scholarly journals Rhythmic neural spiking and attentional sampling arising from cortical receptive field interactions

2018 ◽  
Author(s):  
Ricardo Kienitz ◽  
Joscha T. Schmiedt ◽  
Katharine A. Shapcott ◽  
Kleopatra Kouroupaki ◽  
Richard C. Saunders ◽  
...  

SummaryGrowing evidence suggests that distributed spatial attention may invoke theta (3-9 Hz) rhythmic sampling processes. The neuronal basis of such attentional sampling is however not fully understood. Here we show using array recordings in visual cortical area V4 of two awake macaques that presenting separate visual stimuli to the excitatory center and suppressive surround of neuronal receptive fields elicits rhythmic multi-unit activity (MUA) at 3-6 Hz. This neuronal rhythm did not depend on small fixational eye movements. In the context of a distributed spatial attention task, during which the monkeys detected a spatially and temporally uncertain target, reaction times (RT) exhibited similar rhythmic fluctuations. RTs were fast or slow depending on the target occurrence during high or low MUA, resulting in rhythmic MUA-RT cross-correlations at at theta frequencies. These findings suggest that theta-rhythmic neuronal activity arises from competitive receptive field interactions and that this rhythm may subserve attentional sampling.HighlightsCenter-surround interactions induce theta-rhythmic MUA of visual cortex neuronsThe MUA rhythm does not depend on small fixational eye movementsReaction time fluctuations lock to the neuronal rhythm under distributed attention

2007 ◽  
Vol 97 (5) ◽  
pp. 3439-3448 ◽  
Author(s):  
Yamei Tang ◽  
Alan Saul ◽  
Moshe Gur ◽  
Stephanie Goei ◽  
Elsie Wong ◽  
...  

Studies of visual function in behaving subjects require that stimuli be positioned reliably on the retina in the presence of eye movements. Fixational eye movements scatter stimuli about the retina, inflating estimates of receptive field dimensions, reducing estimates of peak responses, and blurring maps of receptive field subregions. Scleral search coils are frequently used to measure eye position, but their utility for correcting the effects of fixational eye movements on receptive field maps has been questioned. Using eye coils sutured to the sclera and preamplifiers configured to minimize cable artifacts, we reexamined this issue in two rhesus monkeys. During repeated fixation trials, the eye position signal was used to adjust the stimulus position, compensating for eye movements and correcting the stimulus position to place it at the desired location on the retina. Estimates of response magnitudes and receptive field characteristics in V1 and in LGN were obtained in both compensated and uncompensated conditions. Receptive fields were narrower, with steeper borders, and response amplitudes were higher when eye movement compensation was used. In sum, compensating for eye movements facilitated more precise definition of the receptive field. We also monitored horizontal vergence over long sequences of fixation trials and found the variability to be low, as expected for this precise behavior. Our results imply that eye coil signals can be highly accurate and useful for optimizing visual physiology when rigorous precautions are observed.


2003 ◽  
Vol 90 (2) ◽  
pp. 946-960 ◽  
Author(s):  
Jenny C. A. Read ◽  
Bruce G. Cumming

One difficulty with measuring receptive fields in the awake monkey is that even well-trained animals make small eye movements during fixation. These complicate the measurement of receptive fields by blurring out the region where a response is observed, causing underestimates of the ability of individual neurons to signal changes in stimulus position. In simple cells, this blurring may severely disrupt estimates of receptive field structure. An accurate measurement of eye movements would allow correction of this blurring. Scleral search coils have been used to provide such measurements, although little is known about their accuracy. We have devised a range of approaches to address this issue: implanting two coils into a single eye, exploiting the small size of V1 receptive fields and developing maximum-likelihood fitting techniques to extract receptive field parameters in the presence of eye movements. All our investigations lead to the same conclusion: our scleral search coils (which were not sutured to the globe) are subject to an error of approximately the same magnitude as the small eye movements which occur during fixation: SD ∼ 0.1°. This error is large enough to explain the SD of measured vergence in the absence of any real changes in vergence state. This, and a variety of other arguments, indicate that the real variation in vergence is much smaller than coil measurements suggest. These results suggest that monkeys, like humans, maintain very stable vergence. The error has a slower time course than fixational eye movements so that search coils report the difference in eye position between two consecutive trials more accurately than the eye position itself on either trial. Receptive field estimates are unlikely to be improved by assuming the coil record is veridical and correcting for eye position accordingly. However, receptive field parameters can reliably be determined by a fitting technique that allows for eye movements. It is possible that suturing coils to the globe reduces the artifacts, but no method has been available to demonstrate this. These receptive field measurements provide a general means by which the reliability of eye-position measurements can be assessed.


