Treue and Martinez Trujillo, 1999). Another set of studies, relying on modulations observed when multiple stimuli are presented within a receptive field, suggests that attention can alter the weighting of sensory inputs (Moran and Desimone, 1985; Luck et al., 1997; Reynolds et al., 1999; Chelazzi et al., 2001). In these studies, when preferred and nonpreferred stimuli are simultaneously presented, responses are much stronger when attention is directed to the preferred stimulus than when it is directed to the nonpreferred stimulus. In this study, we recorded neuronal responses from individual neurons in visual cortical area V4 to both single and paired stimuli with a variety of attentional allocations and stimulus combinations. For each neuron studied, we constructed a quantitative model of input summation and then tested various models of attention. In many neurons, we are able to explain neuronal responses across the entire range of stimuli and attentional allocations tested. Specifically, we are able to reconcile seemingly inconsistent observations of single and paired stimuli attentional modulation with a new model in which attention can facilitate or suppress specific inputs to a neuron but does not fundamentally alter the integration of these inputs.

Spatial attention does not strongly modulate neuronal responses in early human visual cortex.

Attention can dramatically enhance behavioral performance based on a visual stimulus, but the degree to which attention modulates activity in early visual cortex is unclear. Whereas single-unit studies of spatial attention in monkeys have repeatedly revealed relatively modest attentional modulations in V1, human functional magnetic resonance imaging studies demonstrate a large attentional enhancement of the blood oxygen level-dependent (BOLD) signal in V1. To explore this discrepancy, we used intracranial electrodes to directly measure the effect of spatial attention on the responses of neurons near the human occipital pole. We found that spatial attention does not robustly modulate stimulus-driven local field potentials in early human visual cortex, but instead produces modest modulations that are consistent with those seen in monkey neurophysiology experiments. This finding suggests that the neuronal activity that underlies visual attention in humans is similar to that found in other primates and that behavioral state may alter the linear relationship between neuronal activity and BOLD.

Integration of color, orientation, and size functional domains in the ventral pathway.

Functional specialization within the extrastriate areas of the ventral pathway associated with visual form analysis is poorly understood. Studies comparing the functional selectivities of neurons within the early visual areas have found that there are more similar than different between the areas. We simultaneously imaged visually evoked activation over regions of V2 and V4 and parametrically varied three visual attributes for which selectivity exists in both areas: color, orientation, and size. We found that color selective regions were observed in both areas and were of similar size and spatial distribution. However, two major areal distinctions were observed: V4 contained a greater number and diversity of color-specific regions than V2 and exhibited a higher degree of overlap between domains for different functional attributes. In V2, size and color regions were largely segregated from orientation domains, whereas in V4 both color and size regions overlapped considerably with orientation regions. Our results suggest that higher-order composite selectivities in the extrastriate cortex may arise organically from the interactions afforded by an overlap of functional domains for lower order selectivities.

Learning in mammalian sensory cortex.

The improvement of perceptual capabilities with training can offer important insight into the physiological basis of learning in the cerebral cortex. The rapid time course and ease with which some perceptual capabilities can improve suggest that learning is an integral part of normal perception. Electrophysiological and neuroimaging studies of sensory systems in the cortex suggest that the changes underlying perceptual learning can occur in a variety of areas and are likely to involve multiple mechanisms. In particular, recent psychological and physiological studies suggest that perceptual learning might often involve the task-specific suppression of signals that interfere with performance.

Strategies optimize the detection of motion transients.

Strategies are implicitly formed when a task is consistent and can be used to improve performance. To investigate how strategies can alter perceptual performance, I trained animals in a reaction time (RT) detection task in which the probability of a fixed duration motion pulse appearing varied over time in a consistent manner. Consistent with previous studies suggesting the implicit representation of task timing, I found that RTs were inversely related to the probability of the pulse appearing and decreased with training. I then inferred the sensory integration underlying responses using behavioral reverse correlation analysis. This analysis revealed that training and anticipation optimized detection by improving the correlation between sensory integration and the spatiotemporal extent of the motion pulse. Moreover, I found that these improvements in sensory integration could largely explain observed changes in the distribution of RT with training and anticipation. These results suggest that training can increase detection performance by optimizing sensory integration according to implicitly formed representations of the likelihood and nature of the stimulus.

Improvement of Eye Alignment in Adult Strabismic Monkeys by Sustained IGF-1 Treatment.

