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Noudoost, B.

Publications and source records attributed to Noudoost, B..

11 recordsLinked to original sources

A population readout of extrastriate activity reveals biased and smoothed temporal representations across saccades

Perception of visual time is transiently distorted around saccadic eye movements, yet the neuronal mechanisms constructing perisaccadic representations of time remain unclear. Here, we investigate how perisaccadic temporal information is encoded and read out in extrastriate cortex, by combining electrophysiological recordings in V4 and MT neuronal population in macaque monkeys under high spatiotemporal resolution visual stimulation, and a statistical modeling framework capturing perisaccadic response modulations at single-trial precision. Our analyses show that perisaccadic neuronal responses systematically shift the temporal representation of presaccadic stimuli within receptive fields-biasing them toward earlier times, and also reduce temporal sensitivity for presaccadic stimuli-impairing discrimination of stimulus onset times. Model-based readout using time-varying spatiotemporal sensitivity maps in neuronal ensembles enables quantitative characterization of these effects and identifies their specific neuronal response components at millisecond resolution. In silico manipulations further demonstrate a causal role of representational bias in reducing temporal sensitivity. These findings suggest that extrastriate cortex implements an active encoding strategy to stabilize presaccadic temporal information by favoring the most recent reliable input, revealing a fundamental tradeoff between temporal precision and robustness that supports a continuous visual percept across saccades. This finding also establishes a general role for extrastriate populations in constructing the perception of visual time.

neuroscience↗

Limits of V4 perisaccadic firing rate modulations in explaining perceptual mislocalization

Whether and how various visual sensory areas contribute to the perceived location of visual stimuli remains unknown. To test the role of neurons in extrastriate area V4 in generating alterations in spatial perception during saccadic eye movements (saccades), we examined perisaccadic mislocalization--the perceptual phenomenon in which visual stimuli appearing around the time of a saccade are perceived at a different position than their actual location. We designed and implemented a combined behavioral and electrophysiological framework in non-human primates to directly relate trial-by-trial spatial perception reports during saccades to neuronal firing rates in V4 populations. We measured monkeys perception of stimulus location behaviorally and found perisaccadic mislocalization opposite to the saccade direction. We also quantified population responses by computing the center of mass of firing rate activity across probe locations for V4 neurons with receptive fields close to the saccade target. While perisaccadic neuronal responses showed shifts toward the saccade target, these shifts did not systematically vary with the magnitude of perceptual mislocalization across trials. In conclusion, receptive field shifts based on the perisaccadic firing rate of V4 neurons are not sufficient to account for the magnitude of perceptual mislocalization in each trial, suggesting that more complex neural representation of perisaccadic visual information may be critical for linking extrastriate neural activity to saccade-induced perception.

neuroscience↗

Spectral decomposition of local field potentials uncovers frequency-tuned gain modulation of working memory in primate visual system

Working memory has been shown to modulate visual processing in a variety of ways, including changes in visual response gain, oscillatory power, spike timing, and phase coding of information1-3. Here we probe working memorys influence on various oscillatory components within visual areas, using the Maximal Overlap Discrete Wavelet Transform (MODWT) technique to decompose the local field potential(LFP)4; this method allows single-trial quantification of the properties of various oscillatory components. We examine the impact of spatial working memory on visual processing within the extrastriate middle temporal (MT) visual area of rhesus macaque monkeys, comparing the responses in MT when remembering a location inside or outside the receptive fields of the neurons being recorded. Using traditional bandpass filtering, we replicate previous reports that working memory enhances visual responses, low-frequency oscillatory power, spike-phase locking, and phase coding of visual information. Applying the MODWT method, we find that working memory modulates both oscillatory power and the precise frequency of oscillations within a general frequency band. The precise frequency of several lower frequency components (alpha, theta, and beta frequencies, but not gamma or high gamma) correlates with visually-evoked firing rates of MT neurons on a trial-by-trial basis. This relationship between firing rate and oscillatory component frequency is maintained across memory conditions, indicating a close link between the neural mechanisms driving oscillatory frequency and firing rates.

