scholarly journals Adolescent frontal top-down neurons receive heightened local drive to establish adult attentional behavior in mice

2020 ◽  
Author(s):  
Elisa M Nabel ◽  
Yury Garkun ◽  
Hiroyuki Koike ◽  
Masato Sadahiro ◽  
Ana Liang ◽  
...  

AbstractFrontal top-down cortical neurons projecting to sensory cortical regions are well-positioned to integrate long-range inputs with local circuitry in frontal cortex to implement top-down attentional control of sensory regions. How adolescence contributes to the maturation of top-down neurons and associated local/long-range input balance, and the establishment of attentional control is poorly understood. Here we combine projection-specific electrophysiological and rabies-mediated input mapping in mice to uncover adolescence as a developmental stage when frontal top-down neurons projecting from the anterior cingulate to visual cortex are highly functionally integrated into local excitatory circuitry and have heightened activity compared to adulthood. Chemogenetic suppression of top-down neuron activity selectively during adolescence, but not later periods, produces long-lasting visual attentional behavior deficits, and results in excessive loss of local excitatory inputs in adulthood. Our study reveals an adolescent sensitive period when top-down neurons integrate local circuits with long-range connectivity to produce attentional behavior.

2004 ◽  
Vol 91 (1) ◽  
pp. 223-229 ◽  
Author(s):  
Soo-Hyun Lee ◽  
Daniel J. Simons

Local circuitry within layer IV whisker-related barrels is preferentially sensitive to thalamic population firing synchrony, and neurons respond most vigorously to stimuli, such as high-velocity whisker deflections, that evoke it. Field potential recordings suggest that thalamic barreloid neurons having similar angular preferences fire synchronously. To examine whether angular tuning of cortical neurons might also be affected by thalamic firing synchrony, we characterized responses of layer IV units to whisker deflections that varied in angular direction and velocity. Barrel regular-spike units (RSUs) became more tuned for deflection angle with slower whisker movements. Deflection amplitude had no affect. Barrel fast-spike units (FSUs) were poorly tuned for deflection angle, and their responses remained constant with different deflection velocity. The dependence of angular tuning on deflection velocity among barrel RSUs appears to reflect the same underlying response dynamics that determine their velocity sensitivity and receptive field focus. Unexpectedly, septal RSUs and FSUs are largely similar to their barrel counterparts despite available evidence suggesting that they receive different afferent inputs and are embedded within different local circuits.


2021 ◽  
Vol 7 (10) ◽  
pp. eabe1527
Author(s):  
Elisa N. Falk ◽  
Kevin J. Norman ◽  
Yury Garkun ◽  
Michael P. Demars ◽  
Susanna Im ◽  
...  

Cognitive function depends on frontal cortex development; however, the mechanisms driving this process are poorly understood. Here, we identify that dynamic regulation of the nicotinic cholinergic system is a key driver of attentional circuit maturation associated with top-down frontal neurons projecting to visual cortex. The top-down neurons receive robust cholinergic inputs, but their nicotinic tone decreases following adolescence by increasing expression of a nicotinic brake, Lynx1. Lynx1 shifts a balance between local and long-range inputs onto top-down frontal neurons following adolescence and promotes the establishment of attentional behavior in adulthood. This key maturational process is disrupted in a mouse model of fragile X syndrome but was rescued by a suppression of nicotinic tone through the introduction of Lynx1 in top-down projections. Nicotinic signaling may serve as a target to rebalance local/long-range balance and treat cognitive deficits in neurodevelopmental disorders.


Science ◽  
2014 ◽  
Vol 345 (6197) ◽  
pp. 660-665 ◽  
Author(s):  
Siyu Zhang ◽  
Min Xu ◽  
Tsukasa Kamigaki ◽  
Johnny Phong Hoang Do ◽  
Wei-Cheng Chang ◽  
...  

