scholarly journals Neuronal correlates of attentional selectivity and intensity in visual area V4 are invariant of motivational context

2021 ◽  
Author(s):  
Supriya Ghosh ◽  
John H. R. Maunsell

Flexibly switching attentional strategies is crucial for adaptive behavior in changing environments. Depending on the context, task demand employs different degrees of the two fundamental components of attention- attentional selectivity (preferentially attending to one location in visual space) and effort (the total non-selective intensity of attention). Neuronal responses in the visual cortex that show modulation with changes in either selective attention or effort are reported to partially represent motivational aspect of the task context. The relative contributions and interactions of these two components of attention to modulate neuronal signals and their sensitivity to distinct motivational drives are poorly understood. To address this question, we independently controlled monkeys' spatially selective attention and non-selective attentional intensity in the same experimental session during a novel visual orientation change detection task. Attention was controlled either by adjusting the relative difficulty of the orientation changes at the two locations or by the reward associated with stimuli at two locations while simultaneously recording spikes from populations of neurons in area V4. We found that V4 neurons are robustly modulated by either selective attention or attentional intensity. Notably, as attentional selectivity for a neuron's receptive field location decreased, its responses became weaker, despite an increase in the animal's overall attentional intensity. This strong interaction between attentional selectivity and intensity could be identified in single trial spike trains. A simple divisive normalization of spatially distributed attention performances can explain the interaction between attention components well at the single neuron level. The effects of attentional selectivity and attentional intensity on neuronal responses were the same regardless of whether the changes were motivated by reward or task difficulty. These results provide a detailed cellular-level mechanism of how fundamental components of attention integrate and affect sensory processing in varying motivational and stimulus contexts.

2019 ◽  
Vol 121 (3) ◽  
pp. 1059-1077 ◽  
Author(s):  
Dina V. Popovkina ◽  
Wyeth Bair ◽  
Anitha Pasupathy

Visual area V4 is an important midlevel cortical processing stage that subserves object recognition in primates. Studies investigating shape coding in V4 have largely probed neuronal responses with filled shapes, i.e., shapes defined by both a boundary and an interior fill. As a result, we do not know whether form-selective V4 responses are dictated by boundary features alone or if interior fill is also important. We studied 43 V4 neurons in two male macaque monkeys ( Macaca mulatta) with a set of 362 filled shapes and their corresponding outlines to determine how interior fill modulates neuronal responses in shape-selective neurons. Only a minority of neurons exhibited similar response strength and shape preferences for filled and outline stimuli. A majority responded preferentially to one stimulus category (either filled or outline shapes) and poorly to the other. Our findings are inconsistent with predictions of the hierarchical-max (HMax) V4 model that builds form selectivity from oriented boundary features and takes little account of attributes related to object surface, such as the phase of the boundary edge. We modified the V4 HMax model to include sensitivity to interior fill by either removing phase-pooling or introducing unoriented units at the V1 level; both modifications better explained our data without increasing the number of free parameters. Overall, our results suggest that boundary orientation and interior surface information are both maintained until at least the midlevel visual representation, consistent with the idea that object fill is important for recognition and perception in natural vision. NEW & NOTEWORTHY The shape of an object’s boundary is critical for identification; consistent with this idea, models of object recognition predict that filled and outline versions of a shape are encoded similarly. We report that many neurons in a midlevel visual cortical area respond differently to filled and outline shapes and modify a biologically plausible model to account for our data. Our results suggest that representations of boundary shape and surface fill are interrelated in visual cortex.


2015 ◽  
Author(s):  
Iris Grothe ◽  
David Rotermund ◽  
Simon D. Neitzel ◽  
Sunita Mandon ◽  
Udo A. Ernst ◽  
...  

