Publications

  2017 Nat Comm, Yaser Merrikhi, Kelsey Clark, Eddy Albarran, Mohammadbagher Parsa, Marc Zirnsak, Tirin Moore & Behrad Noudoost

Prefrontal cortex modulates sensory signals in extrastriate visual cortex, in part via its direct projections from the frontal eye field (FEF), an area involved in selective attention. We find that working memory-related activity is a dominant signal within FEF input to visual cortex. Although this signal alone does not evoke spiking responses in areas V4 and MT during memory, the gain of visual responses in these areas increases, and neuronal receptive fields expand and shift towards the remembered location, improving the stimulus representation by neuronal populations. These results provide a basis for enhancing the representation of working memory targets and implicate persistent FEF activity as a basis for the interdependence of working memory and selective attention.

   2017  J Neurophys,Behrad Noudoost, Neda Nategh, Kelsey Clark, and Hossein Esteky

One goal of our nervous system is to form predictions about the world around us to facilitate our responses to upcoming events. One basis for such predictions could be the recently encountered visual stimuli, or the recent statistics of the visual environment. We examined the effect of recently experienced stimulus statistics on the visual representation of face stimuli by recording the responses of face-responsive neurons in the final stage of visual object recognition, the inferotemporal (IT) cortex, during blocks in which the probability of seeing a particular face was either 100% or only 12%. During the block with only face images, ∼30% of IT neurons exhibit enhanced anticipatory activity before the evoked visual response. This anticipatory modulation is followed by greater activity, broader view tuning, more distributed processing, and more reliable responses of IT neurons to the face stimuli. These changes in the visual response were sufficient to improve the ability of IT neurons to represent a variable property of the predictable face images (viewing angle), as measured by the performance of a simple linear classifier. These results demonstrate that the recent statistics of the visual environment can facilitate processing of stimulus information in the population neuronal representation.

    2015 Prog Neurob, Kelsey Clark, Ryan Fox Squire, Yaser Merrikhi, Behrad Noudoost.

Attention is a means of flexibly selecting and enhancing a subset of sensory input based on the current behavioral goals. Numerous signatures of attention have been identified throughout the brain, and now experimenters are seeking to determine which of these signatures are causally related to the behavioral benefits of attention, and the source of these modulations within the brain. Here, we review the neural signatures of attention throughout the brain, their theoretical benefits for visual processing, and their experimental correlations with behavioral performance. We discuss the importance of measuring cue benefits as a way to distinguish between impairments on an attention task, which may instead be visual or motor impairments, and true attentional deficits. We examine evidence for various areas proposed as sources of attentional modulation within the brain, with a focus on the prefrontal cortex. Lastly, we look at studies that aim to link sources of attention to its neuronal signatures else where in the brain.

    2015 J Neurosci.,Hu M, Clark KL, Gong X, Noudoost B, Li M, Moore T, Liang H.
Inferotemporal (IT) neurons are known to exhibit persistent, stimulus-selective activity during the delay period of object-based working memory tasks.Frontal eye field (FEF) neurons show robust, spatially selective delay period activity during memory-guided saccade tasks. We present a copularegression paradigm to examine neural interaction of these two types of signals between areas IT and FEF of the monkey during a working memorytask. This paradigm is based on copula models that can account for both marginal distribution over spiking activity of individual neurons within each area and joint distribution over ensemble activity of neurons between areas. Considering the popular GLMs as marginal models, we developed a general and flexible likelihood framework that uses the copula to integrate separate GLMs into a joint regression analysis. Such joint analysisessentially leads to a multivariate analog of the marginal GLM theory and hence efficient model estimation. In addition, we show that Granger causality between spike trains can be readily assessed via the likelihood ratio statistic. The performance of this method is validated by extensive simulations, and compared favorably to the widely used GLMs. When applied to spiking activity of simultaneously recorded FEF and IT neurons during working memory task, we observed significant Granger causality influence from FEF to IT, but not in the opposite direction, suggesting the role of the FEF in the selection and retention of visual information during working memory. The copula model has the potential to provide unique neurophysiological insights about network properties of the brain.

