Attention facilitates initiation of perceptual decision making: a combined psychophysical and electroencephalography study.

Humans can selectively process information and make decisions by directing their attention to desired locations in their daily lives. Numerous studies have shown that attention increases the rate of correct responses and shortens reaction time, and it has been hypothesized that this phenomenon is caused by an increase in sensitivity of the sensory signals to which attention is directed. The present study employed psychophysical methods and electroencephalography (EEG) to test the hypothesis that attention accelerates the onset of information accumulation. Participants were asked to discriminate the motion direction of one of two random dot kinematograms presented on the left and right sides of the visual field, one of which was cued by an arrow in 80% of the trials. The drift-diffusion model was applied to the percentage of correct responses and reaction times in the attended and unattended fields of view. Attention primarily increased sensory sensitivity and shortened the time unrelated to decision making. Next, we measured centroparietal positivity (CPP), an EEG measure associated with decision making, and found that CPP latency was shorter in attended trials than in unattended trials. These results suggest that attention not only increases sensory sensitivity but also accelerates the initiation of decision making.

Employment of time-varying sensory evidence to test the mechanisms underlying flexible decision-making.

To make flexible decisions in dynamic environments, the brain must integrate behaviorally relevant information while simultaneously discarding irrelevant information. This study aimed to investigate the mechanisms responsible for discarding irrelevant information during context-dependent decision-making. We trained two macaque monkeys to switch between direction and depth discrimination tasks in successive trials. During decision-making, the strength of the motion or depth signal changes transiently at various times, introducing a brief pulse. We assessed the effects of pulse on behavioral choices. Consistent with previous findings, early relevant pulses, such as motion pulses during direction discrimination, had a significantly larger effect compared to late pulses. Critically, the effects of irrelevant pulses, such as motion pulses during depth discrimination, exhibited an initial minimal effect, followed by an increase and subsequent decrease as a function of pulse timing. Gating mechanisms alone, aimed at discarding irrelevant information, did not account for the observed time course of pulse effects. Instead, the observed increase in the effects of irrelevant pulses with time suggested the involvement of a leaky integration mechanism. The results suggested that the brain controls the amount of disposal in accumulating sensory evidence during flexible decision-making.

Representation of Motion Direction in Visual Area MT Accounts for High Sensitivity to Centripetal Motion, Aligning with Efficient Coding of Retinal Motion Statistics.

The overrepresentation of centrifugal motion in the middle temporal visual area (area MT) has long been thought to provide an efficient coding strategy for optic flow processing. However, this overrepresentation compromises the detection of approaching objects, which is essential for survival. In the present study, we revisited this long-held notion by reanalyzing motion selectivity in area MT of three macaque monkeys (two males, one female) using random-dot stimuli instead of spot stimuli. We found no differences in the number of neurons tuned to centrifugal versus centripetal motion; however, centrifugally tuned neurons showed stronger tuning than centripetally tuned neurons. This was attributed to the heightened suppression of responses in centrifugal neurons to centripetal motion compared with that of centripetal neurons to centrifugal motion. Our modeling implies that this intensified suppression accounts for superior detection performance for weak centripetal motion stimuli. Moreover, through Fisher information analysis, we establish that the population sensitivity to motion direction in peripheral vision corresponds well with retinal motion statistics during forward locomotion. While these results challenge established concepts, considering the interplay of logarithmic Gaussian receptive fields and spot stimuli can shed light on the previously documented overrepresentation of centrifugal motion. Significantly, our findings reconcile a previously found discrepancy between MT activity and human behavior, highlighting the proficiency of peripheral MT neurons in encoding motion direction efficiently.SIGNIFICANCE STATEMENT The efficient coding hypothesis states that sensory neurons are tuned to specific, frequently experienced stimuli. Whereas previous work has found that neurons in the middle temporal (MT) area favor centrifugal motion, which results from forward locomotion, we show here that there is no such bias. Moreover, we found that the response of centrifugal neurons for centripetal motion was more suppressed than that of centripetal neurons for centrifugal motion. Combined with modeling, this provides a solution to a previously known discrepancy between reported centrifugal bias in MT and better detection of centripetal motion by human observers. Additionally, we show that population sensitivity in peripheral MT neurons conforms to an efficient code of retinal motion statistics during forward locomotion.