neuroscience↗

Frontotemporal bursting supports human working memory

Cortical neural activity varies dynamically during memory periods, when relevant information is not present in the environment. But how those dynamics are related to a code defining working memory (WM) performance is not known. Recent data shows brief bursts of activity in the high gamma (70-140 Hz) and beta (12-30 Hz) band within non-human primate lateral prefrontal cortex (PFC) is associated with WM processing. However, WM may be related to activity within a network of frontal executive and posterior sensory areas involved in stimulus perception. Here we tested whether gamma and beta bursting exist in lateral PFC and multisensory lateral temporal areas in humans during visual WM, and whether these areas are coupled via a phase-burst code. We used intracranial macroelectrode recordings from the middle frontal gyrus (MFG), which includes dorsolateral PFC, and from the middle temporal gyrus (MTG), an area important for visual processing. High gamma bursting increased in human left PFC during encoding and delay periods while beta bursting decreased. Interestingly, beta bursting increased in multisensory areas during encoding and remained high during the delay period, more so on the right. These effects varied with WM performance. Finally, we quantify the degree to which delay-period gamma bursting is locked to beta phase within and between regions of this network using a proposed metric termed phase-burst coupling (PBC). We find evidence that delay-period gamma bursting in temporal areas is locked to beta phase in PFC. Our findings suggest that WM may use bursting to support memory maintenance until readout. Significance StatementWorking memory is critical for everyday functioning and its disruption results in significant disability in patients with dementia, traumatic brain injury, and stroke. We recorded human intracranial data during a visual working memory task. We found that prefrontal cortex and multisensory temporal brain areas show neural bursting activity during the memory period and that such bursting is related to trial performance. Furthermore, these two areas may be coupled by a phase-burst code. Bursting has been found in non-human primates, rodents, and even crows, suggesting it is a general feature of memory, and perhaps of other aspects of cognition.

neuroscience↗

Prefrontal working memory signal primarily controls phase-coded information within extrastriate cortex

In order to understand how prefrontal cortex provides the benefits of working memory (WM) for visual processing we examined the influence of WM on the representation of visual signals in V4 neurons in two macaque monkeys. We found that WM induces strong {beta} oscillations in V4 and that the timing of action potentials relative to this oscillation reflects sensory information-i.e., a phase coding of visual information. Pharmacologically inactivating the Frontal Eye Field part of prefrontal cortex, we confirmed the necessity of prefrontal signals for the WM-driven boost in phase coding of visual information. Indeed, changes in the average firing rate of V4 neurons were correlated with WM-induced oscillatory changes. We present a network model to describe how WM signals can recruit sensory areas by inducing oscillations within these areas and discuss the implications of these findings for a sensory recruitment theory of WM through coherence.

animal behavior and cognition↗

Neural correlates of perisaccadic visual mislocalization in extrastriate cortex

When interacting with the visual world using saccadic eye movements (saccades), the perceived location of visual stimuli becomes biased, a phenomenon called perisaccadic mislocalization, which is indeed an exemplar of the brains dynamic representation of the visual world. However, the neural mechanism underlying this altered visuospatial perception and its potential link to other perisaccadic perceptual phenomena have not been established. Using a combined experimental and computational approach, we were able to quantify spatial bias around the saccade target (ST) based on the perisaccadic dynamics of extrastriate spatiotemporal sensitivity captured by statistical models. This approach could predict the perisaccadic spatial bias around the ST, consistent with the psychophysical studies, and revealed the precise neuronal response components underlying representational bias. These findings also established the crucial role of response remapping toward ST representation for neurons with receptive fields far from the ST in driving the ST spatial bias. Moreover, we showed that, by allocating more resources for visual target representation, visual areas enhance their representation of the ST location, even at the expense of transient distortions in spatial representation. This potential neural basis for perisaccadic ST representation, also supports a general role for extrastriate neurons in creating the perception of stimulus location.

neuroscience↗

Prefrontal activity sharpens spatial sensitivity of extrastriate neurons

Prefrontal cortex is known to exert its control over representation of visual signals in extrastriate areas such as V4. Frontal Eye Field (FEF) is suggested to be the proxy for the prefrontal control of visual signals. However, it is not known which aspects of sensory representation within extrastriate areas are under the influence of FEF activity. We employed a causal manipulation to examine how FEF activity contributes to spatial sensitivity of extrastriate neurons. Finding FEF and V4 areas with overlapping response field (RF) in two macaque monkeys, we recorded V4 responses before and after inactivation of the overlapping FEF. We assessed spatial sensitivity of V4 neurons in terms of their response gain, RF spread, coding capacity, and spatial discriminability. Unexpectedly, we found that in the absence of FEF activity, spontaneous and visually-evoked activity of V4 neurons both increase and their RFs enlarge. However, assessing the spatial sensitivity within V4, we found that these changes were associated with a reduction in the ability of V4 neurons to represent spatial information: After FEF inactivation, V4 neurons showed a reduced response gain and a decrease in their spatial discriminability and coding capacity. These results show the necessity of FEF activity for shaping spatial responses of extrastriate neurons and indicates the importance of FEF inputs in sharpening the sensitivity of V4 responses.