    2014 Front. Neural Circuits, Noudoost B, Clark KL,  

While much progress has been made in identifying the brain regions and neurochemical systems involved in the cognitive processes disrupted in mental illnesses, To date, the level of detail at which neurobiologists can describe the chain of events giving rise to cognitive functions is very rudimentary. Much of the intense interest in understanding cognitive functions is motivated by the hope that it might be possible to understand these complex functions at the level of neurons and neural circuits. Here, we review the current state of the literature regarding how modulations in catecholamine levels within the prefrontal cortex alter the neuronal and behavioral correlates of cognitive functions, particularly attention and working memory.

     2014 J Cogn Neurosci.  Clark KL,  Noudoost B, Moore T. 

We previously reported the existence of a persistent spatial signal in the FEF during object-based STM. This persistent activity reflected the location at which the sample appeared, irrespective of the location of upcoming targets. We hypothesized that such a spatial signal could be used to maintain or enhance object-selective memory activity elsewhere in cortex, analogous to the role of a spatial signal during attention. Here, we inactivated a portion of the FEF with GABA-a agonist muscimol to test whether the observed activity contributes to object memory performance. We found that, while RTs were slowed for saccades into the inactivated portion of retinotopic space, performance for samples appearing in that region was unimpaired. This contrasts with the devastating effects of the same FEF inactivation on purely spatial working memory, as assessed with the memory-guided saccade task. Thus, in a task in which a significant fraction of FEF neurons displayed persistent, sample location-based activity, disrupting this activity had no impact on task performance.

     2014 Nature, Zimsak M., Stelnmetz NA, Noudoost B, Xu KZ, Moore T. 

We experience the visual world through a series of saccadic eye movements, each one shifting our gaze to bring objects of interest to the fovea for further processing. Although such movements lead to frequent and substantial displacements of the retinal image, these displacements go unnoticed. It is widely assumed that a primary mechanism underlying this apparent stability is an anticipatory shifting of visual receptive fields (RFs) from their presaccadic to their postsaccadic locations before movement onset. Evidence of this predictive 'remapping' of RFs has been particularly apparent within brain structures involved in gaze control. However, critically absent among that evidence are detailed measurements of visual RFs before movement onset. Here we show that during saccade preparation, rather than remap, RFs of neurons in a prefrontal gaze control area massively converge towards the saccadic target. We mapped the visual RFs of prefrontal neurons during stable fixation and immediately before the onset of eye movements, using multi-electrode recordings in monkeys. Following movements from an initial fixation point to a target, RFs remained stationary in retinocentric space. However, in the period immediately before movement onset, RFs shifted by as much as 18 degrees of visual angle, and converged towards the target location. This convergence resulted in a threefold increase in the proportion of RFs responding to stimuli near the target region. In addition, like in human observers, the population of prefrontal neurons grossly mislocalized presaccadic stimuli as being closer to the target. Our results show that RF shifts do not predict the retinal displacements due to saccades, but instead reflect the overriding perception of target space during eye movements.

    2014  J Neurosci.,  Noudoost B, Clark KL,  Moore T. 

The responses of neurons within posterior visual cortex are enhanced when response field (RF) stimuli are targeted with saccadic eye movements. Although the motor-related activity within oculomotor structures seems a likely source of the enhancement, the origin of the modulation is unknown. We tested the role of the frontal eye field (FEF) in driving presaccadic modulation in area V4 by inactivating FEF neurons at retinotopically corresponding sites within the macaque monkey (Macaca mulatta) brain. As previously observed, FEF inactivation produced profound, and spatially specific, deficits in memory-guided saccades, and increased the latency, scatter, and duration of visually guided saccades. Despite the clear behavioral deficits, we found that rather than being eliminated or reduced by FEF inactivation, presaccadic enhancement of V4 activity was increased. FEF inactivation nonetheless diminished the stimulus discriminability of V4 visual responses both during fixation and in the presaccadic period. Thus, without input from the FEF, V4 neurons signaled more about the direction of saccades and less about the features of the saccadic target. In addition, FEF inactivation significantly increased the suppressive effects of non-RF stimuli on V4 activity. These results reveal multiple sources of presaccadic modulation in V4 and suggest that the FEF contributes uniquely to the presaccadic specification of visual target features.