Prediction-Related Frontal-Temporal Network for Omission Mismatch Activity in the Macaque Monkey.

Sensory prediction is considered an important element of mismatch negativity (MMN) whose reduction is well known in patients with schizophrenia. Omission MMN is a variant of the MMN which is elicited by the absence of a tone previously sequentially presented. Omission MMN can eliminate the effects of sound differences in typical oddball paradigms and affords the opportunity to identify prediction-related signals in the brain. Auditory predictions are thought to reflect bottom-up and top-down processing within hierarchically organized auditory areas. However, the communications between the various subregions of the auditory cortex and the prefrontal cortex that generate and communicate sensory prediction-related signals remain poorly understood. To explore how the frontal and temporal cortices communicate for the generation and propagation of such signals, we investigated the response in the omission paradigm using electrocorticogram (ECoG) electrodes implanted in the temporal, lateral prefrontal, and orbitofrontal cortices of macaque monkeys. We recorded ECoG data from three monkeys during the omission paradigm and examined the functional connectivity between the temporal and frontal cortices by calculating phase-locking values (PLVs). This revealed that theta- (4-8 Hz), alpha- (8-12 Hz), and low-beta- (12-25 Hz) band synchronization increased at tone onset between the higher auditory cortex and the frontal pole where an early omission response was observed in the event-related potential (ERP). These synchronizations were absent when the tone was omitted. Conversely, low-beta-band (12-25 Hz) oscillation then became stronger for tone omission than for tone presentation approximately 200 ms after tone onset. The results suggest that auditory input is propagated to the frontal pole via the higher auditory cortex and that a reciprocal network may be involved in the generation of auditory prediction and prediction error. As impairments of prediction may underlie MMN reduction in patients with schizophrenia, an aberrant hierarchical temporal-frontal network might be related to this pathological condition.

Task-specific employment of sensory signals underlies rapid task switching.

Much of our flexible behavior is dependent on responding efficiently to relevant information while discarding irrelevant information. Little is known, however, about how neural pathways governing sensory-motor associations can rapidly switch to accomplish such flexibility. Here, we addressed this question by electrically microstimulating middle temporal (MT) neurons selective for both motion direction and binocular disparity in monkeys switching between direction and depth discrimination tasks. Surprisingly, we frequently found that the observed psychophysical bias precipitated by delivering microstimulation to neurons whose preferred direction and depth were related to opposite choices in the two tasks was substantially shifted toward a specific movement. Furthermore, these effects correlated with behavioral switching performance. Our findings suggest that the outputs of sensory signals are task specific and that irrelevant sensory-motor pathways are gated depending on task demand so as to accomplish rapid attentional switching.

Context-Dependent Accumulation of Sensory Evidence in the Parietal Cortex Underlies Flexible Task Switching.

Switching behavior based on multiple rules is a fundamental ability of flexible behavior. Although interactions among the frontal, parietal, and sensory cortices are necessary for such flexibility, little is known about the neural computations concerning context-dependent information readouts. Here, we provide evidence that neurons in the lateral intraparietal area (LIP) accumulate relevant information preferentially depending on context. We trained monkeys to switch between direction and depth discrimination tasks and analyzed the buildup activity in the LIP depending on task context. In accordance with behavior, the rate of buildup to identical visual stimuli differed between tasks and buildup was prominent only for the stimulus dimension relevant to the task. These results indicate that LIP neurons accumulate relevant information depending on context to decide flexibly where to move the eye, suggesting that flexibility is, at least partly, implemented in the form of temporal integration gain control. SIGNIFICANCE STATEMENT: Flexible behavior depending on context is a hallmark of human cognition. During flexible behavior, the frontal and parietal cortices have complex representations that hinder efforts to conceptualize their underlying computations. We now provide evidence that neurons in the lateral intraparietal area accumulate relevant information preferentially depending on context. We suggest that behavioral flexibility is implemented in the form of temporal integration gain control in the parietal cortex.

