Biology subjects

Banaie Boroujeni, K.

Publications and source records attributed to Banaie Boroujeni, K..

9 recordsLinked to original sources

bioRxiv2026

Ephaptic coupling improves the neural population code

Neurons share an extracellular medium, so every spikes current sets up a local field that feeds back onto the membrane potential of nearby cells, an interaction known as ephaptic coupling. The local field is usually studied by imposing it externally, for example by injecting sinusoidal currents through an extracellular electrode, which entrains and synchronizes firing. However, an endogenous field, self-generated by the networks own spiking, is a different phenomenon whose functional role stays unclear, because it cannot be removed without silencing the neurons that produce it. We built matched spiking networks with and without a self-consistent endogenous field, and a rate-matched control separating the field from firing rate. The results show that the origin of the field determines the effect. A field the network generated for itself decorrelated the population, expanded its dimensionality, and improved decoding, whereas the same field imposed from outside did the opposite, synchronizing the population and reducing coding performance. The benefit held across a spatial and a temporal coding task and survived rate-matching. A closed-form theory connects the decorrelation to the field acting as a spatial filter on the slow component that neurons share. To look for this in cortex, we analyzed multi-patch recordings, showing that a neurons spikes left a distance-dependent trace in unconnected neighbors which we reproduced by the same field model. The self-generated field is therefore not a by-product but a mechanism that, without wiring, can improve the population code and reshape the geometry of neural population dynamics.

neuroscience↗

bioRxiv2022

Routing States Transition During Oscillatory Bursts and Attention States

Neural information routing relies on spatiotemporal activity dynamics across interconnected brain areas. However, it remains unclear how routing states emerge at fast spiking timescales and interact with the slower activity dynamics of larger networks during cognitive processes. Here, we show that localized neural spiking events generate long-range directional routing states with spiking activity in distant brain areas that dynamically switch or amplify during oscillatory bursts, selective attention, and decision-making. Computational modeling and neural recordings from lateral prefrontal cortex (LPFC), anterior cingulate cortex (ACC), and striatum of nonhuman primates revealed that cross-areal, directional routing states arise within [~]20 ms around spikes of single neurons. On average, LPFC spikes led activity in the ACC and striatum by few milliseconds. The routing state was amplified during LPFC beta bursts between the LPFC and striatum and switched direction during ACC theta/alpha bursts between ACC and LPFC. Selective attention amplified the lead of these theta/alpha-specific lead-ensembles in the ACC, while decision-making amplified the lead of ACC and LPFC spiking output over the striatum. Notably, the fast lead/lag relationships of cross-areal neuronal ensembles that were modulated by attention states or decision-making predicted firing rate dynamics of their neurons during those functional states at slower timescales. Overall, our findings demonstrate directional routing of spiking activity across nonhuman primate frontal and striatal areas, as well as the functional and network states that modulate the direction and magnitude of these interactions. SummaryFast spatio-temporal dynamics of brain activity subserves the routing of information across distant regions and is integral to flexible cognition, decision-making, and selective attention. This study demonstrates that routing dynamics emerge as 20 ms brief lead and lag relationships of spiking activities across distant brain areas. The direction and magnitude of the lead and lag relationships systematically switched during frequency-specific oscillatory bursts and when attention shifts to visual cues.

neuroscience↗

bioRxiv2021

Dose-dependent dissociation of pro-cognitive effects of donepezil on attention and cognitive flexibility in rhesus monkeys

BACKGROUNDDonepezil exerts pro-cognitive effects by non-selectively enhancing acetylcholine (ACh) across multiple brain systems. The brain systems that mediate pro-cognitive effects of attentional control and cognitive flexibility are the prefrontal cortex and the anterior striatum which have different pharmacokinetic sensitivities to ACh modulation. We speculated that these area-specific ACh profiles lead to distinct optimal dose-ranges for donepezil to enhance the cognitive domains of attention and flexible learning. METHODSTo test for dose-specific effects of donepezil on different cognitive domains we devised a multi-task paradigm for nonhuman primates (NHPs) that assessed attention and cognitive flexibility. NHPs received either vehicle or variable doses of donepezil prior to task performance. We measured donepezil intracerebral and how strong it prevented the breakdown of ACh within prefrontal cortex and anterior striatum using solid-phase-microextraction neurochemistry. RESULTSThe highest administered donepezil dose improved attention and made subjects more robust against distractor interference, but it did not improve flexible learning. In contrast, only a lower dose range of donepezil improved flexible learning and reduced perseveration, but without distractor-dependent attentional improvement. Neurochemical measurements confirmed a dose-dependent increase of extracellular donepezil and decreases in choline within the prefrontal cortex and the striatum. CONCLUSIONSThe donepezil dose for maximally improving attention functions differed from the dose range that enhanced cognitive flexibility despite the availability of the drug in the major brain systems supporting these cognitive functions. Thus, the non-selective acetylcholine esterase inhibitor donepezil inherently trades improvement in the attention domain for improvement in the cognitive flexibility domain at a given dose range.