Selective attention causes visual cortical neurons to act as if only one of multiple stimuli are within their receptive fields. This suggests that attention employs a, yet unknown, neuronal gating mechanism for transmitting only the information that is relevant for the current behavioral context. We introduce an experimental paradigm to causally investigate this putative gating and the mechanism underlying selective attention by determining the signal availability of two time-varying stimuli in local field potentials of V4 neurons. We find transmission of the low frequency (<20Hz) components only from the attended visual input signal and that the higher frequencies from both stimuli are attenuated. A minimal model implementing routing by synchrony replicates the attentional gating effect and explains the spectral transfer characteristics of the signals. It supports the proposal that selective gamma-band synchrony subserves signal routing in cortex and further substantiates our experimental finding that attention selectively gates signals already at the level of afferent synaptic input.


eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Bram-Ernst Verhoef ◽  
John HR Maunsell

Shifting attention among visual stimuli at different locations modulates neuronal responses in heterogeneous ways, depending on where those stimuli lie within the receptive fields of neurons. Yet how attention interacts with the receptive-field structure of cortical neurons remains unclear. We measured neuronal responses in area V4 while monkeys shifted their attention among stimuli placed in different locations within and around neuronal receptive fields. We found that attention interacts uniformly with the spatially-varying excitation and suppression associated with the receptive field. This interaction explained the large variability in attention modulation across neurons, and a non-additive relationship among stimulus selectivity, stimulus-induced suppression and attention modulation that has not been previously described. A spatially-tuned normalization model precisely accounted for all observed attention modulations and for the spatial summation properties of neurons. These results provide a unified account of spatial summation and attention-related modulation across both the classical receptive field and the surround.


2010 ◽  
Vol 103 (5) ◽  
pp. 2433-2445 ◽  
Author(s):  
Tadashi Ogawa ◽  
Hidehiko Komatsu

Previous studies have suggested that spontaneous fluctuations in neuronal activity reflect intrinsic functional brain architecture. Inspired by these findings, we analyzed baseline neuronal activity in the monkey frontal eye field (FEF; a visuomotor area) and area V4 (a visual area) during the fixation period of a cognitive behavioral task in the absence of any task-specific stimuli or behaviors. Specifically, we examined the temporal storage capacity of the instantaneous discharge rate in FEF and V4 neurons by calculating the correlation of the spike count in a bin with that in another bin during the baseline activity of a trial. We found that most FEF neurons fired significantly more (or less) in one bin if they fired more (or less) in another bin within a trial, even when these two time bins were separated by hundreds of milliseconds. By contrast, similar long time-lag correlations were observed in only a small fraction of V4 neurons, indicating that temporal correlations were considerably stronger in FEF compared with those in V4 neurons. Additional analyses revealed that the findings were not attributable to other task-related variables or ongoing behavioral performance, suggesting that the differences in temporal correlation strength reflect differences in intrinsic structural and functional architecture between visual and visuomotor areas. Thus FEF neurons probably play a greater role than V4 neurons in neural circuits responsible for temporal storage in activity.


2004 ◽  
Vol 92 (1) ◽  
pp. 622-629 ◽  
Author(s):  
Mark A. Pinsk ◽  
Glen M. Doniger ◽  
Sabine Kastner

Selective attention operates in visual cortex by facilitating processing of selected stimuli and by filtering out unwanted information from nearby distracters over circumscribed regions of visual space. The neural representation of unattended stimuli outside this focus of attention is less well understood. We studied the neural fate of unattended stimuli using functional magnetic resonance imaging by dissociating the activity evoked by attended (target) stimuli presented to the periphery of a visual hemifield and unattended (distracter) stimuli presented simultaneously to a corresponding location of the contralateral hemifield. Subjects covertly directed attention to a series of target stimuli and performed either a low or a high attentional-load search task on a stream of otherwise identical stimuli. With this task, target-search-related activity increased with increasing attentional load, whereas distracter-related activity decreased with increasing load in areas V4 and TEO but not in early areas V1 and V2. This finding presents evidence for a load-dependent push-pull mechanism of selective attention that operates over large portions of the visual field at intermediate processing stages. This mechanism appeared to be controlled by a distributed frontoparietal network of brain areas that reflected processes related to target selection during spatially directed attention.


