scholarly journals Working memory gates visual input to primate prefrontal neurons

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Behrad Noudoost ◽  
Kelsey Lynne Clark ◽  
Tirin Moore

Visually guided behavior relies on the integration of sensory input and information held in working memory (WM). 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 efficacy of visual input to prefrontal cortex is gated by information held in WM. 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 WM directly influences the circuitry that transforms visual input into visually guided behavior.

2020 ◽  
Author(s):  
Behrad Noudoost ◽  
Kelsey L. Clark ◽  
Tirin Moore

AbstractVisually 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.


2003 ◽  
Vol 15 (6) ◽  
pp. 771-784 ◽  
Author(s):  
T. Jason Druzgal ◽  
Mark D'Esposito

Interactions between prefrontal cortex (PFC) and stimulusspecific visual cortical association areas are hypothesized to mediate visual working memory in behaving monkeys. To clarify the roles for homologous regions in humans, event-related fMRI was used to assess neural activity in PFC and fusiform face area (FFA) of subjects performing a delay-recognition task for faces. In both PFC and FFA, activity increased parametrically with memory load during encoding and maintenance of face stimuli, despite quantitative differences in the magnitude of activation. Moreover, timing differences in PFC and FFA activation during memory encoding and retrieval implied a context dependence in the flow of neural information. These results support existing neurophysiological models of visual working memory developed in the nonhuman primate.


2021 ◽  
Vol 15 ◽  
Author(s):  
William H. Nesse ◽  
Zahra Bahmani ◽  
Kelsey Clark ◽  
Behrad Noudoost

Extrastriate visual neurons show no firing rate change during a working memory (WM) task in the absence of sensory input, but both αβ oscillations and spike phase locking are enhanced, as is the gain of sensory responses. This lack of change in firing rate is at odds with many models of WM, or attentional modulation of sensory networks. In this article we devised a computational model in which this constellation of results can be accounted for via selective activation of inhibitory subnetworks by a top-down working memory signal. We confirmed the model prediction of selective inhibitory activation by segmenting cells in the experimental neural data into putative excitatory and inhibitory cells. We further found that this inhibitory activation plays a dual role in influencing excitatory cells: it both modulates the inhibitory tone of the network, which underlies the enhanced sensory gain, and also produces strong spike-phase entrainment to emergent network oscillations. Using a phase oscillator model we were able to show that inhibitory tone is principally modulated through inhibitory network gain saturation, while the phase-dependent efficacy of inhibitory currents drives the phase locking modulation. The dual contributions of the inhibitory subnetwork to oscillatory and non-oscillatory modulations of neural activity provides two distinct ways for WM to recruit sensory areas, and has relevance to theories of cortical communication.


2010 ◽  
Vol 20 (04) ◽  
pp. 249-265 ◽  
Author(s):  
MASSIMILIANO VERSACE ◽  
MARCO ZORZI

How do organisms select and organize relevant sensory input in working memory (WM) in order to deal with constantly changing environmental cues? Once information has been stored in WM, how is it protected from and altered by the continuous stream of sensory input and internally generated planning? The present study proposes a novel role for dopamine (DA) in the maintenance of WM in the prefrontal cortex (Pfc) neurons that begins to address these issues. In particular, DA mediates the alternation of the Pfc network between input-driven and internally-driven states, which in turn drives WM updates and storage. A biologically inspired neural network model of Pfc is formulated to provide a link between the mechanisms of state switching and the biophysical properties of Pfc neurons. This model belongs to the recurrent competitive fields33 class of dynamical systems which have been extensively mathematically characterized and exhibit the two functional states of interest: input-driven and internally-driven. This hypothesis was tested with two working memory tasks of increasing difficulty: a simple working memory task and a delayed alternation task. The results suggest that optimal WM storage in spite of noise is achieved with a phasic DA input followed by a lower DA sustained activity. Hypo and hyper-dopaminergic activity that alter this ideal pattern lead to increased distractibility from non-relevant pattern and prolonged perseverations on presented patterns, respectively.


2011 ◽  
Vol 106 (5) ◽  
pp. 2180-2188 ◽  
Author(s):  
Xin Zhou ◽  
Xue-Lian Qi ◽  
Kristy Douglas ◽  
Kathini Palaninathan ◽  
Hyun Sug Kang ◽  
...  