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.


eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Tao Yao ◽  
Madhura Ketkar ◽  
Stefan Treue ◽  
B Suresh Krishna

Maintaining attention at a task-relevant spatial location while making eye-movements necessitates a rapid, saccade-synchronized shift of attentional modulation from the neuronal population representing the task-relevant location before the saccade to the one representing it after the saccade. Currently, the precise time at which spatial attention becomes fully allocated to the task-relevant location after the saccade remains unclear. Using a fine-grained temporal analysis of human peri-saccadic detection performance in an attention task, we show that spatial attention is fully available at the task-relevant location within 30 milliseconds after the saccade. Subjects tracked the attentional target veridically throughout our task: i.e. they almost never responded to non-target stimuli. Spatial attention and saccadic processing therefore co-ordinate well to ensure that relevant locations are attentionally enhanced soon after the beginning of each eye fixation.


2007 ◽  
Vol 24 (2) ◽  
pp. 217-230 ◽  
Author(s):  
GAËLLE DESBORDES ◽  
MICHELE RUCCI

During visual fixation, small eye movements keep the retinal image continuously in motion. It is known that neurons in the visual system are sensitive to the spatiotemporal modulations of luminance resulting from this motion. In this study, we examined the influence of fixational eye movements on the statistics of neural activity in the macaque's retina during the brief intersaccadic periods of natural visual fixation. The responses of parvocellular (P) and magnocellular (M) ganglion cells in different regions of the visual field were modeled while their receptive fields scanned natural images following recorded traces of eye movements. Immediately after the onset of fixation, wide ensembles of coactive ganglion cells extended over several degrees of visual angle, both in the central and peripheral regions of the visual field. Following this initial pattern of activity, the covariance between the responses of pairs of P and M cells and the correlation between the responses of pairs of M cells dropped drastically during the course of fixation. Cell responses were completely uncorrelated by the end of a typical 300-ms fixation. This dynamic spatial decorrelation of retinal activity is a robust phenomenon independent of the specifics of the model. We show that it originates from the interaction of three factors: the statistics of natural scenes, the small amplitudes of fixational eye movements, and the temporal sensitivities of ganglion cells. These results support the hypothesis that fixational eye movements, by shaping the statistics of retinal activity, are an integral component of early visual representations.


2021 ◽  
Author(s):  
Jacob L Yates ◽  
Shanna H Coop ◽  
Gabriel H Sarch ◽  
Ruei-Jr Wu ◽  
Daniel A Butts ◽  
...  

Virtually all vision studies use a fixation point to stabilize gaze, rendering stimuli on video screens fixed to retinal coordinates. This approach requires trained subjects, is limited by the accuracy of fixational eye movements, and ignores the role of eye movements in shaping visual input. To overcome these limitations, we developed a suite of hardware and software tools to study vision during natural behavior in untrained subjects. We show this approach recovers receptive fields and tuning properties of visual neurons from multiple cortical areas of marmoset monkeys. Combined with high-precision eye-tracking, it achieves sufficient resolution to recover the receptive fields of foveal V1 neurons. These findings demonstrate the power of this approach for characterizing neural response while simultaneously studying the dynamics of natural behavior.