Visual impairment by surrounding noise is due to interactions among stimuli in the higher-order visual cortex.

Observers have difficulty identifying a target in their peripheral vision in the presence of surrounding stimuli. Although hypotheses addressing this phenomenon have been proposed, such as the integration of stimuli and surround suppression in the higher-order visual cortex, no direct comparisons of the psychophysical and neuronal sensitivities have been performed. Here we measured the performance of monkeys with a variant of the direction discrimination task using a center/surround bipartite random-dot stimulus while simultaneously recording from isolated neurons from the middle temporal visual area (MT). The psychophysical threshold increased with the addition of a task-irrelevant noise annulus that surrounded the task-relevant motion stimuli. The neuronal threshold of MT neurons also increased at a spatial scale similar to the psychophysical threshold. This suggests that the impaired ability in our task resulted from impairment in the MT area. Importantly, reduced neuronal performance was due to both a reduced response to preferred motion and an enhanced response to nonpreferred motion. These observations suggest that impairment caused by surrounding noise results from interactions between stimuli and noise and not from a reduction in the response of visual neurons.

Responses to random dot motion reveal prevalence of pattern-motion selectivity in area MT.

How the visual system reconstructs global patterns of motion from components is an important issue in vision. Conventional studies using plaids have shown that approximately one-third of neurons in cortical area MT respond to one-dimensional (1D) components of a moving pattern (component cells), whereas another third responds to the global two-dimensional (2D) motion of a pattern (pattern cells). Conversely, studies using spots of light or random dots that contain multiple orientations have seldom reported directional tuning that is consistent with 1D motion preference. To bridge the gap between these studies, we recorded from isolated neurons in macaque area MT and measured tuning for velocity (direction and speed) using random dot stimuli. We used the "intersection of constraints" principle to classify our population into pattern-direction-selective (PDS) neurons and component-direction-selective (CDS) neurons. We found a larger proportion of PDS cells (68%) and a smaller proportion of CDS cells (8%) compared with prior studies using plaids. We further compared velocity tuning, measured using random dot stimuli, with direction tuning, measured using plaids. Although there was a correlation between the degree of preference for 2D over 1D motion of the two measurements, tuning seemed to prefer 2D motion using random dot stimuli. Modeling analyses suggest that integration across orientations contributes to the 2D motion preference of both dots and plaids, but opponent inhibition mainly contributes to the 2D motion preference of plaids. We conclude that MT neurons become more capable of identifying a particular 2D velocity when stimuli contain multiple orientations.

Neuronal mechanisms of visual perceptual learning.

Numerous psychophysical studies have described perceptual learning as long-lasting improvements in perceptual discrimination and detection capabilities following practice. Where and how long-term plastic changes occur in the brain is central to understanding the neural basis of perceptual learning. Here, neurophysiological research using non-human primates is reviewed to address the neural mechanisms underlying visual perceptual learning. Previous studies have shown that training either has no effect on or only weakly alters the sensitivity of neurons in early visual areas, but more recent evidence indicates that training can cause long-term changes in how sensory signals are read out in the later stages of decision making. These results are discussed in the context of learning specificity, which has been crucial in interpreting the mechanisms underlying perceptual learning. The possible mechanisms that support learning-related plasticity are also discussed.

Change in choice-related response modulation in area MT during learning of a depth-discrimination task is consistent with task learning.

What are the neural mechanisms underlying improvement in perceptual performance due to learning? A recent study using motion-direction discrimination suggested that perceptual learning is due to improvements in the "readout" of sensory signals in sensory-motor cortex and not to improvements in neural sensitivity of the sensory cortex. To test the generality of this hypothesis, we examined this in a similar but different task. We recorded from isolated neurons in the middle temporal (MT) area while monkeys were trained in a depth-discrimination task. Consistent with earlier reports using direction discrimination, we found no long-term improvement in MT neuron sensitivity to depth, although monkey performance improved over months with extensive training, even when taking out the effect of behavioral biases. We further addressed improvement in the readout of sensory signals by focusing on choice-related response modulation [choice probability (CP)]. CP increased with training, suggesting an improvement in the readout of sensory signals from MT. CP, however, correlated more strongly with lapse rate than psychophysical threshold, suggesting that changes in readout may be restricted to early phases of learning. To test how behavioral learning, as well as the magnitude of CP, transferred across visual fields, we measured CP variation in one hemifield after training monkeys on the depth-discrimination task in the opposite hemifield. CP was large from the beginning of training in the untrained hemifield, even though a small but significant improvement in sensitivity was observed behaviorally. Overall, our findings are consistent with the idea that increases in CP reflect task learning.