pharmacology and toxicology↗

bioRxiv2021

Transcranial Ultrasound Stimulation in Anterior Cingulate Cortex Impairs Information Sampling and Learning in Loss Contexts

Neuronal subgroups in anterior cingulate cortex (ACC) and the anterior striatum (STR) encode the reward structure of a given environment. But whether or how this reward information is used to guide information sampling, optimize decision making, or motivate behavior in cognitively challenging situations has remained elusive. Here, we causally tested these scenarios by transiently disrupting ACC and STR of rhesus monkeys with transcranial ultrasound with a learning task that independently varied cognitive and motivational demands. We found that disrupting the ACC, but not the STR, prolonged information sampling and reduced learning efficiency whenever the motivational payoff was low. These impairments were most pronounced at high cognitive demands and based on an inability to use loss experiences to improve performance. These results provide causal evidence that the ACC is necessary for motivation, to overcome anticipated costs from negative (loss) outcomes, and for cognition, to enhance visual information sampling during adaptive behavior. HIGHLIGHTSO_LITranscranial ultrasound stimulation of the anterior cingulate cortex disrupts learning after loss experience. C_LIO_LIThe ultrasound-induced learning deficit is exacerbated at high cognitive load. C_LIO_LIThe ultrasound-induced learning deficit is accompanied by inefficient fixational information sampling. C_LIO_LIAnterior cingulate cortex causally supports credit assignment of aversive outcomes to visual features. C_LI

neuroscience↗

bioRxiv2021

A Kiosk Station for the Assessment of Multiple Cognitive Domains and Enrichment of Monkeys

BackgroundNonhuman primates (NHPs) are self-motivated to perform cognitive tasks on touchscreens in their animal housing setting. To leverage this ability, fully integrated hardware and software solutions are needed, that work within housing and husbandry routines while also spanning cognitive task constructs of the Research Domain Criteria (RDoC). New MethodWe describe a Kiosk Station (KS-1) that provides robust hardware and software solutions for running cognitive tasks in cage-housed NHPs. KS-1 consists of a frame for mounting flexibly on housing cages, a touchscreen animal interface with mounts for receptables, reward pumps and cameras, and a compact computer cabinet with an interface for controlling behavior. Behavioral control is achieved with a unity3D program that is virtual-reality capable, allowing semi-naturalistic visual tasks to assess multiple cognitive domains. ResultsKS-1 is fully integrated into the regular housing routines of monkeys. A single person can operate multiple KS-1s. Monkeys engage with KS-1 at high motivation and cognitive performance levels at high intra-individual consistency. Comparison with Existing MethodsKS-1 is optimized for flexible mounting onto standard apartment cage systems. KS-1 has a robust animal interface with options for gaze/reach monitoring. It has an integrated user interface for controlling multiple cognitive task using a common naturalistic object space designed to enhance task engagement. All custom KS-1 components are open-sourced. ConclusionsKS-1 is a versatile tool for cognitive profiling and enrichment of cage-housed monkeys. It reliably measures multiple cognitive domains which promises to advance our understanding of animal cognition, inter-individual differences and underlying neurobiology in refined, ethologically meaningful behavioral foraging contexts.

animal behavior and cognition↗

bioRxiv2020

Gains and Losses Differentially Regulate Attentional Efficacy and Learning at Low and High Attentional Load

Prospective gains and losses modulate cognitive processing, but it is unresolved whether gains and losses can facilitate flexible learning in changing environments. The prospect of gains might enhance flexible learning through prioritized processing of reward-predicting stimuli but is unclear how far this learning benefit extends when task demands increase. Similarly, experiencing losses might facilitate learning when they trigger attentional re-orienting away from loss-inducing stimuli, but losses may also impair learning by reducing the precise encoding of loss-inducing stimuli. To clarify these divergent views, we tested how varying magnitudes of gains and losses affect the flexible learning of object values in environments that varied attentional load by increasing the number of interfering object features during learning. With this task design we found that larger prospective gains improved learning efficacy and learning speed, but only when attentional load was low. In contrast, expecting losses generally impaired learning efficacy and this impairment was larger at higher attentional load. These findings functionally dissociate the contributions of prospective gains and losses on flexible learning, suggesting they operate via separate control mechanisms. One process is triggered by experiencing loss and seems to disrupt the encoding of specific loss-inducing features which leads to less efficient exploration during learning. The second process is triggered by experiencing gains which enhances learning through a more efficient prioritizing of reward-predicting stimulus features as long as the interference of distracting information is limited. These results demonstrate strengths and limitations of motivational regulation of learning efficacy in multidimensional environments having variable attentional loads. Significance statementIncreasing the prospective gains is assumed to enhance flexible learning, but there is no consensus on whether imposing losses enhances or impairs flexible learning. We show that anticipating loss of already attained assets generally reduced learning changes in the relevance of visual objects and that this learning impediment is more pronounced when learning demands higher attentional control of interference from distracting object features. Moreover, we show that increasing the prospective gains indeed facilitates learning, but only when the learning problem has intermediate or low attentional demands. These findings document that the beneficial effects of gains hit a limit when task demands increase, and that prospective losses reduce cognitive flexibility already at low task demands which is exacerbated when task demands increase. These findings provide novel insight into the strengths and limitations of gains and of losses to support flexible learning in multidimensional environments imposing variable attentional loads.