PURPOSE: The goal of this study was to determine if continuous application of insulin-like growth factor-1 (IGF-1) could improve eye alignment of adult strabismic nonhuman primates and to assess possible mechanisms of effect. METHODS: A continuous release pellet of IGF-1 was placed on one medial rectus muscle in two adult nonhuman primates (M1, M2) rendered exotropic by the alternating monocular occlusion method during the first months of life. Eye alignment and eye movements were recorded for 3 months, after which M1 was euthanized, and the lateral and medial rectus muscles were removed for morphometric analysis of fiber size, nerve, and neuromuscular density. RESULTS: Monkey 1 showed a 40% reduction in strabismus angle, a reduction of exotropia of approximately 11° to 14° after 3 months. Monkey 2 showed a 15% improvement, with a reduction of its exotropia by approximately 3°. The treated medial rectus muscle of M1 showed increased mean myofiber cross-sectional areas. Increases in myofiber size also were seen in the contralateral medial rectus and lateral rectus muscles. Similarly, nerve density increased in the contralateral medial rectus and yoked lateral rectus. CONCLUSIONS: This study demonstrates that in adult nonhuman primates with a sensory-induced exotropia in infancy, continuous IGF-1 treatment improves eye alignment, resulting in muscle fiber enlargement and altered innervational density that includes the untreated muscles. This supports the view that there is sufficient plasticity in the adult ocular motor system to allow continuous IGF-1 treatment over months to produce improvement in eye alignment in early-onset strabismus.

Vision and vigilance on the go.

Moving purposefully through the world requires the seamless coordination of a wide variety of sensory, motor, and motivation systems. Recent experiments suggest that mouse visual cortex may offer a particularly well suited forum for experimental investigation of this coordination.

Rapid shape detection signals in area V4.

Vision in foveate animals is an active process that requires rapid and constant decision-making. For example, when a new object appears in the visual field, we can quickly decide to inspect it by directing our eyes to the object's location. We studied the contribution of primate area V4 to these types of rapid foveation decisions. Animals performed a reaction time task that required them to report when any shape appeared within a peripherally-located noisy stimulus by making a saccade to the stimulus location. We found that about half of the randomly sampled V4 neurons not only rapidly and precisely represented the appearance of this shape, but they were also predictive of the animal's saccades. A neuron's ability to predict the animal's saccades was not related to the specificity with which the cell represented a single type of shape but rather to its ability to signal whether any shape was present. This relationship between sensory sensitivity and behavioral predictiveness was not due to global effects such as alertness, as it was equally likely to be observed for cells with increases and decreases in firing rate. Careful analysis of the timescales of reliability in these neurons implies that they reflect both feedforward and feedback shape detecting processes. In approximately 7% of our recorded sample, individual neurons were able to predict both the delay and precision of the animal's shape detection performance. This suggests that a subset of V4 neurons may have been directly and causally contributing to task performance and that area V4 likely plays a critical role in guiding rapid, form-based foveation decisions.

Featural and temporal attention selectively enhance task-appropriate representations in human primary visual cortex.

Our perceptions are often shaped by focusing our attention towards specific features or periods of time irrespective of location. Here we explore the physiological bases of these non-spatial forms of attention by imaging brain activity while subjects perform a challenging change-detection task. The task employs a continuously varying visual stimulus that, for any moment in time, selectively activates functionally distinct subpopulations of primary visual cortex (V1) neurons. When subjects are cued to the timing and nature of the change, the mapping of orientation preference across V1 systematically shifts towards the cued stimulus just prior to its appearance. A simple linear model can explain this shift: attentional changes are selectively targeted towards neural subpopulations, representing the attended feature at the times the feature was anticipated. Our results suggest that featural attention is mediated by a linear change in the responses of task-appropriate neurons across cortex during appropriate periods of time.

Attention directed by expectations enhances receptive fields in cortical area MT.

Expectations, especially those formed on the basis of extensive training, can substantially enhance visual performance. However, it is not clear that the physiological mechanisms underlying this enhancement are identical to those examined by experiments in which attention is directed by explicit instructions rather than strong expectations. To study the changes in visual representations associated with strong expectations, we trained animals to detect a brief motion pulse that was embedded in noise. Because the nature of the pulse and the statistics of its appearance were well known to the animals, they formed strong expectations which determined their behavioral performance. We used white-noise methods to infer the receptive field structure of single neurons in area MT while they were performing this task. Incorporating non-linearities, we compared receptive fields during periods of time when the animals were expecting the motion pulse with periods of time when they were not. We found receptive field changes consistent with an increased reliability in signaling pulse occurrence. Moreover, these changes were not consistent with a simple gain modulation. The results suggest that strong expectations can create very specific changes in the visual representations at a cellular level to enhance performance.

Attentional modulation of visual responses by flexible input gain.

Although it is clear that sensory responses in the cortex can be strongly modulated by stimuli outside of classical receptive fields as well as by extraretinal signals such as attention and anticipation, the exact rules governing the neuronal integration of sensory and behavioral signals remain unclear. For example, most experiments studying sensory interactions have not explored attention, while most studies of attention have relied on the responses to relatively limited sets of stimuli. However, a recent study of V4 responses, in which location, orientation, and spatial attention were systematically varied, suggests that attention can both facilitate and suppress specific sensory inputs to a neuron according to behavioral relevance. To explore the implications of such input gain, we modeled the effects of a center-surround organization of attentional modulation using existing receptive field models of sensory integration. The model is consistent with behavioral measurements of a suppressive effect that surrounds the facilitatory locus of spatial attention. When this center-surround modulation is incorporated into realistic models of sensory integration, it is able to explain seemingly disparate observations of attentional effects in the neurophysiological literature, including spatial shifts in receptive field position and the preferential modulation of low contrast stimuli. The model is also consistent with recent formulations of attention to features in which gain is variably applied among cells with different receptive field properties. Consistent with functional imaging results, the model predicts that spatial attention effects will vary between different visual areas and suggests that attention may act through a common mechanism of selective and flexible gain throughout the visual system.