Reduction in receptive field size of macaque MT neurons in the presence of visual noise.

The visual system faces a trade-off between increased spatial integration of disparate local signals and improved spatial resolution to filter out irrelevant noise. Increased spatial integration is beneficial when signals are weak, whereas increased spatial resolution is particularly beneficial when focusing on a small object in a cluttered natural scene. The receptive field (RF) size of visual cortical neurons can be modulated depending on various factors such as sensory context, allowing adaptive integration of sensory signals. In this study, we explored the spatial integration properties of neurons in macaque middle temporal visual area (MT). We hypothesized that spatial resolution would increase when high-contrast noise was presented simultaneously with a visual stimulus, enabling focus on a small object in a cluttered scene. To test this hypothesis, we mapped the RFs of MT neurons of two fixating monkeys in a 5 × 5 grid manner using a small patch of random-dot motion. To examine the effects of noise on RF profile, a dynamic noise (0% coherence dots) of varying diameter was concurrently presented at the RF center. We found that RF size decreased when noise diameter increased. Analyses based on the response normalization model and area summation provided evidence for the potential contribution of spatial summation properties within the RF and surround suppression to the apparent contraction of RF size. Our results suggest that MT neurons integrate smaller regions of motion signals when signals are embedded in noise, an efficient strategy to filter out surrounding noise.

The spatial profile of macaque MT neurons is consistent with Gaussian sampling of logarithmically coordinated visual representation.

Neurons in extrastriate visual areas have large receptive fields (RFs) compared with those in primary visual cortex (V1), suggesting extensive spatial integration. To examine the spatial integration of neurons in area MT, we modeled the RFs of MT neurons based on a symmetrical (Gaussian) integration of V1 outputs and tested the model using single-unit recording in two fixating macaque monkeys. Because visual representation in V1 is logarithmically compressed along eccentricity, the resulting RF model is log-Gaussian along the radial axis in polar coordinates. To test the log-Gaussian model, the RF of each neuron was mapped on a 5 x 5 grid using a small patch of random dots drifting at the preferred velocity of the neuron. The majority of MT neurons had RFs with a steeper slope near the fovea and a shallower slope away from the fovea. Among various two-dimensional Gaussian models fitted to the RFs, the log-Gaussian model provided the best description. The fitted parameters revealed that the range of sampling by MT neurons has no systematic relationship with eccentricities, consistent with a recent study for V4 neurons. Our results suggest that MT neurons integrate inputs from constant-sized patches of V1 cortex.

Spatial frequency integration for binocular correspondence in macaque area V4.

Neurons in the primary visual cortex (V1) detect binocular disparity by computing the local disparity energy of stereo images. The representation of binocular disparity in V1 contradicts the global correspondence when the image is binocularly anticorrelated. To solve the stereo correspondence problem, this rudimentary representation of stereoscopic depth needs to be further processed in the extrastriate cortex. Integrating signals over multiple spatial frequency channels is one possible mechanism supported by theoretical and psychophysical studies. We examined selectivities of single V4 neurons for both binocular disparity and spatial frequency in two awake, fixating monkeys. Disparity tuning was examined with a binocularly correlated random-dot stereogram (RDS) as well as its anticorrelated counterpart, whereas spatial frequency tuning was examined with a sine wave grating or a narrowband noise. Neurons with broader spatial frequency tuning exhibited more attenuated disparity tuning for the anticorrelated RDS. Additional rectification at the output of the energy model does not likely account for this attenuation because the degree of attenuation does not differ among the various types of disparity-tuned neurons. The results suggest that disparity energy signals are integrated across spatial frequency channels for generating a representation of stereoscopic depth in V4.