animal behavior and cognition↗

bioRxiv2020

Interneuron Specific Gamma Synchronization Encodes Uncertain Cues and Prediction Errors in Lateral Prefrontal and Anterior Cingulate Cortex

Inhibitory interneurons are believed to realize critical gating functions in cortical circuits, but it has been difficult to ascertain the content of gated information for well characterized interneurons in primate cortex. Here, we address this question by characterizing putative interneurons in primate prefrontal and anterior cingulate cortex while monkeys engaged in attention demanding reversal learning. We find that subclasses of narrow spiking neurons have a relative suppressive effect on the local circuit indicating they are inhibitory interneurons. One of these interneuron subclasses showed prominent firing rate modulations and (35-45 Hz) gamma synchronous spiking during periods of uncertainty in both, lateral prefrontal cortex (LPFC) and in anterior cingulate cortex (ACC). In LPFC this interneuron subclass activated when the uncertainty of attention cues was resolved during flexible learning, whereas in ACC it fired and gamma-synchronized when outcomes were uncertain and prediction errors were high during learning. Computational modeling of this interneuron-specific gamma band activity in simple circuit motifs suggests it could reflect a soft winner-take-all gating of information having high degree of uncertainty. Together, these findings elucidate an electrophysiologically-characterized interneuron subclass in the primate, that forms gamma synchronous networks in two different areas when resolving uncertainty during adaptive goal-directed behavior.

neuroscience↗

bioRxiv2019

Cell-type Specific Learning of Attentional Gating in Primate Striatum

Cognitive flexibility depends on a fast neural learning mechanism for enhancing momentary relevant over irrelevant information. A possible neural mechanism realizing this enhancement uses fast-spiking interneurons (FSIs) in the striatum to train striatal projection neurons to gate relevant and suppress distracting cortical inputs. We found support for such a mechanism in nonhuman primates during the flexible adjustment of visual attention. FSIs gated visual attention cues during feature-based learning. One FSI population showed stronger inhibition during learning, while another FSI subpopulation showed weaker inhibition after learning signifying post-learning disinhibition. Additionally, a smaller neural subpopulation increased activity when salient distractor events were successfully suppressed. These findings highlight that fast behavioral learning of feature relevance is accompanied by fast neural learning of cell-type specific cortico-striatal gating.

neuroscience↗

bioRxiv2019

Adaptive Spike-Artifact Removal from Local Field Potentials Uncovers Prominent Beta and Gamma Band Neuronal Synchronization

BackgroundMany neurons synchronize their action potentials to the phase of local field potential (LFP) fluctuations in one or more frequency bands. Analyzing this spike-to-LFP synchronization is challenging, however, when neural spikes and LFP are generated in the same local circuit, because the spikes action potential waveform leak into the LFP and distort phase synchrony estimates. Existing approaches to address this spike bleed-through artifact relied on removing the average action potential waveforms of neurons, but this leaves artifacts in the LFP and distorts synchrony estimates.\n\nNew MethodWe describe a spike-removal method that surpasses these limitations by decomposing individual action potentials into their frequency components before their removal from the LFP. The adaptively estimated frequency components allow for variable spread, strength and temporal variation of the spike artifact.\n\nResultsThis adaptive approach effectively removes spike bleed-through artifacts in synthetic data with known ground truth, and in single neuron and LFP recordings in nonhuman primate striatum. For a large population of neurons with both narrow and broad action potential waveforms, the use of adaptive artifact removal uncovered 20-35 Hz beta and 35-45 Hz gamma band spike-LFP synchronization that would have remained contaminated otherwise.\n\nComparison with Existing MethodsWe demonstrate that adaptive spike-artifact removal cleans LFP data that remained contaminated when applying existing Bayesian and non-Bayesian methods of average spike-artifact removal.\n\nConclusionsApplying adaptive spike-removal from field potentials allows to estimate the phase at which neurons synchronize and the consistency of their phase-locked firing for both beta and low gamma frequencies. These metrics may prove essential to understand cell-to-circuit neuronal interactions in multiple brain systems.

neuroscience↗