Temporal precision of neuronal information in a rapid perceptual judgment.

In many situations, such as pedestrians crossing a busy street or prey evading predators, rapid decisions based on limited perceptual information are critical for survival. The brevity of these perceptual judgments constrains how neuronal signals are integrated or pooled over time because the underlying sequence of processes, from sensation to perceptual evaluation to motor planning and execution, all occur within several hundred milliseconds. Because most previous physiological studies of these processes have relied on tasks requiring considerably longer temporal integration, the neuronal basis of such rapid decisions remains largely unexplored. In this study, we examine the temporal precision of neuronal activity associated with a rapid perceptual judgment. We find that the activity of individual neurons over tens of milliseconds can reliably convey information about sensory events and was well correlated with the animals' judgments. There was a strong correlation between sensory reliability and the correlation with behavioral choice, suggesting that rapid decisions were preferentially based on the most reliable sensory signals. We also find that a simple model in which the responses of a small number of individual neurons (<5) are summed can completely explain behavioral performance. These results suggest that neuronal circuits are sufficiently precise to allow for cognitive decisions to be based on small numbers of action potentials from highly reliable neurons.

Receptive fields in human visual cortex mapped with surface electrodes.

Most of our understanding of the functional organization of human visual cortex comes from lesion and functional imaging studies and by extrapolation from results obtained by neuroanatomical and neurophysiological studies in nonhuman primates. Although some single-unit and field potential recordings have been made in human visual cortex, none has provided quantitative characterization of spatial receptive fields (RFs) of individual sites. Here we use subdural electrodes implanted for clinical purposes to quantitatively measure response properties in different regions of human visual cortex. We find significant differences in RF size, response latency, and response magnitude for sites in early visual areas, versus sites in later stages of both the dorsal and ventral streams. In addition, we use this technique to estimate the cortical magnification factor in early human visual cortex. The spatial and temporal resolution of cortical surface recordings suggest that this technique is well suited to examine further issues in visual processing in humans.

Attentional modulation in visual cortex depends on task timing.

Paying attention to a stimulus selectively increases the ability to process it. For example, when subjects attend to a specific region of a visual scene, their sensitivity to changes at that location increases. A large number of studies describe the behavioural consequences and neurophysiological correlates of attending to spatial locations. There has, in contrast, been little study of the allocation of attention over time. Because subjects can anticipate predictable events with great temporal precision, it seems probable that they might dynamically shift their attention when performing a familiar perceptual task whose constraints changed over time. We trained monkeys to respond to a stimulus change where the probability of occurrence changed over time. Recording from area V4 of the visual cortex in these animals, we found that the modulation of neuronal responses changed according to the probability of the change occurring at that instant. Thus, we show that the attentional modulation of sensory neurons reflects a subject's anticipation of the timing of behaviourally relevant events.

Physiological correlates of perceptual learning in monkey V1 and V2.

Performance in visual discrimination tasks improves with practice. Although the psychophysical parameters of these improvements have suggested the involvement of early areas in visual cortex, there has been little direct study of the physiological correlates of such perceptual learning at the level of individual neurons. To examine how neuronal response properties in the early visual system may change with practice, we trained monkeys for more than 6 mo in an orientation discrimination task in which behaviorally relevant stimuli were restricted to a particular retinal location and oriented around a specific orientation. During training the monkeys' discrimination thresholds gradually improved to much better than those of naive monkeys or humans. Although this improvement was specific to the trained orientation, it showed little retinotopic specificity. The receptive field properties of single neurons from regions representing the trained location and a location in the opposite visual hemifield were measured in V1 and V2. In most respects the receptive field properties in the representations of the trained and untrained regions were indistinguishable. However, in the regions of V1 and V2 representing the trained location, there were slightly fewer neurons whose optimal orientation was near the trained orientation. This resulted in a small but significant decrease in the V1 population response to the trained orientation at the trained location. Consequently, the observed neuronal populations did not exhibit any orientation-specific biases sufficient to explain the orientation specificity of the behavioral improvement. Pooling models suggest that the behavioral improvement was accomplished with a task-dependent and orientation-selective pooling of unaltered signals from early visual neurons. These data suggest that, even for training with stimuli suited to the selectivities found in early areas of visual cortex, behavioral improvements can occur in the absence of pronounced changes in the physiology of those areas.