Geoffrey M. Ghose

Rhythms at a population level are a defining characteristic of both normal and pathological cortical activities, but it is unclear how such rhythms interact with the activity of specific neurons to impact task performance on a trial-by-trial basis. We address this by employing a challenging visual detection task in which male rhesus macaques must signal the presentation of a shape embedded in a noisy background. We analyzed the rhythmic activity in the local field potential (LFP) and single neuron activity in area V4, a brain area strongly implicated in shape perception, prior to such presentations and focused on two different frequency ranges: alpha/beta (10–30 Hz), in which coherence was particularly strong and spatially extensive, and gamma (50–70 Hz), which has traditionally been strongly associated with single unit activity. We find that within sessions, there were periods of time during which successful detection was associated with the absence of rhythmic activity prior to shape presentation in either frequency range. During these periods, rhythmic quiescence prior to shape presentation could predict whether the shape would be detected by the animal with high accuracy. Importantly, for both frequency ranges, the individual neurons carrying the most relevant information with regard to the task had the weakest coupling to LFP rhythms. These results are consistent with spatially distributed rhythmic activity acting as a source of decision noise in the context of rapid visual detection by reducing the moment-to-moment reliability of task-relevant information carried by individual neurons.

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.

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 close 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, while the probability of target occurrence varies with sound frequency. Contrary to previous fMRI studies, we show that selective attention reduces responses to the attended frequencies in those neuronal populations preferring the attended frequency. Through population receptive field (pRF) mapping, we furthermore show that these response reductions are at least partially driven by frequency-induced pRF narrowing. 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, task, and auditory processing stage.

Attention is a fundamental cognitive process that selectively filters sensory information to enable efficient and task-specific behavior. By definition it must be both robust and flexible across different tasks, but the neural mechanisms allowing such flexibility remain poorly understood. Recent theories have proposed that attention is tied to object-based processing and only indirectly modulates lower level sensory representations. However, supportive experiments typically use simple objects and explicit instructions which may not reflect natural task statistics or sensory environments. An alternative is that attentional modulations are selectively targeted to task-appropriate neural populations even when such representations only exist in early sensory areas. To differentiate these models, we trained monkeys to detect small changes, on the order of the size of a primary visual cortex receptive field, within a complex stimulus array. Importantly, the probability of changes varied by location in a fixed pattern. We then measured activity across primary visual cortex during task performance using intrinsic flavoprotein autofluorescence imaging. We found that behavioral performance was better at higher probability locations, and that the spatial pattern of activation within primary visual cortex largely explained spatial variations in behavior. Moreover, the precision of attentional modulations, measured physiologically and behaviorally, matched the precision of the retinotopic map in V1. These results show that attentional modulations may reach the earliest levels of cortical processing with a resolution that matches the local neuronal population and support the notion that experience-based modulations can be targeted to specific task-appropriate cortical populations with sub-millimeter precision.

The brain is organized into distinct, flexible networks. Within these networks, cognitive variables such as attention can modulate sensory representations in accordance with moment-to-moment behavioral requirements. These modulations can be studied by varying task demands; however, the tasks employed are often incongruent with the postulated functions of a sensory system, limiting the characterization of the system in relation to natural behaviors. Here we combine domain-specific task manipulations and ultra-high field fMRI to study the nature of top-down modulations. We exploited faces, a visual category underpinned by a complex cortical network, and instructed participants to perform either a stimulus-relevant/domain-specific or a stimulus-irrelevant task in the scanner. We found that 1. perceptual ambiguity (i.e. difficulty of achieving a stable percept) is encoded in top-down modulations from higher-level cortices; 2. the right inferior-temporal lobe is active under challenging conditions and uniquely encodes trial-by-trial variability in face perception.

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 (similar to 70 ms) transients of coherent motion within similar to 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.

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.

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. 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. 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. 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.

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.