1998 ◽  
Vol 80 (4) ◽  
pp. 1800-1815 ◽  
Author(s):  
Christopher L. Passaglia ◽  
Frederick A. Dodge ◽  
Robert B. Barlow

Passaglia, Christopher L., Frederick A. Dodge, and Robert B. Barlow. Cell-based model of the Limulus lateral eye. J. Neurophysiol. 80: 1800–1815, 1998. We present a cell-based model of the Limulus lateral eye that computes the eye's input to the brain in response to any specified scene. Based on the results of extensive physiological studies, the model simulates the optical sampling of visual space by the array of retinal receptors (ommatidia), the transduction of light into receptor potentials, the integration of excitatory and inhibitory signals into generator potentials, and the conversion of generator potentials into trains of optic nerve impulses. By simulating these processes at the cellular level, model ommatidia can reproduce response variability resulting from noise inherent in the stimulus and the eye itself, and they can adapt to changes in light intensity over a wide operating range. Programmed with these realistic properties, the model eye computes the simultaneous activity of its ensemble of optic nerve fibers, allowing us to explore the retinal code that mediates the visually guided behavior of the animal in its natural habitat. We assess the accuracy of model predictions by comparing the response recorded from a single optic nerve fiber to that computed by the model for the corresponding receptor. Correlation coefficients between recorded and computed responses were typically >95% under laboratory conditions. Parametric analyses of the model together with optic nerve recordings show that animal-to-animal variation in the optical and neural properties of the eye do not alter significantly its response to objects having the size and speed of horseshoe crabs. The eye appears robustly designed for encoding behaviorally important visual stimuli. Simulations with the cell-based model provide insights about the design of the Limulus eye and its encoding of the animal's visual world.


2010 ◽  
Vol 103 (3) ◽  
pp. 1171-1178 ◽  
Author(s):  
Nicholas A. Steinmetz ◽  
Tirin Moore

The visually driven responses of macaque area V4 neurons are modulated during the preparation of saccadic eye movements, but the relationship between presaccadic modulation in area V4 and saccade preparation is poorly understood. Recent neurophysiological studies suggest that the variability across trials of spiking responses provides a more reliable signature of motor preparation than mean firing rate across trials. We compared the dynamics of the response rate and the variability in the rate across trials for area V4 neurons during the preparation of visually guided saccades. As in previous reports, we found that the mean firing rate of V4 neurons was enhanced when saccades were prepared to stimuli within a neuron's receptive field (RF) in comparison with saccades to a non-RF location. Further, we found robust decreases in response variability prior to saccades and found that these decreases predicted saccadic reaction times for saccades both to RF and non-RF stimuli. Importantly, response variability predicted reaction time whether or not there were any accompanying changes in mean firing rate. In addition to predicting saccade direction, the mean firing rate could also predict reaction time, but only for saccades directed to the RF stimuli. These results demonstrate that response variability of area V4 neurons, like mean response rate, provides a signature of saccade preparation. However, the two signatures reflect complementary aspects of that preparation.


2005 ◽  
Vol 94 (4) ◽  
pp. 2726-2737 ◽  
Author(s):  
David A. Hinkle ◽  
Charles E. Connor

We performed a quantitative characterization of binocular disparity-tuning functions in the ventral (object-processing) pathway of the macaque visual cortex. We measured responses of 452 area V4 neurons to stimuli with disparities ranging from −1.0 to +1.0°. Asymmetric Gaussian functions fit the raw data best (median R = 0.90), capturing both the modal components (local peaks in the −1.0 to +1.0° range) and the monotonic components (linear or sigmoidal dependency on disparity) of the tuning patterns. Values derived from the asymmetric Gaussian fits were used to characterize neurons on a modal × monotonic tuning domain. Points along the modal tuning axis correspond to classic tuned excitatory and inhibitory patterns; points along the monotonic axis correspond to classic near and far patterns. The distribution on this domain was continuous, with the majority of neurons exhibiting a mixed modal/monotonic tuning pattern. The distribution in the modal dimension was shifted toward excitatory patterns, consistent with previous results in other areas. The distribution in the monotonic dimension was shifted toward tuning for crossed disparities (corresponding to stimuli nearer than the fixation plane). This could reflect a perceptual emphasis on objects or object parts closer to the observer. We also found that disparity-tuning strength was positively correlated with orientation-tuning strength and color-tuning strength, and negatively correlated with receptive field eccentricity.


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