    2013 Ann Rev Neurosci. Squire RF, Noudoost B, Schafer RJ, Moore T.  

The faculty of attention endows us with the capacity to process important sensory information selectively while disregarding information that is potentially distracting. Much of our understanding of the neural circuitry underlying this fundamental cognitive function comes from neurophysiological studies within the visual modality. Past evidence suggests that a principal function of the prefrontal cortex (PFC) is selective attention and that this function involves the modulation of sensory signals within posterior cortices. In this review, we discuss recent progress in identifying the specific prefrontal circuits controlling visual attention and its neural correlates within the primate visual system. In addition, we examine the persisting challenge of precisely defining how behavior should be affected when attentional function is lost.

    2013 J Neurosci. Noudoost B, Esteky H. 

Recognition of face-views is a crucial component of our social behavior. However, little is known about the neuronal basis of face-view recognition. Recent psychophysical studies have shown that adaptation to a particular face-view changes perception of other views in humans. To understand the neuronal basis of face-view representation and the mechanisms involved in face-view adaptation, we studied the responses of inferotemporal (IT) cortex neurons before and after face-view adaptation. We first used face-view adaptation to show that monkeys, as well as humans, exhibit face-view aftereffect, suggesting the presence of a view-sensitive representation in primates. Then, we recorded from IT neurons of monkeys and found that changes in responses of these neurons can account for changes in perception of face views attributable to adaptation, indicating IT as a neural correlate of face-view perception. More importantly, we provide evidence that IT neurons with wide-view tuning not only conveyed face-view information but also exhibited neural signatures of view aftereffect before neurons with narrower tuning. Our findings show that view-dependent representation of objects does not necessarily depend on narrow-tuned neurons. The finding that wide-view tuned neurons account for view-specific perceptual changes implies the importance of accumulating sensitivity and tolerance at the level of IT neurons, as the final stage of visual object recognition.

    2013 Proc Natl Acad Sci. Soltani A, Noudoost B, Moore T. 

To investigate mechanisms by which reward modulates target selection, we studied the behavioral effects of perturbing dopaminergic activity within the frontal eye field (FEF) of monkeys performing a saccadic choice task and simulated the effects using a plausible cortical network. We found that manipulation of FEF activity either by blocking D1 receptors (D1Rs) or by stimulating D2 receptors (D2Rs) increased the tendency to choose targets in the response field of the affected site. However, the D1R manipulation decreased the tendency to repeat choices on subsequent trials, whereas the D2R manipulation increased that tendency. Moreover, the amount of shift in target selection resulting from the two manipulations correlated in opposite ways with the baseline stochasticity of choice behavior. Our network simulation results suggest that D1Rs influence target selection mainly through their effects on the strength of inputs to the FEF and on recurrent connectivity, whereas D2Rs influence the excitability of FEF output neurons. Altogether, these results reveal dissociable dopaminergic mechanisms influencing target selection and suggest how reward can influence adaptive choice behavior via prefrontal dopamine. 

    2013 Nature Neurosci: News & Views. Noudoost B, Moore T.

The ability to filter out distracting sensory information is crucial to adaptive behavior. A primate study finds that prefrontal cortex is more important than parietal cortex in that function.

    2012 J Neurosci. Clark KL, Noudoost B, Moore T. 

Spatial attention is known to gate entry into visual short-term memory, and some evidence suggests that spatial signals may also play a role in binding features or protecting object representations during memory maintenance. To examine the persistence of spatial signals during object short-term memory, the activity of neurons in the frontal eye field (FEF) of macaque monkeys was recorded during an object-based delayed match-to-sample task. In this task, monkeys were trained to remember an object image over a brief delay, regardless of the locations of the sample or target presentation. FEF neurons exhibited visual, delay, and target period activity, including selectivity for sample location and target location. Delay period activity represented the sample location throughout the delay, despite the irrelevance of spatial information for successful task completion. Furthermore, neurons continued to encode sample position in a variant of the task in which the matching stimulus never appeared in their response field, confirming that FEF maintains sample location independent of subsequent behavioral relevance. FEF neurons also exhibited target-position-dependent anticipatory activity immediately before target onset, suggesting that monkeys predicted target position within blocks. These results show that FEF neurons maintain spatial information during short-term memory, even when that information is irrelevant for task performance.

