Cholinergic Neuromodulation of Prefrontal Attractor Dynamics Controls Performance in Spatial Working Memory

被引:1
作者
Mahrach, Alexandre [1 ]
Bestue, David [1 ]
Qi, Xue-Lian [2 ]
Constantinidis, Christos [3 ]
Compte, Albert [1 ]
机构
[1] Inst Invest Biomed August Pi i Sunyer IDIBAPS, Barcelona 08036, Spain
[2] Wake Forest Sch Med, Winston Salem, NC 27157 USA
[3] Vanderbilt Univ, Nashville, TN 37240 USA
基金
美国国家科学基金会; 美国国家卫生研究院;
关键词
acetylcholine; attractor; neural network; neural tuning; working memory; PERSISTENT ACTIVITY; MODULATION; RECEPTORS; NETWORK; CORTEX; ACETYLCHOLINE; MECHANISMS; NEURONS; MODEL; REPRESENTATION;
D O I
10.1523/JNEUROSCI.1225-23.2024
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
The behavioral and neural effects of the endogenous release of acetylcholine following stimulation of the nucleus basalis (NB) of Meynert have been recently examined in two male monkeys (Qi et al., 2021). Counterintuitively, NB stimulation enhanced behavioral performance while broadening neural tuning in the prefrontal cortex (PFC). The mechanism by which a weaker mnemonic neural code could lead to better performance remains unclear. Here, we show that increased neural excitability in a simple continuous bump attractor model can induce broader neural tuning and decrease bump diffusion, provided neural rates are saturated. Increased memory precision in the model overrides memory accuracy, improving overall task performance. Moreover, we show that bump attractor dynamics can account for the nonuniform impact of neuromodulation on distractibility, depending on distractor distance from the target. Finally, we delve into the conditions under which bump attractor tuning and diffusion balance in biologically plausible heterogeneous network models. In these discrete bump attractor networks, we show that reducing spatial correlations or enhancing excitatory transmission can improve memory precision. Altogether, we provide a mechanistic understanding of how cholinergic neuromodulation controls spatial working memory through perturbed attractor dynamics in the PFC.
引用
收藏
页数:14
相关论文
共 82 条
[71]   Inverted-U dopamine D1 receptor actions on prefrontal neurons engaged in working memory [J].
Vijayraghavan, Susheel ;
Wang, Min ;
Birnbaum, Shari G. ;
Williams, Graham V. ;
Arnsten, Amy F. T. .
NATURE NEUROSCIENCE, 2007, 10 (03) :376-384
[72]   Muscarinic M1 Receptor Overstimulation Disrupts Working Memory Activity for Rules in Primate Prefrontal Cortex [J].
Vijayraghavan, Susheel ;
Major, Alex James ;
Everling, Stefan .
NEURON, 2018, 98 (06) :1256-+
[73]   MODULATION OF MEMORY FIELDS BY DOPAMINE D1 RECEPTORS IN PREFRONTAL CORTEX [J].
WILLIAMS, GV ;
GOLDMANRAKIC, PS .
NATURE, 1995, 376 (6541) :572-575
[74]   EXCITATORY AND INHIBITORY INTERACTIONS IN LOCALIZED POPULATIONS OF MODEL NEURONS [J].
WILSON, HR ;
COWAN, JD .
BIOPHYSICAL JOURNAL, 1972, 12 (01) :1-&
[75]   Bump attractor dynamics in prefrontal cortex explains behavioral precision in spatial working memory [J].
Wimmer, Klaus ;
Nykamp, Duane Q. ;
Constantinidis, Christos ;
Compte, Albert .
NATURE NEUROSCIENCE, 2014, 17 (03) :431-439
[76]   TRPC Channels Mediate a Muscarinic Receptor-Induced Afterdepolarization in Cerebral Cortex [J].
Yan, Hai-Dun ;
Villalobos, Claudio ;
Andrade, Rodrigo .
JOURNAL OF NEUROSCIENCE, 2009, 29 (32) :10038-10046
[77]   The effect of perceptual learning on neuronal responses in monkey visual area V4 [J].
Yang, TM ;
Maunsell, JHR .
JOURNAL OF NEUROSCIENCE, 2004, 24 (07) :1617-1626
[78]   Nicotinic α7 receptors enhance NMDA cognitive circuits in dorsolateral prefrontal cortex [J].
Yang, Yang ;
Paspalas, Constantinos D. ;
Jin, Lu E. ;
Picciotto, Marina R. ;
Arnsten, Amy F. T. ;
Wang, Min .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2013, 110 (29) :12078-12083
[79]  
Zhang K, 1996, J NEUROSCI, V16, P2112
[80]   Neuronal tuning: To sharpen or broaden? [J].
Zhang, KC ;
Sejnowski, TJ .
NEURAL COMPUTATION, 1999, 11 (01) :75-84