neuroscience↗

Dissociating the Contributions of Frontal Eye Field Activity to Spatial Working Memory and Motor Preparation

Neurons within dorsolateral prefrontal cortex of primates are characterized by robust persistent spiking activity exhibited during the delay period of working memory tasks. This includes the frontal eye field (FEF) where nearly half of the neurons are active when spatial locations are held in working memory. Past evidence has established the FEFs contribution to the planning and triggering of saccadic eye movements as well as to the control of visual spatial attention. However, it remains unclear if persistent delay activity reflects a similar dual role in movement planning and visuospatial working memory. We trained monkeys to alternate between different forms of a spatial working memory task which could dissociate remembered stimulus locations from planned eye movements. We tested the effects of inactivation of FEF sites on behavioral performance in the different tasks. Consistent with previous studies, FEF inactivation impaired the execution of memory-guided saccades, and impaired performance when remembered locations matched the planned eye movement. In contrast, memory performance was largely unaffected when the remembered location was dissociated from the correct eye movement response. Overall, the inactivation effects demonstrated clear deficits on eye movements, regardless of task type, but little or no evidence of a deficit in spatial working memory. Thus, our results indicate that persistent delay activity in the FEF contributes primarily to the preparation of eye movements and not to spatial working memory.

neuroscience↗

Working Memory Gates Visual Input to Primate Prefrontal Neurons

Visually guided behavior relies on the integration of sensory input with information held in working memory. Yet it remains unclear how this is accomplished at the level of neural circuits. We studied the direct visual cortical inputs to neurons within a visuomotor area of prefrontal cortex in behaving monkeys. We show that the synaptic efficacy of visual cortical input to prefrontal cortex is gated by information held in working memory. Surprisingly, visual input to prefrontal neurons was found to target those with both visual and motor properties, rather than preferentially targeting other visual neurons. Furthermore, activity evoked from visual cortex was larger in magnitude, more synchronous, and more rapid, when monkeys remembered locations that matched the location of visual input. These results indicate that working memory directly influences the circuitry that transforms visual input into visually guided behavior.

neuroscience↗

Frontotemporal Coordination Predicts Working Memory Performance and its Local Neural Signatures

Neurons in some sensory areas reflect the content of working memory (WM) in their spiking activity. However, this spiking activity is seldom related to behavioral performance. We studied the responses of inferotemporal (IT) neurons, which exhibit object-selective activity, along with Frontal Eye Field (FEF) neurons, which exhibit spatially-selective activity, during the delay period of an object WM task. Unlike the spiking activity and local field potentials (LFPs) within these areas, which were poor predictors of behavioral performance, the phase-locking of IT spikes and LFPs with the beta band of FEF LFPs robustly predicted successful WM maintenance. In addition, IT neurons exhibited greater object-selective persistent activity when their spikes were locked to the phase of FEF LFPs. These results demonstrate a key role of coordination between prefrontal and temporal cortex in the successful maintenance of visual information during WM.

neuroscience↗

A Sensory Memory to Preserve Visual Representations Across Eye Movements

During eye movements, the continuous flow of visual information is frequently disrupted due to abrupt changes of the retinal image, yet our perception of the visual world is uninterrupted. In order to identify the neuronal response components necessary for the integration of perception across eye movements, we developed a computational model to trace the changes in the visuospatial sensitivity of neurons in the extrastriate cortex of macaque monkeys with high temporal precision. Employing the model, we examined the perceptual implications of these changes and found that by maintaining a memory of the visual scene, extrastriate neurons produce an uninterrupted representation of the visual world. These results reveal how our brain exploits available information to maintain the sense of vision in the absence of visual information.

neuroscience↗