    2011 Trends Cogn Sci. Noudoost B, Moore T. 

Several classes of neurotransmitters exert modulatory effects on a broad and diverse population of neurons throughout the brain. Some of these neuromodulators, especially acetylcholine and dopamine, have long been implicated in the neural control of selective attention. We review recent evidence and evolving ideas about the importance of these neuromodulatory systems in attention, particularly visual selective attention. We conclude that, although our understanding of their role in the neural circuitry of selective attention remains rudimentary, recent research has begun to suggest unique contributions of neuromodulators to different forms of attention, such as bottom-up and top-down attention.

     2011 Nature. Noudoost B, Moore T. 

The prefrontal cortex is thought to modulate sensory signals in posterior cortices during top-down attention, but little is known about the underlying neural circuitry. Experimental and clinical evidence indicate that prefrontal dopamine has an important role in cognitive functions, acting predominantly through D1 receptors. Here we show that dopamine D1 receptors mediate prefrontal control of signals in the visual cortex of macaques (Macaca mulatta). We pharmacologically altered D1-receptor-mediated activity in the frontal eye field of the prefrontal cortex and measured the effect on the responses of neurons in area V4 of the visual cortex. This manipulation was sufficient to enhance the magnitude, the orientation selectivity and the reliability of V4 visual responses to an extent comparable with the known effects of top-down attention. The enhancement of V4 signals was restricted to neurons with response fields overlapping the part of visual space affected by the D1 receptor manipulation. Altering either D1- or D2-receptor-mediated frontal eye field activity increased saccadic target selection but the D2 receptor manipulation did not enhance V4 signals. Our results identify a role for D1 receptors in mediating the control of visual cortical signals by the prefrontal cortex and suggest how processing in sensory areas could be altered in mental disorders involving prefrontal dopamine.

     2011 J Neurosci Methods. Noudoost B, Moore T. J Neurosci Methods.

We describe a modified system for the precise delivery of small volumes of drugs to brain sites of behaving monkeys during simultaneous single-neuron electrophysiology. The system combines a conventional microelectrode for recording single neurons and a small gauge microsyringe in a durable design. It incorporates newly available microfluidic components to achieve high-precision fluidic control. The system is inexpensive, reusable and easy to fabricate; it minimizes neural tissue damage and achieves reliable single-neuron recordings at the injection site. 

     2010 Curr Opin Neurobiol. Noudoost B, Chang MC, Steinmetz NA, Moore . 

Top-down visual attention improves perception of selected stimuli and that improvement is reflected in the neural activity at many stages throughout the visual system. Recent studies of top-down attention have elaborated on the signatures of its effects within visual cortex and have begun identifying its causal basis. Evidence from these studies suggests that the correlates of spatial attention exhibited by neurons within the visual system originate from a distributed network of structures involved in the programming of saccadic eye movements. We summarize this evidence and discuss its relationship to the neural mechanisms of spatial working memory. 

   2010 Basic and Clinical Neuroscience. Nilipour R, Saber GT, Noudoost. B.

Introduction:We investigated differential role of cortical and subcortical regions in verbal and non-verbal sound processing in ten patients who were native speakers of Persian with unilateral cortical and/or unilateral and bilateral subcortical lesions and 40 normal speakers as control subjects. Methods: The verbal tasks included monosyllabic, disyllabic dichotic and diotic tasks, and nonverbal tasks were semantic, asemantic recognition and sound localization. Results: Different profiles of ear extinction and hemispatial neglect was observed in our Left Hemisphere-Damaged (LHD) patients. Right Hemisphere-Damaged (RHD) patients with basal ganglia lesions showed mild hemi-spatial inattention of the ipsilesional and contralesional hemispace. LHD patients showed deficient performance in sound localization, but no evidence of significant impairment in sound localization was found in RHD patients except one. The patients with basal ganglia lesions irrespective of lesion side had impaired performance in semantic recognition. The results are suggestive of a network consisting of left and right basal ganglia and left cortical regions for non-verbal sound recognition. Discussion: The results also indicate a different role for left basal ganglia in sound object segregation versus sound localization. 