2021 ◽  
Author(s):  
Noam Tal-Perry ◽  
Shlomit Yuval-Greenberg

Temporal expectation is the ability to construct predictions regarding the timing of events, based on previously-experienced temporal regularities of different types. For example, cue-based expectations are constructed when a cue validly indicates when a target is expected to occur. However, in the absence of such cues, expectations can be constructed based on contextual temporal information, including the event's hazard-rate function - its moment-by-moment conditional probability that changes over time; and prior experiences, which provide probabilistic information regarding the event's predicted timing (sequential effects). It was previously suggested that cue-based temporal expectation is exerted via synchronization of spatially-specific neural activity at a target's predictable time, within receptive fields corresponding to the target's expected location. Here, we tested if the same theoretical model holds for contextual temporal effects. Participants (n = 40) performed a speeded spatial-cueing detection task, with two-thirds valid spatial cues. The target's hazard-rate function was modulated by varying the foreperiod - the interval between the spatial cue and the target - among trials, and was manipulated between groups by changing the interval distribution. Reaction times were analyzed using both frequentist and Bayesian generalized linear mixed models, accounting for hazard and sequential effects. Results showed that the effects of contextual temporal structures on reaction times were independent of spatial attention. This suggests that the spatiotemporal mechanisms, thought to account for cue-based expectation, cannot explain other sources of temporal expectations. We conclude that expectations based on contextual structures have different characteristics than cue-based temporal expectation, suggesting reliance on distinct neural mechanisms.


1977 ◽  
Vol 40 (1) ◽  
pp. 156-173 ◽  
Author(s):  
M. Schlag-Rey ◽  
J. Schlag

1. Visual responses and eye movement-related activities were studied in single neurons of the thalamic internal medullary lamina (IML) of alert cats. The animals faced a tangent screen on which stationary or moving spots of light were presented. Of 95 units, 26% discharged in relation to photic stimuli but not eye movement, 6% in relation to eye movement but not photic stimuli, and 68% in relation to both. These units were intermixed in the same region. 2. Visual responses varied from transient to sustained. IML units were not found particularly sensitive to stimulus movement when the eyes were fixed. Strong and consistent responses could be elicited by extremely dim and weakly contrasted stationary stimuli (e.g.) 3.4 mcd/m2, 2.6% of illumination background) binocularly viewed. Receptive fields (from 250 to 800 deg2) were determined, in absence of eye movements, by computing the position of effective stimuli relative to the point of fixation of the gaze. An area of greatest responsiveness in the receptive field of most units could be detected on the basis of either higher probability of response, minimum latency, greater number of spikes in initial transient burst, or stronger sustained activity. Whole fields or their areas of greatest responsiveness were located on the side toward which saccades were accompanied by increased firing of the unit. 3. On trials in which a delay occurred between stimulus presentation and the cat's targeting saccade, the majority of the units studied changed their activity twice: after the stimulus and before the eye movement. In 16 units, the presaccadic activation occurred only with targeting, not with spontaneous saccades. 4. These results suggest that cells in the IML region of the cat play a significant role in the control of visually elicited eye movements. The resemblance of these cells to the monkey's tectual cells is discussed and hypotheses are proposed a) to relate the receptive field characteristics to the targeting operation, and b) to account for the double activation--sensory and motor--of many IML cells.


2008 ◽  
Vol 99 (5) ◽  
pp. 2158-2182 ◽  
Author(s):  
Calin I. Buia ◽  
Paul H. Tiesinga

Receptive fields of neurons in cortical area V4 are large enough to fit multiple stimuli, making V4 the ideal place to study the effects of selective attention at the single-neuron level. Experiments have revealed evidence for stimulus competition and have characterized the effect thereon of spatial and feature-based attention. We developed a biophysical model with spiking neurons and conductance-based synapses. To account for the comprehensive set of experimental results, it was necessary to include in the model, in addition to regular spiking excitatory (E) cells, two types of interneurons: feedforward interneurons (FFI) and top-down interneurons (TDI). Feature-based attention was mediated by a projection of the TDI to the FFI, stimulus competition was mediated by a cross-columnar excitatory connection to the FFI, whereas spatial attention was mediated by an increase in activity of the feedforward inputs from cortical area V2. The model predicts that spatial attention increases the FFI firing rate, whereas feature-based attention decreases the FFI firing rate and increases the TDI firing rate. During strong stimulus competition, the E cells were synchronous in the beta frequency range (15–35 Hz), but with feature-based attention, they became synchronous in the gamma frequency range (35–50 Hz). We propose that the FFI correspond to fast-spiking, parvalbumin-positive basket cells and that the TDI correspond to cells with a double-bouquet morphology that are immunoreactive to calbindin or calretinin. Taken together, the model results provide an experimentally testable hypothesis for the behavior of two interneuron types under attentional modulation.


Author(s):  
Till S. Hartmann ◽  
Marc Zirnsak ◽  
Michael Marquis ◽  
Fred H. Hamker ◽  
Tirin Moore

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