The prefrontal cortex, a cortical area essential for working memory and higher cognitive functions, is modulated by a number of neurotransmitter systems, including acetylcholine; however, the impact of cholinergic transmission on prefrontal activity is not well understood. We relied on systemic administration of a muscarinic receptor antagonist, scopolamine, to investigate the role of acetylcholine on primate prefrontal neuronal activity during execution of working memory tasks and recorded neuronal activity with chronic electrode arrays and single electrodes. Our results indicated a dose-dependent decrease in behavioral performance after scopolamine administration in all the working memory tasks we tested. The effect could not be accounted for by deficits in visual processing, eye movement responses, or attention, because the animals performed a visually guided saccade task virtually error free, and errors to distracting stimuli were not increased. Performance degradation under scopolamine was accompanied by decreased firing rate of the same cortical sites during the delay period of the task and decreased selectivity for the spatial location of the stimuli. These results demonstrate that muscarinic blockade impairs performance in working memory tasks and prefrontal activity mediating working memory.


2019 ◽  
Author(s):  
Yosef Singer ◽  
Ben D. B. Willmore ◽  
Andrew J. King ◽  
Nicol S. Harper

Visual neurons respond selectively to specific features that become increasingly complex in their form and dynamics from the eyes to the cortex. Retinal neurons prefer localized flashing spots of light, primary visual cortical (V1) neurons moving bars, and those in higher cortical areas, such as middle temporal (MT) cortex, favor complex features like moving textures. Whether there are general computational principles behind this diversity of response properties remains unclear. To date, no single normative model has been able to account for the hierarchy of tuning to dynamic inputs along the visual pathway. Here we show that hierarchical application of temporal prediction - representing features that efficiently predict future sensory input from past sensory input - can explain how neuronal tuning properties, particularly those relating to motion, change from retina to higher visual cortex. This suggests that the brain may not have evolved to efficiently represent all incoming information, as implied by some leading theories. Instead, the selective representation of sensory inputs that help in predicting the future may be a general neural coding principle, which when applied hierarchically extracts temporally-structured features that depend on increasingly high-level statistics of the sensory input.


2017 ◽  
Vol 118 (1) ◽  
pp. 15-28 ◽  
Author(s):  
Kelly R. Bullock ◽  
Florian Pieper ◽  
Adam J. Sachs ◽  
Julio C. Martinez-Trujillo

Common trends observed in many visual and oculomotor-related cortical areas include retinotopically organized receptive and movement fields exhibiting a Gaussian shape and increasing size with eccentricity. These trends are demonstrated in the frontal eye fields, many visual areas, and the superior colliculus but have not been thoroughly characterized in prearcuate area 8Ar of the prefrontal cortex. This is important since area 8Ar, located anterior to the frontal eye fields, is more cytoarchitectonically similar to prefrontal areas than premotor areas. Here we recorded the responses of 166 neurons in area 8Ar of two male macaques while the animals made visually guided saccades to a peripheral sine-wave grating stimulus positioned at 1 of 40 possible locations (8 angles along 5 eccentricities). To characterize the neurons’ receptive and movement fields, we fit a bivariate Gaussian model to the baseline-subtracted average firing rate during stimulus presentation (early and late visual epochs) and before saccade onset (presaccadic epoch). One hundred twenty-one of one hundred sixty-six neurons showed spatially selective visual and presaccadic responses. Of the visually selective neurons, 76% preferred the contralateral visual hemifield, whereas 24% preferred the ipsilateral hemifield. The angular width of visual and movement-related fields scaled positively with increasing eccentricity. Moreover, responses of neurons with visual receptive fields were modulated by target contrast, exhibiting sigmoid tuning curves that resemble those of visual neurons in upstream areas such as MT and V4. Finally, we found that neurons with receptive fields at similar spatial locations were clustered within the area; however, this organization did not appear retinotopic. NEW & NOTEWORTHY We recorded the responses of neurons in lateral prefrontal area 8Ar of macaques during a visually guided saccade task using multielectrode arrays. Neurons have Gaussian-shaped visual and movement fields in both visual hemifields, with a bias toward the contralateral hemifield. Visual neurons show contrast response functions with sigmoid shapes. Visual neurons tend to cluster at similar locations within the cortical surface; however, this organization does not appear retinotopic.


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