Top-down modulation of sensory processing allows the animal to select inputs most relevant to current tasks. We found that the cingulate (Cg) region of the mouse frontal cortex powerfully influences sensory processing in the primary visual cortex (V1) through long-range projections that activate local γ-aminobutyric acid–ergic (GABAergic) circuits. Optogenetic activation of Cg neurons enhanced V1 neuron responses and improved visual discrimination. Focal activation of Cg axons in V1 caused a response increase at the activation site but a decrease at nearby locations (center-surround modulation). Whereas somatostatin-positive GABAergic interneurons contributed preferentially to surround suppression, vasoactive intestinal peptide-positive interneurons were crucial for center facilitation. Long-range corticocortical projections thus act through local microcircuits to exert spatially specific top-down modulation of sensory processing.


2021 ◽  
Author(s):  
Kevin J Norman ◽  
Julia Bateh ◽  
Priscilla Maccario ◽  
Christina Cho ◽  
Keaven Caro ◽  
...  

Top-down attention is a dynamic cognitive process that facilitates the detection of the task-relevant stimuli from our complex sensory environment. A neural mechanism capable of deployment under specific task-demand conditions would be crucial to efficiently control attentional processes and improve goal-directed attention performance in task demand-dependent manner. Previous studies have shown that frontal top-down neurons projecting from anterior cingulate area (ACA) to the visual cortex (VIS; ACAvis) are required for attentional behavior during the 5-choice serial reaction time task (5CSRTT) in mice. However, it is unknown whether the contribution of this projecting neurons is dependent on the extent of task demand. Here, we examine the differential contribution of ACAvis projection neurons to the attentional behavior in adult male mice performing two visual attention tasks of varying task demand: the 5CSRTT and 2-choice serial reaction time task (2CSRTT). We found that optogenetic suppression ACAvis projections immediately before stimulus presentation has no effect during the 2CSRTT in contrast to the impaired performance during the 5CSRTT. Fiber photometry calcium imaging of ACAvis neuron activity revealed that these neurons, which are recruited after errors during 5CSRTT, are not recruited during 2CSRTT. These results suggest that ACAvis projections are necessary only when task demand is high and that ACAvis neuron activity may not provide an error monitoring signal when task demand is low. Collectively, this frontal-sensory ACAvis projection regulates visual attention behavior during specific high task demand conditions, pointing to a flexible circuit-based mechanism for promoting attentional behavior.


NeuroImage ◽  
2010 ◽  
Vol 50 (3) ◽  
pp. 1292-1302 ◽  
Author(s):  
Rebecca Levin Silton ◽  
Wendy Heller ◽  
David N. Towers ◽  
Anna S. Engels ◽  
Jeffrey M. Spielberg ◽  
...  

2006 ◽  
Vol 18 (5) ◽  
pp. 766-780 ◽  
Author(s):  
S. Crottaz-Herbette ◽  
V. Menon

Attentional control provides top-down influences that allow task-relevant stimuli and responses to be processed preferentially. The anterior cingulate cortex (ACC) plays an important role in attentional control, but the spatiotemporal dynamics underlying this process is poorly understood. We examined the activation and connectivity of the ACC using functional magnetic resonance imaging (fMRI) along with fMRI-constrained dipole modeling of event-related potentials (ERPs) obtained from subjects who performed auditory and visual oddball attention tasks. Although attention-related responses in the ACC were similar in the two modalities, effective connectivity analyses showed modality-specific effects with increased ACC influences on the Heschl and superior temporal gyri during auditory task and on the striate cortex during visual task. Dipole modeling of ERPs based on source locations determined from fMRI activations showed that the ACC was the major generator of N2b-P3a attention-related components in both modalities, and that primary sensory regions generated a small mismatch signal about 50 msec prior to feedback from the ACC and a large signal 60 msec after feedback from the ACC. Taken together, these results provide converging neuroimaging and electrophysiological evidence for top-down attentional modulation of sensory processing by the ACC. Our findings suggest a model of attentional control based on dynamic bottom-up and top-down interactions between the ACC and primary sensory regions.


2012 ◽  
Author(s):  
Charles L. Folk ◽  
Deborah Kendzierski ◽  
Brad Wyble

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