    2006 Brain Res. Noudoost B, Afraz SR, Vaziri-Pashkam M, Esteky H. 

Several lines of evidence have confirmed that visual integrity among the two hemifields is severely impaired following transection of posterior part of the corpus callosum (splenium). But the extent of this impairment differs for various visual functions. Here, in a posterior callosectomized patient (MD), interhemispheric visual spatial integrity is investigated in three experiments. In the first experiment, MD was asked to make decision about horizontal alignment of two balls presented simultaneously in one of three conditions: both in right or left hemifield, or each in one hemifield. We have previously shown that she is not able to perform a shape-matching task for stimuli presented to different hemifields. But in this task, MD was able to compare location of the two bilaterally presented stimuli significantly above chance level. Then we investigated whether attentive visual object tracking across vertical meridian of the visual field is possible in the absence of splenium. MD had to attentively track one bouncing ball among three identical balls, while it crossed the vertical midline in half of trials. Her performance in crossed conditions was significantly above chance level, but it was lower than uncrossed conditions. Finally, we investigated the contribution of simple interhemispheric temporal signals in performing the attentive tracking task. Results suggest that the patient was not using such temporal signals. Our results suggest that interhemispheric connections other than splenium can contribute in making an integral visual map across hemifields. Such an integrated map can be used for bilateral visual spatial comparisons and visual spatial attention. 

    2005 Brain Res Cogn Brain Res. Noudoost B, Adibi M, Moeeny A, Esteky H. 

Configural processing could develop for non-face visual objects as one becomes familiar with those objects through repeated exposure. To explore the role of familiarity in object recognition, we studied the effect of adaptation to a visual object (adapting stimulus) on the identification performance of other objects (test stimulus) while adapting and test stimuli were exactly the same, shared parts or were completely different. We used a subset of English alphabets (p, q, d and b) as familiar objects and an unfamiliar set of symbols constructed from same parts but with different configurations. Adaptation to a member of each set led to a lower identification performance for that object in a crowding paradigm. Adaptation to each member of the unfamiliar set resulted in decreased identification performance for the same object and those members of the set that shared parts with the adapting stimulus. But no such transfer of adaptation was observed for the familiar set. Our results support the notion that processing of object parts plays an important role in the recognition of unfamiliar objects while recognition of familiar objects is mainly based on configural processing mechanisms. 

     2004 Acta Neurobiol Exp. Nilipour R, Clarke S, Noudoost B, Saber GT, Najlerahim A.

The full or partial recovery of cognitive functions following brain lesions is believed to rely on the recruitment of alternative neural networks. This has been shown anatomically for selective auditory cognitive functions (Adriani et al. 2003b). We investigate here behavioral correlates that may accompany the use of alternative processing networks and in particular the resulting increase in response times. The performance of 5 patients with right or left unilateral hemispheric infarction and 6 normal control subjects in sound identification, asemantic sound recognition, sound localization, and sound motion perception was evaluated by the number of correct replies and response times for correct and wrong replies. Performance and response times were compared across patients and normal control subjects. Two patients with left lesions were deficient in sound identification and sound motion perception and normal in sound localization and asemantic sound recognition; one patient with right lesion was deficient in sound localization and sound motion perception and normal in sound identification and asemantic sound recognition; deficient performance was associated with increased response times. The remaining 2 patients (1 with left, 1 with right lesion) had normal performance in all 4 tasks but had significantly longer response times in some (but not all) tasks. Patients with normal or deficient performance tended more often than normal subjects to give faster correct than wrong replies. We propose that increased response time is an indication of processing within an alternative network. 

Noudoost B, Albarran E, Moore T. The New Cognitive Neuroscience, edited by Michael Gazzaniga (in press).

Clark KL, Noudoost B, Schafer RJ, Moore T. Handbook of Attention. Edited by Sabine Kastner and Anna Nobre, Oxford (in press).

Moore T, Schafer RJ, Noudoost B. Primate Neuroethology, edited by Michael Platt and Asif Ghazanfar, Elsevier, 2010

Moore T, Schafer RJ, Noudoost B. Primate Neuroethology, edited by Michael Platt and Asif Ghazanfar, Elsevier, 2010